Роль микробиоты кишечника в патогенезе рассеянного склероза. Часть 3. Кишечная микробиота как потенциальный триггер рассеянного склероза

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Аннотация

В предыдущей части обзора была рассмотрена роль кишечной микробиоты как фактора предрасположенности к рассеянному склерозу. В представленной части обзора приведены факты, которые подтверждают триггерную роль кишечной микробиоты. Основное внимание уделено начальным этапам патогенеза, которые, согласно современной концепции рассеянного склероза, происходят в кишечнике.

Об авторах

Ирина Николаевна Абдурасулова

Институт экспериментальной медицины

Автор, ответственный за переписку.
Email: i_abdurasulova@mail.ru
ORCID iD: 0000-0003-1010-6768
SPIN-код: 5019-3940

канд. биол. наук, заведующая физиологическим отделом им. И.П. Павлова

Россия, Санкт-Петербург

Список литературы

  1. De Luca F., Shoenfeld Y. The microbiome in autoimmune diseases // Clin Exp Immunol. 2019. Vol. 195, N 1. P. 74–85. doi: 10.1111/cei.13158
  2. Berer K., Mues M., Koutrolos M. et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination // Nature. 2011. Vol. 479, N 7374. P. 538–541. doi: 10.1038/nature10554
  3. Абдурасулова И.Н. Роль микробиоты кишечника в патогенезе рассеянного склероза. Часть 1. Клинические и экспериментальные доказательства вовлечения микробиоты кишечника в развитие рассеянного склероза // Медицинский академический журнал. 2022. Т. 22, № 2. С. 9–36. EDN: BZXZDJ doi: 10.17816/MAJ108241
  4. Абдурасулова И.Н., Клименко В.М. Гетерогенность механизмов повреждения нервных клеток при демиелинизирующих аутоиммунных заболеваниях ЦНС // Российский физиологический журнал им. И.М. Сеченова. 2010. Т. 96, № 1. С. 50–68. EDN: OJGJUV
  5. Dendrou C.A., Lars F., Friese M.A. Immunopathology of multiple sclerosis // Nat Rev Immunol. 2015. Vol. 15, N 9. P. 545–558. doi: 10.1038/nri3871
  6. Bornstein M.B., Appel S.H. Tissue culture studies of demyelination // Ann NY Acad Sci. 1965. Vol. 122. P. 280–286. doi: 10.1111/j.1749-6632.1965.tb20212.x
  7. Lucchinetti C., Brück W., Parisi J., et al. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination // Ann Neurol. 2000. Vol. 47, N 6. P. 707–717. doi: 10.1002/1531-8249(200006)47:6<707::aid-ana3>3.0.co;2-q
  8. Linington C., Bradl M., Lassmann H., et al. Augmentation of demyelination in rat acute allergic encephalomyelitis by circulating mouse monoclonal antibodies directed against a myelin ⁄ oligodendrocytes glycoprotein // Am J Pathol. 1988. Vol. 130, N 3. P. 443–454.
  9. Litzenburger T., Fässler R., Bauer J., et al. B lymphocytes producing demyelinating autoantibodies: development and function in gene-targeted transgenic mice // J Exp Med. 1998. Vol. 188, N 1. P. 169–180. doi: 10.1084/jem.188.1.169
  10. Marrodan M., Alessandro L., Farez M.F., Correale J. The role of infections in multiple sclerosis // Mult Scler. 2019. Vol. 25, N 7. P. 891–901. doi: 10.1177/1352458518823940
  11. Sintzel M.B., Rametta M., Reder A.T. Vitamin D and multiple sclerosis: A comprehensive review // Neurol Ther. 2018. Vol. 7, N 1. P. 59–85. doi: 10.1007/s40120-017-0086-4
  12. Artemiadis A.K., Anagnostouli M.C., Alexopoulos E.C. Stress as a risk factor for multiple sclerosis onset or relaps: a systematic rewiew // Neuroepidemiology. 2011. Vol. 36, N 2. P. 109–120. doi: 10.1159/000323953
  13. Stoiloudis P., Kesidou E., Bakirtzis C., et al. The role of diet and interventions on multiple sclerosis: a review // Nutrients. 2022. Vol. 14, N 6. P. 1150. doi: 10.3390/nu14061150
  14. Mirza A., Mao-Draayer Y. The gut microbiome and microbial translocation in multiple sclerosis // Clin Immunol. 2017. Vol. 183. P. 213–224. doi: 10.1016/j.clim.2017.03.001
  15. Petersen C., Round J.L. Defining dysbiosis and its influence on host immunity and disease // Cell Microbiol. 2014. Vol. 16, N 7. P. 1024–1033. doi: 10.1111/cmi.12308
  16. Gandy K.A.O., Zhang J., Nagarkatti P., Nagarkatti M. The role of gut microbiota in shaping the relapse-remitting and chronic-progressive forms of multiple sclerosis in mouse models // Sci Rep. 2019. Vol. 9, N 1. P. 6923. doi: 10.1038/s41598-019-43356-7
  17. Абдурасулова И.Н. Роль микробиоты кишечника в патогенезе рассеянного склероза. Часть 2. Кишечная микробиота как фактор предрасположенности к развитию рассеянного склероза // Медицинский академический журнал. 2023. Т. 23, № 1. С. 5–40. EDN: ACUJDK doi: 10.17816/MAJ115019
  18. Martin C.R., Osadchiy V., Kalani A., Mayer E.A. The brain-gut-microbiome axis // Cell Mol Gastroenterol Hepatol. 2018. Vol. 6, N 2. P. 133–148. doi: 10.1016/j.jcmgh.2018.04.003
  19. Mikulková Z., Praksová P., Stourac P., et al. Imbalance in T-cell and cytokine profiles in patients with relapsing-remitting multiple sclerosis // J Neurol Sci. 2011. Vol. 300, N 1–2. P. 135–141. doi: 10.1016/j.jns.2010.08.053
  20. Moser A.M., Spindelboeck W., Strohmaier H., et al. Mucosal biopsy shows immunologic changes of the colon in patients with early MS // Neurol Neuroimmunol Neuroinflamm. 2017. Vol. 4, N 4. P. e362. doi: 10.1212/NXI.0000000000000362
  21. Stanisavljević S., Lukić J., Soković S., et al. Correlation of gut microbiota composition with resistance to experimental autoimmune encephalomyelitis in rats // Front Microbiol. 2016. Vol. 7. P. 2005. doi: 10.3389/fmicb.2016.02005
  22. Stanisavljević S., Dinić M., Jevtić B., et al. Gut microbiota confers resistance of Albino Oxford rats to the induction of experimental autoimmune encephalomyelitis // Front Immunol. 2018. Vol. 9. P. 942. doi: 10.3389/fimmu.2018.00942
  23. Cosorich I., Dalla-Costa G., Sorini C., et al. High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis // Sci Adv. 2017. Vol. 3, N 7. P. e1700492. doi: 10.1126/sciadv.1700492
  24. Абдурасулова И.Н., Тарасова Е.А., Мацулевич А.В. и др. Изменение качественного и количественного состава кишечной микробиоты у крыс в течение экспериментального аллергического энцефаломиелита // Российский физиологический журнал им. И.М. Сеченова. 2015. Т. 101, № 11. С. 1235–1249. EDN: UWPLYH
  25. Lee Y.K., Menezes J.S., Umesaki Y., Mazmanian S.K. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis // Proc Natl Acad Sci USA. 2011. Vol. 108, N Suppl 1. P. 4615–4622. doi: 10.1073/pnas.1000082107
  26. López P., Gueimonde M., Margolles A., Suárez A. Distinct Bifidobacterium strains drive different immune responses in vitro // Int J Food Microbiol. 2010. Vol. 138, N 1–2. P. 157–165. doi: 10.1016/j.ijfoodmicro.2009.12.023
  27. Tan T.G., Sefik E., Geva-Zatorsky N., et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice // Proc Natl Acad Sci USA. 2016. Vol. 113, N 50. P. E8141–E81150. doi: 10.1073/pnas.1617460113
  28. Абдурасулова И.Н., Тарасова Е.А., Мацулевич А.В. и др. Влияние бифидобактерий в составе кишечной микробиоты на течение рассеянного склероза // Проблемы медицинской микологии. 2022. Т. 24, № 2. С. 38. EDN: EAEXJJ
  29. Alexander M., Ang Q.Y., Nayak R.R., et al. Human gut bacterial metabolism drives Th17 activation and colitis // Cell Host Microbe. 2022. Vol. 30, N 1. P. 17–30. doi: 10.1016/j.chom.2021.11.001
  30. Bacher P., Hohnstein T., Beerbaum E., et al. Human fnti-fungal Th17 immunity and pathology rely on cross-reactivity against Candida albicans // Cell. 2019. Vol. 176, N 6. P. 1340–1355.e15. doi: 10.1016/j.cell.2019.01.041
  31. Bartsch P., Kilian C., Hellmig M., et al. Th17 cell plasticity towards a T-bet-dependent Th1 phenotype is required for bacterial control in Staphylococcus aureus infection // PLoS Pathog. 2022. Vol. 18, N 4. P. e1010430. doi: 10.1371/journal.ppat.1010430
  32. Miyake S., Kim S., Suda W., et al. Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to Clostridia XIVa and IV cluster // PLoS One. 2015. Vol. 10, N 9. P. e0137429. doi: 10.1371/journal.pone.0137429
  33. Forbes J.D., Chen C.-Y., Knox N.C., et al. A comparative study of the gut microbiota in immune-mediated inflammatory diseases – does a common dysbiosis exist? // Microbiome. 2018. Vol. 6, N 1. P. 221. doi: 10.1186/s40168-018-0603-4
  34. Chen J., Chia N., Kalari K.R., et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls // Sci Rep. 2016. Vol. 6. P. 28484. doi: 10.1038/srep28484
  35. Cekanaviciute E., Yoo B.B., Runia T.F., et al. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models // Proc Natl Acad Sci USA. 2017. Vol. 114, N 40. P. 10713–10718. doi: 10.1073/pnas.1711235114
  36. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E., et al. Central nervous system demyelinating disease protection by the human commensal Bacteroides fragilis dependson polysaccharide A expression // J Immunol. 2010. Vol. 185, N 7. P. 4101–4108. doi: 10.4049/jimmunol.1001443
  37. Tremlett H., Fadrosh D., Faruqi A.A., et al. Gut microbiome in early pediatric multiple sclerosis: a case-control study // Eur J Neurol. 2016. Vol. 23, N 8. P. 1308–1321. doi: 10.1111/ene.13026
  38. Swidsinski A., Dörffel Y., Loening-Baucke V., et al. Reduced mass and diversity of the colonic microbiome in patients with multiple sclerosis and their improvement with ketogenic diet // Front Microbiol. 2017. Vol. 8. P. 1141. doi: 10.3389/fmicb.2017.01141
