Changes in the Expression of Purinergic Receptors of the CNS Cells during Cerebral Ischemia

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Abstract

Purines and their derivatives, adenosine and ATP, are key molecules that control intracellular energy homeostasis and nucleotide synthesis. Purines act as endogenous ligands of purine receptors, which activation triggers intracellular purinergic signaling. Purinergic signaling is cross-linked with other signaling cascades, thereby participating in the coordination of cellular processes such as proliferation, differentiation, migration, apoptosis and other physiological and pathological reactions that are critical for the body. In neurodegenerative disorders such as ischemic stroke, encephalopathy (including diabetic), Alzheimer’s disease, Parkinson’s disease and a number of other neurodegenerative disorders associated with neuroinflammation, there is a change in purine metabolism and a change in the expression of purinergic receptors. Purinergic receptors are involved in the regulation of neuroinflammatory reactions that modulate the functions of neurons, microglia and astrocytes. The study of the mechanisms of purinergic signaling in various pathological conditions demonstrates the significant therapeutic potential of using purinergic agonists and antagonists for the correction of pathological conditions of the CNS.

About the authors

I. G. Savinkova

Institute of Physiology, Pirogov Russian National Research Medical University

Email: irenesavik@mail.ru
Moscow, Russia

I. I. Babkina

Institute of Physiology, Pirogov Russian National Research Medical University

Moscow, Russia

M. P. Morozova

Institute of Physiology, Pirogov Russian National Research Medical University

Moscow, Russia

L. R. Gorbacheva

Lomonosov Moscow State University

Moscow, Russia

References

  1. Lindberg D., Andres-Beck L., Jia Y.-F., Kang S., Choi D.-S. // Front. in Physiol. 2018. V. 9. P. 9.
  2. Burnstock G. // Physiol. Rev. 2007. V. 87. № 2. P. 659–797.
  3. Fields R.D., Burnstock G. // Nat. Rev. Neurosci. 2006. V. 7. № 6. P. 423–436.
  4. Franke H., Verkhratsky A., Burnstock G., Illes P. // Purinergic Signal. 2012. V. 8. № 3. P. 629–657.
  5. Koizumi S., Ohsawa K., Inoue K., Kohsaka S. // Glia. 2013. V. 61. № 1. P. 47–54.
  6. Melani A., Turchi D., Vannucchi M.G., Cipriani S., Gianfriddo M., Pedata F. // Neurochem. Int. 2005. V. 47. № 6. P. 442–448.
  7. Shigetomi E., Sakai K., Koizumi S. // Front. in Cell and Dev. B. 2024. V. 11. P. 1343653.
  8. Burnstock G. // Brain and Neurosci. Adv. 2018. V. 2. P. 1–10.
  9. Jacobson K.A., Balasubramanian R., Deflorian F., Gao Z.-G. // Purinergic Signal. 2012. V. 8. № 3. P. 419–436.
  10. Huang Z., Xie N., Illes P., Di Virgilio F., Ulrich H., Semyanov A., Verkhratsky A., Sperlagh B., Yu S.-G., Huang C., Tang Y. // Signal Transduct. and Target. Ther. 2021. V. 6. № 1. P. 1–20.
  11. Manwani B., McCullough L.D. // J. of Neur. R. 2013. V. 91. № 8. P. 1018–1029.
  12. Allaman I., Lengacher S., Magistretti P.J., Pellerin L. // Am. J. of Physiol.-Cell Physiol. 2003. V. 284. № 3. P. C696–C704.
  13. Biber K., Klotz K.-N., Berger M., Gebicke-Härter P.J., Calker D. van // J. Neurosci. 1997. V. 17. № 13. P. 4956–4964.
  14. Gebicke-Haerter P.J., Christoffel F., Timmer J., Northoff H., Berger M., Van calker D. // Neurochem. Int. 1996. V. 29. № 1. P. 37–42.
  15. Gonçalves F.Q., Pires J., Pliassova A., Beleza R., Lemos C., Marques J.M., Rodrigues R.J., Canas P.M., Köfalvi A., Cunha R.A., Rial D. // Eur. J. Neurosci. 2015. V. 41. № 7. P. 878–888.
  16. Li X.X., Nomura T., Aihara H., Nishizaki T. // Life Sci. 2001. V. 68. № 12. P. 1343–1350.
  17. Lopes C.R., Cunha R.A., Agostinho P. // Front. in Neurosci. 2021. V. 15. P. 666710.
  18. Melani A., Cipriani S., Vannucchi M.G., Nosi D., Donati C., Bruni P., Giovannini M.G., Pedata F. // Brain. 2009. V. 132. № 6. P. 1480–1495.
  19. Othman T., Yan H., Rivkees S.A. // Glia. 2003. V. 44. № 2. P. 166–172.