  39. Mangalam A., Shahi S.K., Luckey D., et al. Human gut-derived commensal bacteria suppress CNS inflammatory and demyelinating disease // Cell Rep. 2017. Vol. 20, N 6. P. 1269–1277. doi: 10.1016/j.celrep.2017.07.031
  40. Абдурасулова И.Н., Тарасова Е.А., Кудрявцев И.В., и др. Состав микробиоты кишечника и популяций циркулирующих Тh-клеток у пациентов с рассеянным склерозом // Инфекция и иммунитет. 2019. Т. 9, № 3. С. 504–522. EDN: GYYNNL doi: 10.15789/2220-7619-2019-3-4-504-522
  41. Yamashita M., Ukibe K., Matsubara Y., et al. Lactobacillus helveticus SBT2171 attenuates experimental autoimmune encephalomyelitis in mice // Front Microbiol. 2018. Vol. 8. P. 2596. doi: 10.3389/fmicb.2017.02596
  42. Lavasani S., Dzhambazov B., Nouri M., et al. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells // PLoS One. 2010. Vol. 5, N 2. P. e9009. doi: 10.1371/journal.pone.0009009
  43. Kadowaki A., Saga R., Lin Y., et al. Gut microbiota-dependent CCR9+ CD4+ T cells are altered in secondary progressive multiple sclerosis // Brain. 2019. Vol. 142, N 4. P. 916–931. doi: 10.1093/brain/awz012
  44. Hemmer B., Fleckenstein B.T., Vergelli M., et al. Identification of high potency microbial and self ligands for a human autoreactive class II–restricted T cell clone // J Exp Med. 1997. Vol. 185, N 9. P. 1651–1660. doi: 10.1084/jem.185.9.1651
  45. Westall F.C. Molecular mimicry revisited: gut bacteria and multiple sclerosis // J Clin Microbiol. 2006. Vol. 44, N 6. P. 2099–2104. doi: 10.1128/JCM.02532-05
  46. Zeng Q., Gong J., Liu X., et al. Gut dysbiosis and lack of short chain fatty acids in a Chinese cohort of patients with multiple sclerosis // Neurochem Int. 2019. Vol. 129. P. 104468. doi: 10.1016/j.neuint.2019.104468
  47. Hughes L.E., Smith P.A., Bonell S., et al. Cross-reactivity between related sequences found in Acinetobacter sp., Pseudomonas aeruginosa, myelin basic protein and myelin oligodendrocyte glycoprotein in multiple sclerosis // J Neuroimmunol. 2003. Vol. 144, N 1–2. P. 105–115. doi: 10.1016/s0165-5728(03)00274-1
  48. Ebringer A., Rashid T., Wilson C. The role of Acinetobacter in the pathogenesis of multiple sclerosis examined by using Popper sequences // Med Hypotheses. 2012. Vol. 78, N 6. P. 763–769. doi: 10.1016/j.mehy.2012.02.026
  49. Yadav S.K., Ito N., Mindur J.E., et al. Fecal Lcn-2 level is a sensitive biological indicator for gut dysbiosis and intestinal inflammation in multiple sclerosis // Front Immunol. 2022. Vol. 13. P. 1015372. doi: 10.3389/fimmu.2022.1015372
  50. Szabó T.G., Palotai R., Antal P., et al. Critical role of glycosylation in determining the length and structure of T cell epitopes // Immunol Res. 2009. Vol. 5. P. 4. doi: 10.1186/1745-7580-5-4
  51. Grogan J.L., Kramer A., Nogai A., et al. Cross-reactivity of myelin basic protein-specific T cells with multiple microbial peptides: Experimental autoimmune encephalomyelitis induction in TCR transgenic mice // J Immunol. 1999. Vol. 163, N 7. P. 3764–3770.
  52. Planas R., Santos R., Tomas-Ojer P., et al. GDP-l-fucose synthase is a CD4+ T cell-specific autoantigen in DRB3*02:02 patients with multiple sclerosis // Sci Transl Med. 2018. Vol. 10, N 462. P. eaat4301. doi: 10.1126/scitranslmed.aat4301
  53. Goodyear C.S., Silverman G.J. B cell superantigens: a microbe’s answer to innate-like B cells and natural antibodies // Springer Semin Immunopathol. 2005. Vol. 26, N 4. P. 463–484. doi: 10.1007/s00281-004-0190-2
  54. Stinissen P., Vandevyver C., Raus J., Zhang J. Superantigen reactivity of γδ T cell clones isolated from patients with multiple sclerosis and controls // Cell Immunol. 1995. Vol. 166, N 2. P. 227–235. doi: 10.1006/cimm.1995.9975
  55. Deacy A.M., Gan S.K., Derrick J.P. Superantigen recognition and interactions: Functions, mechanisms and applications // Front Immunol. 2021. Vol. 12. P. 731845. doi: 10.3389/fimmu.2021.731845
  56. Saha D., Cepeda J., Hayden D., Ciment A. Empyema presenting as low extremity weakness // Chest. 2014. Vol. 145, N 3 Suppl. P. 118A. doi: 10.1378/chest.1836709
  57. Sterlin D., Larsen M., Fadlallah J., et al. Perturbed microbiota / immune homeostasis in multiple sclerosis // Neurol Neuroimmunol Neuroinflamm. 2021. Vol. 8, N 4. P. e997. doi: 10.1212/NXI.0000000000000997
  58. Hughes L.E., Bonell S., Natt R.S., et al. Antibody responses to Acinetobacter spp. and Pseudomonas aeruginosa in multiple sclerosis: Prospects for diagnosis using the myelin-Acinetobacter-neurofilament antibody index // Clin Diagn Lab Immunol. 2001. Vol. 8, N 6. P. 1181–1188. doi: 10.1128/CDLI.8.6.1181–1188.2001
  59. Rollenske T., Szijarto V., Lukasiewicz J., et al. Cross-specificity of protective human antibodies against Klebsiella pneumoniae LPS O-antigen // Nat Immunol. 2018. Vol. 19, N 6. P. 617–624. doi: 10.1038/s41590-018-0106-2
  60. Sterlin D., Fadlallah J., Adams O., et al. Human IgA binds a diverse array of commensal bacteria // J Exp Med. 2020. Vol. 217, N 3. P. e20181635. doi: 10.1084/jem.20181635
  61. Banati M., Csecsei P., Koszegi E., et al. Antibody response against gastrointestinal antigens in demyelinating diseases of the central nervous system // Eur J Neurol. 2013. Vol. 20, N 11. P. 1492–1495. doi: 10.1111/ene.12072
  62. Nordenbo A.M., Andersen J.R., Andersen J.T. Disturbances of ano-rectal function in multiple sclerosis // J Neurol. 1996. Vol. 243, N 6. P. 445–451. doi: 10.1007/BF00900497
  63. Wiesel P.H., Norton C., Roy A.J., et al. Gut focused behavioural treatment for constipation and faecal incontinence in MS // J Neurol Neurosurg Psychiatry. 2000. Vol. 69, N 2. P. 240–243. doi: 10.1136/jnnp.69.2.240
  64. Levinthal D.J., Rahman A., Nusrat S., et al. Adding to the burden: gastrointestinal symptoms and syndromes in multiple sclerosis // Mult Scler Int. 2013. Vol. 2013. P. 319201. doi: 10.1155/2013/319201
  65. Preziosi G., Raptis D.A., Raeburn A., et al. Gut dysfunction in patients with multiple sclerosis and the role of spinal cord involvement in the disease // Eur J Gastroenterol Hepatol. 2013. Vol. 25, N 9. P. 1044–1050. doi: 10.1097/MEG.0b013e328361eaf8
  66. Waldron D.J., Horgan P.G., Patel F.R., et al. Multiple sclerosis: assessment of colonic and anorectal function in the presence of faecal incontinence // Dis Colon Rectum. 2014. Vol. 57, N 4. P. 514–521. doi: 10.1097/DCR.0000000000000048
  67. Абдурасулова И.Н., Тарасова Е.А., Ермоленко Е.И. и др. При рассеянном склерозе изменяется качественный и количественный состав микробиоты кишечника // Медицинский академический журнал. 2015. Т. 15, № 3. С. 55–67. EDN: UNEYGH
  68. Абдурасулова И.Н., Тарасова Е.А., Никифорова И.Г. и др. Особенности состава микробиоты кишечника у пациентов с рассеянным склерозом, получающих препараты, изменяющие течение рассеянного склероза // Журнал неврологии и психиатрии им. С.С. Корсакова. 2018. Т. 118, № 8–2. С. 62–69. EDN: YBMCDZ doi: 10.17116/jnevro201811808262
  69. Тарасова Е.А., Людыно В.И. , Мацулевич А.В. и др. Особенности состава микробиоты кишечника у пациентов с рассеянным склерозом, получающих пероральные препараты, изменяющие течение рассеянного склероза // Медицинский академический журнал. 2021. Т. 21, № 4. С. 47–56. EDN: UFKJVO doi: 10.17816/MAJ88595
  70. Khanna L., Zeydan B., Kantarci O.H., Camilleri M. Gastrointestinal motility disorders in patients with multiple sclerosis: A single-center study // Neurogastroenterol Motil. 2022. Vol. 34, N 8. P. e14326. doi: 10.1111/nmo.14326
  71. Ascanelli S., Bombardini C., Chimisso L., et al. Trans-anal irrigation in patients with multiple sclerosis: Efficacy in treating disease-related bowel dysfunctions and impact on the gut microbiota: A monocentric prospective study // Mult Scler J Exp Transl Clin. 2022. Vol. 8, N 3. P. 20552173221109771. doi: 10.1177/20552173221109771
  72. Quesada-Simó A., Garrido-Marín A., Nos P., Gil-Perotín S. Impact of Anti-CD20 therapies on the immune homeostasis of gastrointestinal mucosa and their relationship with de novo intestinal bowel disease in multiple sclerosis: a review // Front Pharmacol. 2023. Vol. 14. P. 1186016. doi: 10.3389/fphar.2023.1186016
  73. Spear E.T., Holt E.A., Joyce E.J., et al. Altered gastrointestinal motility involving autoantibodies in the experimental autoimmune encephalomyelitis model of multiple sclerosis // Neurogastroenterol Motil. 2018. Vol. 30, N 9. P. e13349. doi: 10.1111/nmo.13349
  74. Wunsch M., Jabari S., Voussen B., et al. The enteric nervous system is a potential autoimmune target in multiple sclerosis // Acta Neuropathol. 2017. Vol. 134, N 2. P. 281–295. doi: 10.1007/s00401-017-1742-6
  75. Kosmidou M., Katsanos A.H., Katsanos K.H., et al. Multiple sclerosis and inflammatory bowel diseases: A systematic review and meta-analysis // J Neurol. 2017. Vol. 264, N 2. P. 254–259. doi: 10.1007/s00415-016-8340-8
  76. Rang E.H., Brooke B.N., Hermon-Taylor J. Association of ulcerative colitis with multiple sclerosis // Lancet. 1982. Vol. 2, N 8297. P. 555. doi: 10.1016/s0140-6736(82)90629-8
  77. Sadovnick A.D., Paty D.W., Yannakoulias G. Concurrence of multiple sclerosis and inflammatory bowel disease // N Engl J Med. 1989. Vol. 321, N 11. P. 762–763.
  78. Kimura K., Hunter S.F., Thollander M.S., et al. Concurrence of inflammatory bowel disease and multiple sclerosis // Mayo Clin Proc. 2000. Vol. 75, N 8. P. 802–806. doi: 10.4065/75.8.802
  79. Gupta G., Gelfand J.M., Lewis J.D. Increased risk for demyelinating diseases in patients with inflammatory bowel disease // Gastroenterology. 2005. Vol. 129, N 3. P. 819–826. doi: 10.1053/j.gastro.2005.06.022
  80. Pokorny C.S., Beran R.G., Pokorny M.J. Association between ulcerative colitis and multiple sclerosis // Intern Med. J. 2007. Vol. 37, N 10. P. 721–724. doi: 10.1111/j.1445-5994.2007.01452.x
  81. Marrie R.A., Yu B.N., Leung S., et al. The utility of administrative data for surveillance of comorbidity in multiple sclerosis: a validation study // Neuroepidemiology. 2013. Vol. 40, N 2. P. 85–92. doi: 10.1159/000343188
  82. Yacyshyn B., Meddings J., Sadowski D., Bowen-Yacyshyn M.B. Multiple sclerosis patients have peripheral blood CD45RO+ B cells and increased intestinal permeability // Dig Dis Sci. 1996. Vol. 41, N 12. P. 2493–2498. doi: 10.1007/BF02100148
  83. Fasano A. Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer // Physiol Rev. 2011. Vol. 91, N 1. P. 151–175. doi: 10.1152/physrev.00003.2008
  84. Teixeira B., Bittencourt V.C.B., Ferreira T.B., et al. Low sensitivity to glucocorticoid inhibition of in vitro Th17-related cytokine production in multiple sclerosis patients is related to elevated plasma lipopolysaccharide levels // Clin Immunol. 2013. Vol. 148, N 2. P. 209–218. doi: 10.1016/j.clim.2013.05.012
  85. Buscarinu M.C., Cerasoli B., Annibali V., et al. Altered intestinal permeability in patients with relapsing-remitting multiple sclerosis: A pilot study // Mult Scler. 2017. Vol. 23, N 3. P. 442–446. doi: 10.1177/1352458516652498
  86. Pellizoni F.P., Leite A.Z., Rodrigues N.C., et al. Detection of dysbiosis and increased intestinal permeability in Brazilian patients with relapsing-remitting multiple sclerosis // Int J Environ Res Public Health. 2021. Vol. 18, N 9. P. 4621. doi: 10.3390/ijerph18094621
  87. Sjöström B., Bredberg A., Mandl T., et al. Increased intestinal permeability in primary Sjögren’s syndrome and multiple sclerosis // J Transl Autoimmun. 2021. Vol. 4. P. 100082. doi: 10.1016/j.jtauto.2021.100082
  88. Buscarinu M.C., Romano S., Mechelli R. Intestinal permeability in relapsing-remitting multiple sclerosis // Neurotherapeutics. 2018. Vol. 15, N 1. P. 68–74. doi: 10.1007/s13311-017-0582-3
  89. Olsson A., Gustavsen S., Langkilde A.R., et al. Circulating levels of tight junction proteins in multiple sclerosis: Association with inflammation and disease activity before and after disease modifying therapy // Mult Scler Relat Disord. 2021. Vol. 54. P. 103136. doi: 10.1016/j.msard.2021.103136
  90. Rahman M.T., Ghosh C., Hossain M., et al. IFN-g, IL-17A, or zonulin rapidly increase the permeability of the blood-brain and small intestinal epithelial barriers: relevance for neuroinflammatory diseases // Biochem Biophys Res Commun. 2018. Vol. 507, N 1–2. P. 274–279. doi: 10.1016/j.bbrc.2018.11.021
  91. Camara-Lemarroy C.R., Silva C., Greenfield J., et al. Biomarkers of intestinal barrier function in multiple sclerosis are associated with disease activity // Mult Scler. 2020. Vol. 26, N 11. P. 1340–1350. doi: 10.1177/1352458519863133
  92. Nouri M., Bredberg A., Weström B., Lavasani S. Intestinal barrier dysfunction develops at the onset of experimental autoimmune encephalomyelitis, and can be induced by adoptive transfer of autoreactive T cells // PLoS One. 2014. Vol. 9, N 9. P. e106335. doi: 10.1371/journal.pone.0106335
  93. Secher T., Kassem S., Benamar M., et al. Oral Administration of the probiotic strain Escherichia coli Nissle 1917 reduces susceptibility to neuroinflammation and repairs experimental futoimmune encephalomyelitis-induced intestinal barrier dysfunction // Front Immunol. 2017. Vol. 8. P. 1096. doi: 10.3389/fimmu.2017.01096
  94. Abdurasulova I.N., Matsulevich A.V., Kirik O.V., et al. The protective effect of Enterococcus faecium L-3 in experimental allergic encephalomyelitis in rats is dose-dependent // Nutrafoods. 2019. Vol. 1. P. 1–11. doi: 10.17470/NF-019-0001
  95. Sonoda N., Furuse M., Sasaki H. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier // J Cell Biol. 1999. Vol. 147, N 1. P. 195–204. doi: 10.1083/jcb.147.1.195
  96. Madi A., Svinareff P., Orange N., et al. Pseudomonas fluorescens alters epithelial permeability and translocates across Caco-2/TC7 intestinal cells // Gut Pathog. 2010. Vol. 2, N 1. P. 16. doi: 10.1186/1757-4749-2-16
  97. Wu S., Lim K.C., Huang J., et al. Bacteroides fragilis enterotoxin cleaves the zonula adherens protein, E-cadherin // Proc Natl Acad Sci USA. 1998. Vol. 95, N 25. P. 14979–14984. doi: 10.1073/pnas.95.25.14979
  98. Bates J.M., Akerlund J., Mittge E., Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota // Cell Host Microbe. 2007. Vol. 2, N 6. P. 371–382. doi: 10.1016/j.chom.2007.10.010
  99. Huang Z., Wang J., Xu X., et al. Antibody neutralization of microbiota-derived circulating peptidoglycan dampens inflammation and ameliorates autoimmunity // Nat Microbiol. 2019. Vol. 4, N 5. P. 766–773. doi: 10.1038/s41564-019-0381-1
  100. Jiang W., Lederman M.M., Hunt P., et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection // J Infect Dis. 2009. Vol. 199, N 8. P. 1177–1185. doi: 10.1086/597476
  101. Sandler N.G., Douek D.C. Microbial translocation in HIV infection: causes, consequences and treatment opportunities // Nat Rev Microbiol. 2012. Vol. 10, N 9. P. 655–666. doi: 10.1038/nrmicro2848
  102. Садеков Т.Ш., Бойко А.Н., Омарова М.А. и др. Оценка структуры микробиома человека при рассеянном склерозе по концентрациям микробных маркеров в крови // Клиническая лабораторная диагностика. 2022. Т. 67, № 10. С. 600–606. EDN: TBRRGZ doi: 10.51620/0869-2084-2022-67-10-600-606
  103. Ebringer A., Hughes L., Rashid T., Wilson C. Acinetobacter immune responses in multiple sclerosis: etiopathogenetic role and its possible use as a diagnostic marker // Arch Neurol. 2005. Vol. 62, N 1. P. 33–36. doi: 10.1001/archneur.62.1.33
  104. Benito-Leon J., Pisa D., Alonso R., et al. Association between multiple sclerosis and Candida species: evidence from a case-control study // Eur J Clin Microbiol Infect Dis. 2010. Vol. 29, N 9. P. 1139–1145. doi: 10.1007/s10096-010-0979-y
  105. Braniste V., Al-Asmakh M., Kowal C., et al. The gut microbiota influences blood-brain barrier permeability in mice // Sci Transl Med. 2014. Vol. 6, N 263. P. 263ra158. doi: 10.1126/scitranslmed.3009759
  106. Leech S., Kirk J., Plumb J., McQuaid S. Persistent endothelial abnormalities and blood-brain barrier leak in primary and secondary progressive multiple sclerosis // Neuropathol Appl Neurobiol. 2007. Vol. 33, N 1. P. 86–98. doi: 10.1111/j.1365-2990.2006.00781.x
  107. Alvarez J.I., Cayrol R., Prat A. Disruption of central nervous system barriers in multiple sclerosis // Biochim Biophys Acta. 2011. Vol. 1812, N 2. P. 252–264. doi: 10.1016/j.bbadis.2010.06.017
  108. Bartholomaus I., Kawakami N., Odoardi F., et al. Effector Tcell interactions with meningeal vascular structures in nascent autoimmune CNS lesions // Nature. 2009. Vol. 462, N 7269. P. 94–98. doi: 10.1038/nature08478
  109. Hoyles L., Snelling T., Umlai U.-K., et al. Microbiome-host systems interactions: protective effects of propionate upon the blood-brain barrier // Microbiome. 2018. Vol. 6, N 1. P. 55. doi: 10.1186/s40168-018-0439-y
  110. Melbye P., Olsson A., Hansen T.H., et al. Short-chain fatty acids and gut microbiota in multiple sclerosis // Acta Neurol Scand. 2019. Vol. 139, N 3. P. 208–219. doi: 10.1111/ane.13045
  111. Li Z., Zhang F., Sun M., et al. The modulatory effects of gut microbes and metabolites on blood–brain barrier integrity and brain function in sepsis-associated encephalopathy // Peer J. 2023. Vol. 11. P. e15122. doi: 10.7717/peerj.15122
  112. Hoyles L., Pontifex M.G., Rodriguez-Ramiro I., et al. Regulation of blood-brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide // Microbiome. 2021. Vol. 9, N 1. P. 235. doi: 10.1186/s40168-021-01181-z
  113. Stachulski A.V., Knausenbergrer T.B., Shah S.N., et al. A host-gut microbial co-metabolite of aromatic amino acids, p-cresol glucuronide, promotes blood-brain barrier integrity in vivo // Tissue Barriers. 2023. Vol. 11, N 1. P. 2073175. doi: 10.1080/21688370.2022.2073175
  114. Vallino A., Dos Santos A., Mathé C.V., et al. Gut bacteria Akkermansia elicit a specific IgG response in CSF of patients with MS // Neurol Neuroimmunol Neuroinflamm. 2020. Vol. 7, N 3. P. e688. doi: 10.1212/NXI.0000000000000688
  115. Boussamet L., Montassier E., Soulillou J.-P., Berthelot L. Anti α1-3Gal antibodies and Gal content in gut microbiota in immune disorders and multiple sclerosis // Clin Immunol. 2022. Vol. 235. P. 108693. doi: 10.1016/j.clim.2021.108693
  116. Eckman E., Laman J.D., Fischer K.F., et al. Spinal fluid IgG antibodies from patients with demyelinating diseases bind multiple sclerosis-associated bacteria // J Mol Med (Berl). 2021. Vol. 99, N 10. P. 1399–1411. doi: 10.1007/s00109-021-02085-z
  117. Aasjord P., Nyland H., Haaheim L.R. Intrathecal synthesis of antibodies to staphylococcal antigens in multiple sclerosis patients // Acta Pathol Microbiol Immunol Scand. C. 1986. Vol. 94, N 3. P. 97–103. doi: 10.1111/j.1699-0463.1986.tb02097.x
  118. Бойко А.Н., Мельников М.В., Бойко О.В. и др. Исследование содержания маркеров микробиоты в цереброспинальной жидкости пациентов с рассеянным склерозом и радиологически изолированным синдромом // Неврология, нейропсихиатрия, психосоматика. 2021. Т. 13, № S1. С. 27–30. EDN: ORSJHL doi: 10.14412/2074-2711-2021-1S-27-30
  119. Pisa D., Alonso R., Jimenez-Jimenez F.J., Carrasco L. Fungal infection in cerebrospinal fluid from some patients with multiple sclerosis // Eur J Clin Microbiol Infect. Dis. 2013. Vol. 32, N 6. P. 795–801. doi: 10.1007/s10096-012-1810-8
  120. Schrijver I.A., van Meurs M., Melief M.J. Bacterial peptidoglycan and immune reactivity in central nervous system in multiple sclerosis // Brain. 2001. Vol. 124, N Pt 8. P. 1544–1554. doi: 10.1093/brain/124.8.1544
  121. Visser L., Melief M.-J., van Riel D., et al. Phagocytes containing a disease-promoting Toll-like receptor/Nod ligand are present in the brain during demyelinating disease in primates // Am J Pathol. 2006. Vol. 169, N 5. P. 1671–1685. doi: 10.2353/ajpath.2006.060143
  122. Branton W.G., Lu J.Q., Surette M.G., et al. Brain microbiota disruption within inflammatory demyelinating lesions in multiple sclerosis // Sci Rep. 2016. Vol. 6. P. 37344. doi: 10.1038/srep37344
  123. Kriesel J.D., Bhetariya P., Wang Z.M., et al. Spectrum of microbial sequences and a bacterial cell wall antigen in primary demyelination brain specimens obtained from living patients // Sci Rep. 2019. Vol. 9, N 1. P. 1387. doi: 10.1038/s41598-018-38198-8
  124. Alonso R., Fernández-Fernández A.M., Pisa D., Carrasco L. Multiple sclerosis and mixed microbial infections. Direct identification of fungi and bacteria in nervous tissue // Neurobiol Dis. 2018. Vol. 117. P. 42–61. doi: 10.1016/j.nbd.2018.05.022
  125. Pröbstel A.-K., Zhou X., Baumann R., et al. Gut microbiota-specific IgA+ B cells traffic to the CNS in active multiple sclerosis // Sci Immunol. 2020. Vol. 5, N 53. P. eabc7191. doi: 10.1126/sciimmunol.abc7191
  126. Kim K.S. Mechanisms of microbial traversal of the blood-brain barrier // Nat Rev Microbiol. 2008. Vol. 6, N 8. P. 625–634. doi: 10.1038/nrmicro1952
  127. Erny D., Hrabě de Angelis A.L., Jaitin D., et al. Host microbiota constantly control maturation and function of microglia in the CNS // Nat Neurosci. 2015. Vol. 18, N 7. P. 965–977. doi: 10.1038/nn.4030
  128. Luczynsci P., Whelan S.O., O’Sullivan C., et al. Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdale and hippocampus // Eur J Neurosci. 2016. Vol. 44. P. 2654–2666. doi: 10.1111/ejn.13291
  129. Heijtz R.D., Wang S., Anuar F., Petterson S. Normal gut microbiota modulates brain developmant and behavior // Proc Natl Acad Sci USA. 2011. Vol. 108, N 7. P. 3047–3052. doi: 10.1073/pnas.1010529108
  130. Lu J., Lu L., Yu Y., et al. Effects of Intestinal microbiota on brain development in humanized gnotobiotic mice // Sci Rep. 2018. Vol. 8, N 1. P. 5443. doi: 10.1038/s41598-018-23692-w
  131. Luo C., Jian C., Liao Y., et al. The role of microglia in multiple sclerosis // Neuropsychiatr Dis Treat. 2017. Vol. 13. P. 1661–1667. doi: 10.2147/NDT.S140634
  132. Vogel D.Y.S., Vereyken E.J.F., Glim J.E., et al. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status // J Neuroinflammation. 2013. Vol. 10. P. 35. doi: 10.1186/1742-2094-10-35
  133. Heppner F.L., Greter M., Marino D., et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis // Nat Med. 2005. Vol. 11, N 2. P. 146–152. doi: 10.1038/nm1177
  134. Rothhammer V., Mascanfroni I.D., Bunse L., et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor // Nat Med. 2016. Vol. 22, N 6. P. 586–597. doi: 10.1038/nm.4106
  135. Zelante T., Iannotti R.G., Cunha C., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22 // Immunity. 2013. Vol. 39, N 2. P. 372–385. doi: 10.1016/j.immuni.2013.08.003
  136. Li G., Young K.D. Indole production by the tryptophanase TnaA in Escherichia coli is determined by the amount of exogenous tryptophan // Microbiology. 2013. Vol. 159, N Pt 2. P. 402–410. doi: 10.1099/mic.0.064139-0
  137. Devlin A.S., Marcobal A., Dodd D., et al. Modulation of a circulating uremic solute via rational genetic manipulation of the gut microbiota // Cell Host Microbe. 2016. Vol. 20, N 6. P. 709–715. doi: 10.1016/j.chom.2016.10.021
  138. Shapira L., Ayalon S., Brenner T. Effects of Porphyromonas gingivalis on the central nervous system: Activation of glial cells and exacerbation of experimental autoimmune encephalomyelitis // J Periodontol. 2002. Vol. 73, N 5. P. 511–516. doi: 10.1902/jop.2002.73.5.511
  139. Wang Y., Telesford K.M., Ochoa-Repáraz J., et al. An intestinal commensal symbiosis factor controls neuroinflammation via TLR2-mediated CD39 signalling // Nat Commun. 2014. Vol. 5. P. 4432. doi: 10.1038/ncomms5432
  140. Hoban A.E., Stilling R.M., Ryan F.J., et al. Regulation of prefrontal cortex myelination by the microbiota // Transl Psychiatry. 2016. Vol. 6, N 4. P. e774. doi: 10.1038/tp.2016.42
  141. Kuhlman T., Miron V., Cui Q., et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis // Brain. 2008. Vol. 131, N Pt 7. P. 1749–1758. doi: 10.1093/brain/awn096
  142. Gacias M., Gaspari S., Santos P.M.G., et al. Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior // Elife. 2016. Vol. 5. P. e13442. doi: 10.7554/eLife.13442
  143. Cox L.M., Maghzi A.H., Liu S., et al. The gut microbiome in progressive multiple sclerosis // Ann Neurol. 2021. Vol. 89, N 6. P. 1195–1211. doi: 10.1002/ana.26084
  144. Reynders T., Devolder L., Valles-Colomer M., et al. Gut microbiome variation is associated to multiple sclerosis phenotypic subtypes // Ann Clin Transl Neurol. 2020. Vol. 7, N 4. P. 406–419. doi: 10.1002/acn3.51004
  145. Saito Y., Sato T., Nomoto K., Tsuji H. Identification of phenol- and p-cresol-producing intestinal bacteria by using media supplemented with tyrosine and its metabolites // FEMS Microbiol Ecol. 2018. Vol. 94, N 9. P. fiy125. doi: 10.1093/femsec/fiy125
  146. Rumah K.R., Linden J., Fischetti V.A., Vartanian T. Isolation of Clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease // PLoS One. 2013. Vol. 8, N 10. P. e76359. doi: 10.1371/journal.pone.0076359
  147. Cekanaviciute E., Pröbstel A.-K., Thomann A., et al. Multiple sclerosis-associated changes in the composition and immune functions of spore-forming bacteria // mSystems. 2018. Vol. 3, N 6. P. e00083–18. doi: 10.1128/mSystems.00083-18
  148. Szmigielski S., Blankenship M., Robinson J.P., Harshman S. Injury of myelin sheaths in isolated rabbit vagus nerves by alpha-toxin of Staphylococcus aureus // Toxicon. 1979. Vol. 17, N 4. P. 363–371. doi: 10.1016/0041-0101(79)90264-2
  149. Uyeda C., Gerstl B., Smith J., Carr W. Anti-staphylococcal β-hemolysin antibodies in humans with neurological disease // Proc Soc Exp Biol Med. 1966. Vol. 123, N 1. P. 143–146. doi: 10.3181/00379727-123-31425
  150. Ntranos A., Park H.J., Wentling M., et al. Bacterial neurotoxic metabolites in multiple sclerosis cerebrospinal fluid and plasma // Brain. 2022. Vol. 145, N 2. P. 569–583. doi: 10.1093/brain/awab320
  151. Schepici G., Silvestro S., Bramanti P., Mazzon E. The gut microbiota in multiple sclerosis: An overview of clinical trials // Cell Transplant. 2019. Vol. 28, N 12. P. 1507–1527. doi: 10.1177/0963689719873890
  152. Yadav S.K., Mindur J.E., Ito K., Dhib-Jalbut S. Advances in the immunopathogenesis of multiple sclerosis // Curr Opin Neurol. 2015. Vol. 28, N 3. P. 206–219. doi: 10.1097/WCO.0000000000000205
  153. Fletcher J.M., Lalor S.J., Sweeney C.M., et al. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis // Clin Exp Immunol. 2010. Vol. 162, N 1. P. 1–11. doi: 10.1111/j.1365-2249.2010.04143.x
  154. Ivanov I.I., Atarashi K., Manel N., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria // Cell. 2009. Vol. 139, N 3. P. 485–498. doi: 10.1016/j.cell.2009.09.033
  155. Legroux L., Arbour N. Multiple sclerosis and T lymphocytes: An entangled story // J Neuroimmune Pharmacol. 2015. Vol. 10, N 4. P. 528–546. doi: 10.1007/s11481-015-9614-0
  156. McGeachy M.J., Chen Y., Tato C.M., et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo // Nat Immunol. 2009. Vol. 10, N 3. P. 314–324. doi: 10.1038/ni.1698
  157. Jadidi-Niaragh F., Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis // Scand J Immunol. 2011. Vol. 74, N 1. P. 1–13. doi: 10.1111/j.1365-3083.2011.02536.x
  158. Vaknin-Dembinsky A., Balashov K., Weiner H.L. IL-23 is increased in dendritic cells in multiple sclerosis and down-regulation of IL-23 by antisense oligos increases dendritic cell IL-10 production // J Immunol. 2006. Vol. 176, N 12. P. 7768–7774. doi: 10.4049/jimmunol.176.12.7768
  159. Berer K., Boziki M., Krishnamoorthy G. Selective accumulation of pro-inflammatory T cells in the intestine contributes to the resistance to autoimmune demyelinating disease // PLoS One. 2014. Vol. 9, N 2. P. e87876. doi: 10.1371/journal.pone.0087876
  160. Kohm A.P., Carpentier P.A., Anger H.A., Miller S.D. Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis // J Immunol. 2002. Vol. 169, N 9. P. 4712–4716. doi: 10.4049/jimmunol.169.9.4712
  161. Абдурасулова И.Н., Клименко В.М. Роль иммунных и глиальных клеток в процессах нейродегенерации // Медицинский академический журнал. 2011. T. 11, № 1. C. 12–29. EDN: TKPSIT
  162. Castillo-Alvarez F., Marzo-Sola M.E. Role of intestinal microbiota in the development of multiple sclerosis // Neurologia. 2017. Vol. 32, N 3. P. 175–184. doi: 10.1016/j.nrl.2015.07.005
  163. Jäger A., Dardalhon V., Sobel R.A., et al. Th1, Th17 and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes // J Immunol. 2009. Vol. 183, N 11. P. 7169–7177. doi: 10.4049/jimmunol.0901906
  164. Kamma E., Lasisi W., Libner C., et al. Central nervous system macrophages in progressive multiple sclerosis: relationship to neurodegeneration and therapeutics // J Neuroinflammation. 2022. Vol. 19. P. 45. doi: 10.1186/s12974-022-02408-y
  165. Gazzinelli-Guimaraes P.H., Nutman T.B. Helminth parasites and immune regulation // F1000Res. 2018. Vol. 7. P. F1000. Faculty Rev-1685. doi: 10.12688/f1000research.15596
  166. Barone M., Mendozzi L., D’Amico F., et al. Influence of a high-impact multidimensional rehabilitation program on the gut microbiota of patients with multiple sclerosis // Int J Mol Sci. 2021. Vol. 22, N 13. P. 7173. doi: 10.3390/ijms22137173
  167. Bitan M., Weiss L., Reibstein I., et al. Influence of a high-impact multidimensional rehabilitation program on the gut microbiota of patients with multiple sclerosis // Mol Immunol. 2010. Vol. 47, N 10. P. 1890–1898. doi: 10.1016/j.molimm.2010.03.014
  168. Badolati I., Sverremark-Ekström E., van der Heiden M. Th9 cells in allergic diseases: A role for the microbiota? // Scand J Immunol. 2020. Vol. 91, N 4. P. e12857. doi: 10.1111/sji.12857
  169. Badolati I., van der Heiden M., Brodin D., et al. Staphylococcus aureus-derived factors promote human Th9 cell polarization and enhance a transcriptional program associated with allergic inflammation // Eur J Immunol. 2023. Vol. 53, N 3. P. e2250083. doi: 10.1002/eji.202250083
  170. Nowak E.C., Weaver C.T., Turner H., et al. IL-9 as a mediator of Th17-driven inflammatory disease // J Exp Med. 2009. Vol. 206, N 8. P. 1653–1660. doi: 10.1084/jem.20090246
  171. Atarashi K., Tanoue T., Ando M., et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells // Cell. 2015. Vol. 163, N 2. P. 367–380. doi: 10.1016/j.cell.2015.08.058
  172. Atarashi K., Nishimura J., Shima T., et al. ATP drives lamina propria T(H)17 cell differentiation // Nature. 2008. Vol. 455, N 7214. P. 808–812. doi: 10.1038/nature07240
  173. Becattini S., Becattini S., Latorre D., et al. Functional heterogeneity of human memory CD4+ T cell clones primed by pathogens or vaccines // Science. 2015. Vol. 347, N 6220. P. 400–406. doi: 10.1126/science.1260668
  174. Zielinski C.E., Mele F., Aschenbrenner D., et al. Pathogen-induced human TH17 cells produce IFN-g or IL-10 and are regulated by IL-1b // Nature. 2012. Vol. 484, N 7395. P. 514–518. doi: 10.1038/nature10957
  175. Tzartos J.S., Friese M.A., Craner M.J., et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis // Am J Pathol. 2008. Vol. 172, N 1. P. 146–155. doi: 10.2353/ajpath.2008.070690
  176. Kebir H., Kreymborg K., Ifergan I., et al. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation // Nat Med. 2007. Vol. 13, N 10. P. 1173–1175. doi: 10.1038/nm1651
  177. Barnes J.L., Plank M.W., Asquith K., et al. T-helper 22 cells develop as a distinct lineage from Th17 cells during bacterial infection and phenotypic stability is regulated by T-bet // Mucosal Immunol. 2021. Vol. 14, N 5. P. 1077–1087. doi: 10.1038/s41385-021-00414-6
  178. Rolla S., Bardina V., De Mercanti S., et al. Th22 cells are expanded in multiple sclerosis and are resistant to IFN-β // J Leukoc Biol. 2014. Vol. 96, N 6. P. 1155–1164. doi: 10.1189/jlb.5A0813-463RR
  179. Xu W., Li R., Dai Y., et al. IL-22 secreting CD4+ T cells in the patients with neuromyelitis optica and multiple sclerosis // J Neuroimmunol. 2013. Vol. 261, N 1–2. P. 87–91. doi: 10.1016/j.jneuroim.2013.04.021
  180. Ansaldo E., Slayden L.C., Ching K.L., et al. Akkermansia muciniphila induces intestinal adaptive immune responses during homeostasis // Science. 2019. Vol. 364, N 6446. P. 1179–1184. doi: 10.1126/science.aaw7479
  181. Takahashi D., Hoshina N., Kabumoto Y., et al. Microbiota-derived butyrate limits the autoimmune response by promoting the differentiation of follicular regulatory T cells // EBioMedicine. 2020. Vol. 58. P. 102913. doi: 10.1016/j.ebiom.2020.102913
  182. Dhaeze T., Peelen E., Hombrouck A., et al. Circulating follicular regulatory T cells are defective in multiple sclerosis // J Immunol. 2015. Vol. 195, N 3. P. 832–840. doi: 10.4049/jimmunol.1500759
  183. Shahi S., Jensen S.N., Murra A.C., et al. Human commensal Prevotella histicola ameliorates disease as effectively as interferone-beta in the experimental autoimmune encephalomyelitis // Front Immunol. 2020. Vol. 11. P. 578648. doi: 10.3389/fimmu.2020.578648
  184. Furusawa Y., Obata Y., Fukuda S., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells // Nature. 2013. Vol. 504, N 7480. P. 446–450. doi: 10.1038/nature12721
  185. Qiu X., Zhang M., Yang X., et al. Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis // J Crohns Colitis. 2013. Vol. 7, N 11. P. e558–568. doi: 10.1016/j.crohns.2013.04.002
  186. Atarashi K., Tanoue T., Shima T., et al. Induction of colonic regulatory T cells by indigenous Clostridium species // Science. 2011. Vol. 331, N 6015. P. 337–341. doi: 10.1126/science.1198469
  187. Vital M., Penton C.R., Wang Q., et al. A gene-targeted approach to investigate the intestinal butyrate-producing bacterial community // Microbiome. 2013. Vol. 1, N 1. P. 8. doi: 10.1186/2049-2618-1-8
  188. Ochoa-Repáraz J., Mielcarz D.W., Wang Y., et al. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease // Mucosal Immunol. 2010. Vol. 3, N 5. P. 487–495. doi: 10.1038/mi.2010.29
  189. Tejon G.P., Manriques V., De Calisto J., et al. Vitamin A impairs the reprogramming of Tregs into IL-17-producing cells during intestinal inflammation // Biomed Res Int. 2015. Vol. 2015. P. 137893. doi: 10.1155/2015/137893
  190. Viglietta V., Baecher-Allan C., Weiner H.L., Hafler D.A. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis // J Exp Med. 2004. Vol. 199, N 7. P. 971–979. doi: 10.1084/jem.20031579
  191. Haas J., Hug A., Viehöver A., et al. Reduced suppressive effect of CD4+CD25high regulatory T cells on the T cell immune response against myelin oligodendrocyte glycoprotein in patients with multiple sclerosis // Eur J Immunol. 2005. Vol. 35, N 11. P. 3343–3352. doi: 10.1002/eji.200526065
  192. Zhang H., Podojil J.R., Chang J., et al. TGF-beta-induced myelin peptide-specific regulatory T cells mediate antigen-specific suppression of induction of experimental autoimmune encephalomyelitis // J Immunol. 2010. Vol. 184, N 12. P. 6629–6636. doi: 10.4049/jimmunol.0904044
  193. Dombrowski Y., O’Hagan T., Dittmer M., et al. Regulatory T cells promote myelin regeneration in the central nervous system // Nat Neurosci. 2017. Vol. 20, N 5. P. 674–680. doi: 10.1038/nn.4528
  194. Takata K., Kinoshita M., Okuno T., et al. The lactic acid bacterium Pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells // PLoS One. 2011. Vol. 6, N 11. P. e27644. doi: 10.1371/journal.pone.0027644
  195. Carrier Y., Yuan J., Kuchroo V.K., Weiner H.L. Th3 cells in peripheral tolerance. I. Induction of Foxp3-positive regulatory T cells by Th3 cells derived from TGF-beta T cell-transgenic mice // J Immunol. 2007. Vol. 178, N 1. P. 179–185. doi: 10.4049/jimmunol.178.1.179
  196. Abdurasulova I.N., Matsulevich A.V., Tarasova E.A., et al. Enterococcus faecium L3 and glatiramer acetate ameliorate of experimental allergic encephalomyelitis (EAE) in rats by affecting different populations of immune cells // Benef Microbes. 2016. Vol. 7, N 5. P. 719–729. doi: 10.3920/BM2016.0018
  197. Brucklacher-Waldert V., Carr E.J., Linterman M.A., Veldhoen M. Cellular plasticity of CD4T cells in the intestine // Front Immunol. 2014. Vol. 5. P. 488. doi: 10.3389/fimmu.2014.00488
  198. Maceiras A.R., Fonseca V.R., Agua-Doce A., Graca L. T follicular regulatory cells in mice and men // Immunology. 2017. Vol. 152, N 1. P. 23–35. doi: 10.1111/imm.12774
  199. Воронина Е.В., Талаев В.Ю. Созревание фолликулярных Т-хелперов // Иммунология. 2018. Т. 39, № 4. C. 230–238. EDN: SCTFLO doi: 18821/0206-4952-2018-39-4-230-238
  200. Maynard C.L., Elson C.O., Hatton R.D., Weaver C.T. Reciprocal interactions of the intestinal microbiota and immune system // Nature. 2012. Vol. 489, N 7415. P. 231–241. doi: 10.1038/nature11551
  201. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut // Nat Rev Immunol. 2008. Vol. 8, N 6. P. 411–420. doi: 10.1038/nri2316
  202. Correa-Oliveira R., Fachi J.L., Vieira A., et al. Regulation of immune cell function by short-chain fatty acids // Clin Transl Immunol. 2016. Vol. 5, N 4. P. e73. doi: 10.1038/cti.2016.17
  203. Honda K., Littman D.R. The microbiota in adaptive immune homeostasis and disease // Nature. 2016. Vol. 535, N 7610. P. 75–84. doi: 10.1038/nature18848
  204. Walker A.W., Sanderson J.D., Churcher C., et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease // BMC Microbiol. 2011. Vol. 11. P. 7. doi: 10.1186/1471-2180-11-7
  205. den Besten G., van Eunen K., Groen A.K., et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism // J Lipid Res. 2013. Vol. 54, N 9. P. 2325–2340. doi: 10.1194/jlr.R036012
  206. Hugenholtz F., Mullaney J.A., Kleerebezem M., et al. Modulation of the microbial fermentation in the gut by fermentable carbohydrates // Bioactive Carbohydr Dietary Fibre. 2013. Vol. 2, N 2. P. 133–142. doi: 10.1016/j.bcdf.2013.09.008
  207. Louis P., Flint H.J. Formation of propionate and butyrate by the human colonic microbiota // Environ Microbiol. 2017. Vol. 19, N 1. P. 29–41. doi: 10.1111/1462-2920.13589
  208. Venegas D.P., De la Fuente M.K., Landskron G. Short chain fatty acids (SCFAs)mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases // Front Immunol. 2019. Vol. 10. P. 277. doi: 10.3389/fimmu.2019.00277
  209. Morrison D.J., Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism // Gut Microbes. 2016. Vol. 7, N 3. P. 189–200. doi: 10.1080/19490976.2015.1134082
  210. Anand S., Kaur H., Mande S.S. Comparative in silico analysis of butyrate production pathways in gut commensals and pathogens // Front Microbiol. 2016. Vol. 7. P. 1945. doi: 10.3389/fmicb.2016.01945
  211. Vital M., Howe A.C., Tiedje J.M. Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data // mBio. 2014. Vol. 5, N 2. P. e00889. doi: 10.1128/mBio.00889-14
  212. Arpaia N., Campbell C., Fan X., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation // Nature. 2013. Vol. 504, N 7480. P. 451–455. doi: 10.1038/nature12726
  213. Park J., Wang Q., Wu Q., et al. Bidirectional regulatory potentials of short-chain fatty acids and their G-protein-coupled receptors in autoimmune neuroinflammation // Sci Rep. 2019. Vol. 9, N 1. P. 8837. doi: 10.1038/s41598-019-45311-y
  214. Duscha A., Gisevius B., Hirschberg S., et al. Propionic acid shapes the multiple sclerosis disease course by an immunomodulatory mechanism // Cell. 2020. Vol. 180, N 6. P. 1067–1080.e16. doi: 10.1016/j.cell.2020.02.035
  215. Saresella M., Marventano I., Barone M., et al. Alterations in circulating fatty acid are associated with gut microbiota dysbiosis and inflammation in multiple sclerosis // Front Immunol. 2020. Vol. 11. P. 1390. doi: 10.3389/fimmu.2020.01390
  216. Takewaki D., Suda W., Sato W., et al. Alterations of the gut ecological and functional microenvironment in different stages of multiple sclerosis // Proc Natl Acad Sci USA. 2020. Vol. 117, N 36. P. 22402–22412. doi: 10.1073/pnas.2011703117
  217. Van den Abbeele P., Belzer C., Goossens M., et al. Butyrate-producing Clostridium cluster XIVa species specifically colonize mucins in an in vitro gut model // ISME J. 2013. Vol. 7, N 5. P. 949–961. doi: 10.1038/ismej.2012.158
  218. Kim C.H., Park J., Kim M. Gut microbiota-derived short-chain fatty acids, T cells, and inflammation // Immune Netw. 2014. Vol. 14, N 6. P. 277–288. doi: 10.4110/in.2014.14.6.277
  219. Round J.L., Mazmanian S.K. Inducible Foxp3+ regulatory Tcell development by a commensal bacterium of the intestinal microbiota // Proc Natl Acad Sci USA. 2010. Vol. 107, N 27. P. 12204–12209. doi: 10.1073/pnas.0909122107
  220. Olsson A., Gustavsen S., Nguyen T.D., et al. Serum short-chain fatty acids and associations with inflammation in newly diagnosed patients with multiple sclerosis and healthy controls // Front Immunol. 2021. Vol. 12. P. 661493. doi: 10.3389/fimmu.2021.661493
  221. Trend S., Leffler J., Jones A.P., et al. Associations of serum short-chain fatty acids with circulating immune cells and serum biomarkers in patients with multiple sclerosis // Sci Rep. 2021. Vol. 11, N 1. P. 5244. doi: 10.1038/s41598-021-84881-8
  222. Becker A., Abuazab M., Schwiertz A., et al. Short-chain fatty acids and intestinal inflammation in multiple sclerosis: modulation of female susceptibility by microbial products? // Auto Immun Highlights. 2021. Vol. 12, N 1. P. 7. doi: 10.1186/s13317-021-00149-1
  223. Viglietta V., Baecher-Allan C., Weiner H.L., Hafler D.A. Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis // J Exp Med. 2004. Vol. 199, N 7. P. 971–979. doi: 10.1084/jem.20031579
  224. Haas J., Fritzsching B., Trübswetter P., et al. Prevalence of newly generated naive regulatory T cells (Treg) is critical for Treg suppressive function and determines Treg dysfunction in multiple sclerosis // J Immunol. 2007. Vol. 179, N 2. P. 1322–1330. doi: 10.4049/jimmunol.179.2.1322
  225. Venken K., Hellings N., Liblau R., Stinissen P. Disturbed regulatory T cell homeostasis in multiple sclerosis // Trends Mol Med. 2010. Vol. 16, N 2. P. 58–68. doi: 10.1016/j.molmed.2009.12.003
  226. Roager H.M., Licht T.R. Microbial tryptophan catabolites in health and disease // Nat Commun. 2018. Vol. 9. P. 3294. doi: 10.1038/s41467-018-05470-4
  227. Singh N.P., Singh U.P., Rouse M., et al. Dietary indoles suppress delayed-type hypersensitivity by inducing a switch from proinflammatory Th17 cells to anti-inflammatory regulatory T cells through regulation of micro-RNA // J Immunol. 2016. Vol. 196, N 3. P. 1108–1122. doi: 10.4049/jimmunol.1501727
  228. Beischlag T.V., Luis Morales J., Hollingshead B.D., Perdew G.H. The aryl hydrocarbon receptor complex and the control of gene expression // Crit Rev Eukaryot Gene Expr. 2008. Vol. 18, N 3. P. 207–250. doi: 10.1615/critreveukargeneexpr.v18.i3.20
  229. Lamas B., Natividad J.M., Sokol H. Aryl hydrocarbon receptor and intestinal immunity // Mucosal Immunol. 2018. Vol. 11, N 4. P. 1024–1038. doi: 10.1038/s41385-018-0019-2
  230. Cervantes-Barragan L., Chai J.N., Tianero M.D., et al. Lactobacillus reuteri induces gut intraepithelial CD4(+)CD8αα(+) T cells // Science. 2017. Vol. 357, N 6353. P. 806–810. doi: 10.1126/science.aah5825
  231. Rothhammer V., Borucki D.M., Sanchez M.I.G., et al. Dynamic regulation of serum aryl hydrocarbon receptor agonists in MS // Neurol Neuroimmunol Neuroinflamm. 2017. Vol. 4, N 4. P. e359. doi: 10.1212/NXI.0000000000000359
  232. Tsaktanis T., Beyer T., Nirschl L., et al. Aryl hydrocarbon receptor plasma agonist activity correlates with disease activity in progressive MS // Neurol Neuroimmunol Neuroinflam. 2021. Vol. 8, N 2. P. e933. doi: 10.1212/NXI.0000000000000933
  233. Quintana F.J., Basso A.S., Iglesias A.H., et al. Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor // Nature. 2008. Vol. 453, N 7191. P. 65–71. doi: 10.1038/nature06880
  234. Hanieh H., Alzahrani A. MicroRNA-132 suppresses autoimmune encephalomyelitis by inducing cholinergic anti-inflammation: A new Ahr-based exploration // Eur J Immunol. 2013. Vol. 43, N 10. P. 2771–2782. doi: 10.1002/eji.201343486
  235. Alzahrani A., Maged M., Hairul-Islam M.I., et al. Activation of aryl hydrocarbon receptor signaling by a novel agonist ameliorates autoimmune encephalomyelitis // PLoS One. 2019. Vol. 14, N 4. P. e0215981. doi: 10.1371/journal.pone.0215981
  236. Neamah W.H., Busbee P.B., Alghetaa H., et al. AhR activation leads to alterations in the gut microbiome with consequent effect on induction of myeloid derived suppressor cells in a CXCR2-dependent manner // Int J Mol Sci. 2020. Vol. 21, N 24. P. 9613. doi: 10.3390/ijms21249613
  237. Mangalam A., Murray J. Microbial monotherapy with Prevotella histicola for patients with multiple sclerosis // Expert Rev Neurother. 2019. Vol. 19, N 1. P. 45–53. doi: 10.1080/14737175.2019.1555473
  238. Hwang S.J., Hwang Y.J., Yun M.O., et al. Indoxyl 3-sulfate stimulates Th17 differentiation enhancing phosphorylation of c-Src and STAT3 to worsen experimental autoimmune encephalomyelitis // Toxicol Lett. 2013. Vol. 220, N 2. P. 109–117. doi: 10.1016/j.toxlet.2013.04.016
  239. Kishikawa T., Ogawa K., Motooka D. A metagenome-wide association study of gut microbiome in patients with multiple sclerosis revealed novel disease pathology // Front Cell Infect Microbiol. 2020. Vol. 10. P. 585973. doi: 10.3389/fcimb.2020.585973
  240. Jangi S., Gandhi R., Cox L.M., et al. Alterations of the human gut microbiome in multiple sclerosis // Nat Commun. 2016. Vol. 7. P. 12015. doi: 10.1038/ncomms12015
  241. Martins T.B., Rose J.W., Jaskowski T.D., et al. Analysis of proinflammatory and anti-inflammatory cytokine serum concentrations in patients with multiple sclerosis by using a multiplexed immunoassay // Am J Clin Pathol. 2011. Vol. 136, N 5. P. 696–704. doi: 10.1309/AJCP7UBK8IBVMVNR
  242. Nichols F.C., Housley W.J., O’Conor C.A., et al. Unique lipids from a common human bacterium represent a new class of Toll-like receptor 2 ligands capable of enhancing autoimmunity // Am J Pathol. 2009. Vol. 175, N 6. P. 2430–2438. doi: 10.2353/ajpath.2009.090544
  243. Farrokhi V., Nemati R., Nichols F.C., et al. Bacterial lipodipeptide, Lipid 654, is a microbiomeassociated biomarker for multiple sclerosis // Clin Trans Immunol. 2013. Vol. 2, N 11. P. e8. doi: 10.1038/cti.2013.11
  244. Yokote H., Miyake S., Croxford J.L., et al. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora // Am J Pathol. 2008. Vol. 173, N 6. P. 1714–1723. doi: 10.2353/ajpath.2008.080622
  245. Haghikia A., Jorg S., Duscha A., et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine // Immunity. 2015. Vol. 43, N 4. P. 817–829. doi: 10.1016/j.immuni.2015.09.007
  246. Lemus H.N., Warrington A.E., Rodriguez M. Multiple sclerosis: mechanisms of disease and strategies for myelin and axonal repair // Neurol Clin. 2018. Vol. 36, N 1. P. 1–11. doi: 10.1016/j.ncl.2017.08.002
  247. Ochoa-Repáraz J., Mielcarz D.W., Ditrio L.E., et al. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis // J Immunol. 2009. Vol. 183, N 10. P. 6041–6050. doi: 10.4049/jimmunol.0900747
  248. Miterski B., Böhringer S., Klein W., et al. Inhibitors in the NFkappaB cascade comprise prime candidate genes predisposing to multiple sclerosis, especially in selected combinations // Genes Immun. 2002. Vol. 3, N 4. P. 211–219. doi: 10.1038/sj.gene.6363846
  249. Gilli F., Lindberg R.L.P., Velentino P., et al. Learning from nature: pregnancy changes the expression of inflammation-related genes in patients with multiple sclerosis // PLoS One. 2010. Vol. 5, N 1. P. e8962. doi: 10.1371/journal.pone.0008962
  250. Bang C., Weidenbach K., Gutsmann T., et al. The intestinal archaea Methanosphaera stadtmanae and Methanobrevibacter smithii activate human dendritic cells // PLoS One. 2014. Vol. 9, N 6. P. e99411. doi: 10.1371/journal.pone.0099411
  251. Samuel B.S., Hansen E.E., Manchester J.K., et al. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut // Proc Natl Acad Sci USA. 2007. Vol. 104, N 25. P. 10643–10648. doi: 10.1073/pnas.0704189104
  252. Kusu T., Kayama H., Konoshita M., et al. Ecto-nucleoside triphosphate diphosphohydrolase 7 controls Th17 cell responses through regulation of luminal ATP in the small intestine // J Immunol. 2013. Vol. 190, N 2. P. 774–783. doi: 10.4049/jimmunol.1103067
  253. Kamada N., Seo S.-U., Chen G.Y., Núñez G. Role of the gut microbiota in immunity and inflammatory disease // Nat Rev Immunol. 2013. Vol. 13, N 5. P. 321–335. doi: 10.1038/nri3430
  254. Fujinami R.S., von Herrath M.G., Christen U., Whitton J.L. Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease // Clin Microbiol Rev. 2006. Vol. 19, N 1. P. 80–94. doi: 10.1128/CMR.19.1.80-94.2006
  255. Vanderlugt C.J., Miller S.D. Epitope spreading // Curr Opin Immunol. 1996. Vol. 8, N 6. P. 831–836. doi: 10.1016/s0952-7915(96)80012-4
  256. Fujinami R.S., Oldstone M.B. Amino acid homology between the encephalitogenic site of myelin basic protein (MBP) and virus: mechanism for autoimmunity // Science. 1985. Vol. 230, N 4729. P. 1043–1045. doi: 10.1126/science.2414848
  257. Christen U., von Herrath M.G. Induction, acceleration or prevention of autoimmunity by molecular mimicry // Mol Immunol. 2004. Vol. 40, N 14–15. P. 1113–1120. doi: 10.1016/j.molimm.2003.11.014
  258. Tough D.F., Sun S., Sprent J. T cell stimulation in vivo by lipopolysaccharide (LPS) // J Exp Med. 1997. Vol. 185, N 12. P. 2089–2094. doi: 10.1084/jem.185.12.2089
  259. Infante-Duarte C., Kamradt T. Lipopeptides of Borrelia burgdorferi outer surface proteins induce Th1 phenotype development in ab TCR transgenic mice // Infect Immun. 1997. Vol. 65, N 10. P. 4094–4099. doi: 10.1128/iai.65.10.4094-4099.1997
  260. Miller S.D., Vanderlugt C.L., Begolka W.S., et al. Persistent infection with Theiler’s virus leads to CNS autoimmunity via epitope spreading // Nat Med. 1997. Vol. 3, N 10. P. 1133–1136. doi: 10.1038/nm1097-1133
  261. Kamradt T., Soloway P.D., Perkins D.L., Gefter M.L. Pertussis toxin prevents the induction of peripheral T cell anergy and enhances the T cell response to an encephalitogenic peptide of myelin basic protein // J Immunol. 1991. Vol. 147, N 10. P. 3296–3302. doi: 10.4049/jimmunol.147.10.3296
  262. White J., Herman A., Pullen A.M., et al. The Vb-specific superantigen staphylococcal enterotoxin B: stimulation of mature T cells and clonal deletion in neonatal mice // Cell. 1989. Vol. 56, N 1. P. 27–35. doi: 10.1016/0092-8674(89)90980-x
  263. Segal B.M., Klinman D.M., Shevach E.M. Microbial products induce autoimmune disease by an IL-12-dependent pathway // J Immunol. 1997. Vol. 158, N 11. P. 5087–5090. doi: 10.4049/jimmunol.158.11.5087
  264. Blander J.M., Torchinsky M.B., Campisi L. Revisiting the old link between infection and autoimmune disease with commensals and T helper 17 cells // Immunol Res. 2012. Vol. 54, N 1–3. P. 50–68. doi: 10.1007/s12026-012-8311-9
  265. Balakrishnan B., Taneja V. Microbial modulation of the gut microbiome for treating autoimmune diseases // Expert Rev Gastroenterol Hepatol. 2018. Vol. 12, N 10. P. 985–996. doi: 10.1080/17474124.2018.1517044
  266. Brocke S., Gaur A., Piercy C., et al. Induction of relapsing paralysis in experimental autoimmune encephalomyelitis by bacterial superantigen // Nature. 1993. Vol. 365, N 6447. P. 642–644. doi: 10.1038/365642a0
  267. Krishnamoorthy G., Holz A., Wekerle H. Experimental models of spontaneous autoimmune disease in the central nervous system // J Mol Med (Berl). 2007. Vol. 85, N 11. P. 1161–1173. doi: 10.1007/s00109-007-0218-x
  268. Banki K., Colombo E., Sia F., et al. Oligodendrocyte-specific expression and autoantigenicity of transaldolase in multiple sclerosis // J Exp Med. 1994. Vol. 180, N 5. P. 1649–1663. doi: 10.1084/jem.180.5.1649
  269. Anderson D.C., van Schooten W.C., Barry M.E., et al. A Mycobacterium leprae-specific human T cell epitope crossreactive with an HLA-DR2 peptide // Science. 1988. Vol. 242, N 4876. P. 259–261. doi: 10.1126/science.2459778
  270. Atkinson M.A., Bowman M.A., Campbell L., et al. Cellular immunity to a determinant common to glutamic acid decarboxylase and Coxsackie virus in insulin dependent diabetes // J Clin Invest. 1994. Vol. 94, N 5. P. 2125–2129. doi: 10.1172/JCI117567
  271. van Eden W., Holoshitz J., Nevo Z., et al. Arthritis induced by a T-lymphocyte clone that responds to Mycobacterium tuberculosis and to cartilage proteoglycans // Proc Natl Acad Sci USA. 1985. Vol. 82, N 15. P. 5117–5120. doi: 10.1073/pnas.82.15.5117
  272. Garza K.M., Tung K.S. Frequency of molecular mimicry among T cell peptides as the basis for autoimmune disease and autoantibody induction // J Immunol. 1995. Vol. 155, N 11. P. 5444–5448.
  273. Singh V.K., Yamaki K., Donoso L.A., Shinohara T. Molecular mimicry: yeast histone H3-induced experimental autoimmune uveitis // J Immunol. 1989. Vol. 142, N 5. P. 1512–1517. doi: 10.4049/jimmunol.142.5.1512
  274. Mangalam A.K., Yadav M., Yadav R. The emerging world of microbiome in autoimmune disorders: Opportunities and challenges // Indian J Rheumatol. 2021. Vol. 16, N 1. P. 57–72. doi: 10.4103/injr.injr_210_20
  275. Evavold B.D., Sloan-Lancaster J., Wilson K.J., et al. Specific T cell recognition of minimally homologous peptides: evidence for multiple endogenous ligands // Immunity. 1995. Vol. 2, N 5. P. 655–663. doi: 10.1016/1074-7613(95)90010-1
  276. Ausubel L.J., Kwan C.K., Sette A., et al. Complementary mutations in an antigenic peptide allow for crossreactivity of autoreactive T-cell clones // Proc Natl Acad Sci USA. 1996. Vol. 93, N 26. P. 15317–15322. doi: 10.1073/pnas.93.26.15317
  277. Martin R., Vergelli M., Gran B., et al. Predictable TCR antigen recognition based on peptide scans leads to the identification of agonist ligands with no sequence homology // J Immunol. 1998. Vol. 160, N 8. P. 3631–3636.
  278. Hausmann S., Martin M., Gauthier L., Wucherpfennig K.W. Structural features of autoreactive TCR that determine the degree of degeneracy in peptide recognition // J Immunol. 1999. Vol. 162, N 1. P. 338–344. doi: 10.4049/jimmunol.162.1.338
  279. Wucherpfennig K.W., Strominger J.L. Molecular mimicry in T-cell mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein // Cell. 1995. Vol. 80, N 5. P. 695–705. doi: 10.1016/0092-8674(95)90348-8
  280. Grogan J.L., Kramer A., Nogai A., et al. Cross-reactivity of myelin basic protein-specific T cells with multiple microbial peptides: experimental autoimmune encephalomyelitis induction in TCR transgenic mice // J Immunol. 1999. Vol. 163, N 7. P. 3764–3770. doi: 10.4049/jimmunol.163.7.3764
  281. Parry S.L., Hall F.C., Olson J., et al. Autoreactivity versus autoaggression: a different perspective on human autoantigens // Curr Opin Immunol. 1998. Vol. 10, N 6. P. 663–668. doi: 10.1016/s0952-7915(98)80086-1
  282. Gautam A.M., Liblau R., Chelvanayagam G., et al. A viral peptide with limited homology to a self peptide can induce clinical signs of experimental autoimmune encephalomyelitis // J Immunol. 1998. Vol. 161, N 1. P. 60–64. doi: 10.4049/jimmunol.161.1.60
  283. Gautam A.M., Pearson C.I., Smilek D.E., et al. A polyalanine peptide with only five native myelin basic protein residues induces autoimmune encephalomyelitis // J Exp Med. 1992. Vol. 176, N 2. P. 605–609. doi: 10.1084/jem.176.2.605
  284. Ufret-Vincenty R.L., Quigley L., Tresser N., et al. In vivo survival of viral antigenspecific T cells that induce experimental autoimmune encephalomyelitis // J Exp Med. 1998. Vol. 188, N 9. P. 1725–1738. doi: 10.1084/jem.188.9.1725
  285. Lerner A., Aminov R., Matthias T. Dysbiosis may trigger autoimmune diseases via inappropriate post-translational modification of host proteins // Front Microbiol. 2016. Vol. 5, N 7. P. 84. doi: 10.3389/fmicb.2016.00084
  286. Root-Bernstein R.S., Westall F.C. Serotonin binding sites. II. Muramyl dipeptide binds serotonin binding sites on MBP, LHRH, and MSH-ACTH 4-10 // Brain Res Bull. 1990. Vol. 25, N 6. P. 827–841. doi: 10.1016/0361-9230(90)90178-3
  287. Westall F.C., Root-Bernstein R.S. An explanation of prevention and suppression of EAE // Mol Immunol. 1983. Vol. 20, N 2. P. 169–177. doi: 10.1016/0161-5890(83)90128-1
  288. Duc D., Vigne S., Bernier-Latmani J., et al. Disrupting myelin-specific Th17 cell gut homing confers protection in an adoptive transfer experimental autoimmune encephalomyelitis // Cell Rep. 2019. Vol. 29, N 2. P. 378–390. doi: 10.1016/j.celrep.2019.09.002
  289. Isailovic N., Daigo K., Mantovani A., Selmi C. Interleukin-17 and innate immunity in infections and chronic inflammation // J Autoimmun. 2015. Vol. 60. P. 1–11. doi: 10.1016/j.jaut.2015.04.006
  290. Fox A., Fox K., Christensson B., et al. Absolute identification of muramic acid, at trace levels, in human septic synovial fluids in vivo and absence in aseptic fluids // Infect Immun. 1996. Vol. 64, N 9. P. 3911–3915. doi: 10.1128/iai.64.9.3911-3915.1996
  291. Blais Lecours P., Duchaine C., Taillefer M., et al. Immunogenic properties of archaeal species found in bioaerosols // PLoS One. 2011. Vol. 6, N 8. P. e23326. doi: 10.1371/journal.pone.0023326
  292. Duchmann R., May E., Heike M., et al. T cell specificity and cross reactivity towards enterobacteria, bacteroides, bifidobacterium, and antigens from resident intestinal flora in humans // Gut. 1999. Vol. 44, N 6. P. 812–818. doi: 10.1136/gut.44.6.812
  293. McCoy K.D., Burkhard R., Geuking M.B. The microbiome and immune memory formation // Immunol Cell Biol. 2019. Vol. 97, N 7. P. 625–635. doi: 10.1111/imcb.12273
  294. Jahnke U., Fischer E.H., Alvord E.C.J. Sequence homology between certain viral proteins and proteins related to encephalomyelitis and neuritis // Science. 1985. Vol. 229, N 4710. P. 282–284. doi: 10.1126/science.2409602
  295. Marietta E.V., Murray J.A., Luckey D.H., et al. Human gut-derived Prevotella histicola suppresses inflammatory arthritis in humanized mice // Arthritis Rheumatol. 2016. Vol. 68, N 12. P. 2878–2888. doi: 10.1002/art.39785
  296. Yadav S.K., Boppana S., Ito N., et al. Gut dysbiosis breaks immunological tolerance toward the central nervous system during young adulthood // Proc Natl Acad Sci USA. 2017. Vol. 114, N 44. P. E9318–E9327. doi: 10.1073/pnas.1615715114
  297. Mosca A., Leclerc M., Hugot J.P. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? // Front Microbiol. 2016. Vol. 7. P. 455. doi: 10.3389/fmicb.2016.00455
  298. Qin J., Li R., Raes J., et al. A human gut microbial gene catalog established by metagenomic sequencing // Nature. 2010. Vol. 464, N 7285. P. 59–65. doi: 10.1038/nature08821
  299. Bergstrom J.H., Birchenough G.M., Katona G., et al. Gram-positive bacteria are held at a distance in the colon mucus by the lectin-like protein ZG16 // Proc Natl Acad Sci USA. 2016. Vol. 113, N 48. P. 13833–13838. doi: 10.1073/pnas.1611400113
  300. Donaldson G.P., Lee S.M., Mazmanian S.K. Gut biogeography of the bacterial microbiota // Nat Rev Microbiol. 2016. Vol. 14, N 1. P. 20–32. doi: 10.1038/nrmicro3552
  301. Derrien M., van Passel M.W., van de Bovenkamp J.H., et al. Mucin-bacterial interactions in the human oral cavity and digestive tract // Gut Microbes. 2010. Vol. 1, N 4. P. 254–268. doi: 10.4161/gmic.1.4.12778
  302. Yu Y., Sitaraman S., Gewirtz A.T. Intestinal epithelial cell regulation of mucosal inflammation // Immunol Res. 2004. Vol. 29, N 1–3. P. 55–68. doi: 10.1385/IR:29:1-3:055
  303. Cerutti F., Rescigno M. The biology of intestinal immunoglobulin A responses // Immunity. 2008. Vol. 28, N 6. P. 740–750. doi: 10.1016/j.immuni.2008.05.001
  304. Wells J.M., Loonen L.M., Karczewski J.M. The role of innate signaling in the homeostasis of tolerance and immunity in the intestine // Int J Med Microbiol. 2010. Vol. 300, N 1. P. 41–48. doi: 10.1016/j.ijmm.2009.08.008
  305. Wells J.M., Rossi O., Meijerink M., van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface // Proc Natl Acad Sci USA. 2011. Vol. 108 Suppl 1, N Suppl 1. P. 4607–4614. doi: 10.1073/pnas.1000092107
  306. Harris G., KuoLee R., Chen W.X. Role of toll-like receptors in health and diseases of gastrointestinal tract // World J Gastroenterol. 2006. Vol. 12, N 14. P. 2149–2160. doi: 10.3748/wjg.v12.i14.2149
  307. Günzel D., Yu A.S. Claudins and the modulation of tight junction permeability // Physiol Rev. 2013. Vol. 93, N 2. P. 525–569. doi: 10.1152/physrev.00019.2012
  308. Sato T., van Es J.H., Snippert H.J., et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts // Nature. 2011. Vol. 469, N 7330. P. 415–418. doi: 10.1038/nature09637
  309. Wells J.M., Brummer R.J., Derrien M., et al. Homeostasis of the gut barrier and potential biomarkers // Am J Physiol Gastrointest Liver Physiol. 2017. Vol. 312, N 3. P. G171–G193. doi: 10.1152/ajpgi.00048.2015
  310. Everard A., Belzer C., Geurts L., et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity // Proc Natl Acad Sci USA. 2013. Vol. 110, N 22. P. 9066–9071. doi: 10.1073/pnas.1219451110
  311. Peng L., Li Z.R., Green R.S., et al. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers // J Nutr. 2009. Vol. 139, N 9. P. 1619–1625. doi: 10.3945/jn.109.104638
  312. Plovier H., Everard A., Druart C., et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice // Nat Med. 2017. Vol. 23, N 1. P. 107–113. doi: 10.1038/nm.4236
  313. Kang C.S., Ban M., Choi E.J., et al. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodiuminduced colitis // PLoS One. 2013. Vol. 8, N 10. P. e76520. doi: 10.1371/journal.pone.0076520
  314. Mo Q., Liu T., Fu A., et al. Novel gut microbiota patterns involved in the attenuation of dextran sodium sulfate-induced mouse colitis mediated by glycerol monolaurate via inducing anti-inflammatory responses // mBio. 2021. Vol. 12, N 5. P. e02148–21. doi: 10.1128/mBio.02148-21
  315. Li J., Li Y., Zhou Y., et al. Actinomyces and alimentary tract diseases: a review of its biological functions and pathology // Biomed Res Int. 2018. Vol. 2018. P. 3820215. doi: 10.1155/2018/3820215
  316. Sellon R.K., Tonkonogy S., Schultz M., et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice // Infect Immun. 1998. Vol. 66, N 11. P. 5224–5231. doi: 10.1128/IAI.66.11.5224-5231.1998
  317. Winter S.E., Winter M.G., Xavier M.N., et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut // Science. 2013. Vol. 339, N 6120. P. 708–711. doi: 10.1126/science.1232467
  318. Baumgart M., Dogan B., Rishniw M., et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum // ISME J. 2007. Vol. 1, N 5. P. 403–418. doi: 10.1038/ismej.2007.52
  319. Williams J.M., Duckworth C.A., Burkitt M.D., et al. Epithelial cell shedding and barrier function: A matter of life and death at the small intestinal villus tip // Vet Pathol. 2015. Vol. 52, N 3. P. 445–455. doi: 10.1177/0300985814559404
  320. Bertin Y., Girardeau J.P., Chaucheyras-Durand F., et al. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content // Environ Microbiol. 2011. Vol. 13, N 2. P. 365–377. doi: 10.1111/j.1462-2920.2010.02334.x
  321. Garsin D.A. Ethanolamine utilization in bacterial pathogens: roles and regulation // Nat Rev Microbiol. 2010. Vol. 8, N 4. P. 290–295. doi: 10.1038/nrmicro2334
  322. Olsen I., Nichols F.C. Are sphingolipids and serine dipeptide lipids underestimated virulence factors of Porphyromonas gingivalis? // Infect Immun. 2018. Vol. 86, N 7. P. e00035–18. doi: 10.1128/IAI.00035-18
  323. Kim Y.J., Kang H.Y., Han Y., et al. A bloodstream infection by Ruminococcus gnavus in a patient with a gall bladder perforation // Anaerobe. 2017. Vol. 47. P. 129–131. doi: 10.1016/j.anaerobe.2017.05.007
  324. Wang F., Graham W.V., Wang Y., et al. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression // Am J Pathol. 2005. Vol. 166, N 2. P. 409–419. doi: 10.2353/ajpath.2006.060681
  325. Marrie R.A., Yu B.N., Leung S., et al. The utility of administrative data for surveillance of comorbidity in multiple sclerosis: a validation study // Neuroepidemiology. 2013. Vol. 40, N 2. P. 85–92. doi: 10.1159/000343188
  326. Koenig J., Cote N. Equine gastrointestinal motility – ileus and pharmacological modification // Can Vet J. 2006. Vol. 47, N 6. P. 551–559.
  327. Christakos S. Recent advances in our understanding of 1,25-dihydroxyvitamin D(3) regulation of intestinal calcium absorption // Arch Biochem Biophys. 2012. Vol. 523, N 1. P. 73–76. doi: 10.1016/j.abb.2011.12.020
  328. Somlyo A.P., Somlyo A.V. Signal transduction and regulation in smooth muscle // Nature. 1994. Vol. 372, N 6503. P. 231–236. doi: 10.1038/372231a0
  329. König J., Wells J., Cani P.D., et al. Human intestinal barrier function in health and disease // Clin Transl Gastroenterol. 2016. Vol. 7, N 10. P. e196. doi: 10.1038/ctg.2016.54
  330. Kawamoto S., Maruya M., Kato L.M., et al. Foxp3(+) T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis // Immunity. 2014. Vol. 41, N 1. P. 152–165. doi: 10.1016/j.immuni.2014.05.016
  331. Nakajima A., Vogelzang A., Maruya M., et al. IgA regulates the composition and metabolic function of gut microbiota by promoting symbiosis between bacteria // J Exp Med. 2018. Vol. 215, N 8. P. 2019–2034. doi: 10.1084/jem.20180427
  332. Shulzhenko N., Morgun A., Hsiao W., et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut // Nat Med. 2011. Vol. 17, N 12. P. 1585–1593. doi: 10.1038/nm.2505
  333. Rojas O.L., Pröbstel A.K., Porfilio E.A., et al. Recirculating intestinal IgA-producing cells regulate neuroinflammation via IL-10 // Cell. 2019. Vol. 176, N 3. P. 610–624.e18. doi: 10.1016/j.cell.2018.11.035

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