  20. Theparambil S.M., Kopach O., Braga A., Nizari S., Hosford P.S., Sagi-Kiss V., Hadjihambi A., Konstantinou C., Esteras N., Gutierrez Del Arroyo A., Ackland G.L., Teschemacher A.G., Dale N., Eckle T., Andrikopoulos P., Rusakov D.A., Kasparov S., Gourine A.V. // Nature. 2024. V. 632. № 8023. P. 139–146.
  21. Lillo A., Serrano-Marín J., Lillo J., Raïch I., Navarro G., Franco R. // Purinergic Signal. 2024. V. 20. № 3. P. 237–245.
  22. Lopes L.V., Rebola N., Pinheiro P.C., Richardson P.J., Oliveira C.R., Cunha R.A. // NeuroReport. 2003. V. 14. № 12. P. 1645.
  23. Stockwell J., Jakova E., Cayabyab F.S. // Molecules. 2017. V. 22. № 4. P. 676.
  24. Fredholm B.B., IJzerman A.P., Jacobson K.A., Linden J., Müller C.E. // Pharmacol. Rev. 2011. V. 63. № 1. P. 1–34.
  25. Adenosine Receptors / Gomes C.V., Kaster M.P., Tomé A.R., Agostinho P.M., Cunha R.A. // Biochim. Biophys. Acta - Biomembr. 2011. V. 1808. № 5. P. 1380–1399.
  26. Roberts J.A., Vial C., Digby H.R., Agboh K.C., Wen H., Atterbury-Thomas A., Evans R.J. // Pflügers Archiv. 2006. V. 452. № 5. P. 486–500.
  27. Burnstock G., B. Fredholm B., Verkhratsky A. // Curr. Top. Med. Chem. 2011. V. 11. № 8. P. 973–1011.
  28. Pankratov Y., Lalo U., Verkhratsky A., North R.A. // Pflügers Archiv. 2006. V. 452. № 5. P. 589–597.
  29. Pankratov Y., Lalo U., Krishtal O., Verkhratsky A. // J. of physiol. 2002. V. 542. № 2. P. 529–536.
  30. Köles L., Leichsenring A., Rubini P., Illes P. // Pharm. of Purine and Pyrimidine Rec. / ed. K. A. Jacobson, J. Linden. Academic Press, 2011. V. 61. P. 441–493.
  31. Illes P., Ribeiro J.A. // Curr. Top. Med. Chem. 2004. V. 4. № 8. P. 831–838.
  32. Dı́az-Hernández M., Gómez-Villafuertes R., Hernando F., Pintor J., Miras-Portugal M.T. // Neurosci. Letters. 2001. V. 301. № 3. P. 159–162.
  33. Vulchanova L., Riedl M.S., Shuster S.J., Stone L.S., Hargreaves K.M., Buell G., Surprenant A., North R.A., Elde R. // Eur. J. Neurosci. 1998. V. 10. № 11. P. 3470–3478.
  34. Dixon S.J., Yu R., Panupinthu N., Wilson J.X. // Glia. 2004. V. 47. № 4. P. 367–376.
  35. Franke H., Grosche J., Schädlich H., Krügel U., Allgaier C., Illes P. // Neurosci. 2001. V. 108. № 3. P. 421–429.
  36. Kukley M., Barden J.A., Steinhäuser C., Jabs R. // Glia. 2001. V. 36. № 1. P. 11–21.
  37. Loesch A., Burnstock G. // Cell and Tissue Res. 1998. V. 294. № 2. P. 253–260.
  38. Palygin O., Lalo U., Verkhratsky A., Pankratov Y. // Cell Calcium. 2010. V. 48. № 4. P. 225–231.
  39. Abbracchio M.P., Ceruti S. // Purinergic Signal. 2006. V. 2. № 4. P. 595–604.
  40. Neary J.T., Zimmermann H. // Trends in Neurosci. 2009. V. 32. № 4. P. 189–198.
  41. Verkhrasky A., Krishtal O.A., Burnstock G. // Mol. Neurobiol. 2009. V. 39. № 3. P. 190–208.
  42. Simões A.P., Silva C.G., Marques J.M., Pochmann D., Porciúncula L.O., Ferreira S., Oses J.P., Beleza R.O., Real J.I., Köfalvi A., Bahr B.A., Lerma J., Cunha R.A., Rodrigues R.J. // Cell Death & Dis.. 2018. V. 9. № 3. P. 297.
  43. Rodrigues R.J., Figueira A.S., Marques J.M. // NeuroSci. 2022. V. 3. № 4. P. 604–615.
  44. Luthardt J., Borvendeg S.J., Sperlagh B., Poelchen W., Wirkner K., Illes P. // Neurochem. Int. 2003. V. 42. № 2. P. 161–172.
  45. Delekate A., Füchtemeier M., Schumacher T., Ulbrich C., Foddis M., Petzold G.C. // Nat. Commun. 2014. V. 5. № 1. P. 5422.
  46. Burgos M., Neary J.T., González F.A. // J. Neurochem. 2007. V. 103. № 5. P. 1785–1800.
  47. Rodríguez‐Zayas A.E., Torrado A.I., Miranda J.D. // Int. J. Dev. Neurosci. 2010. V. 28. № 6. P. 413–421.
  48. Xue L., Chen S., Xue S., Zhang X., Lian Y. // Neuroscience. 2022. V. 480. P. 155–166.
  49. Jurcau A., Simion A. // Int. J. Mol. Sci. 2021. V. 23. № 1. P. 14.
  50. Turovsky E.A., Varlamova E.G., Plotnikov E.Y. // Int. J. Mol. Sci. 2021. V. 22. № 16. P. 8805.
  51. Caba E., Sherman M.D., Farizatto K.L.G., Alcira B., Wang H., Giardina C., Shin D.-G., Sandefur C.I., Bahr B.A. // J. Cell. Mol. Med. 2021. V. 25. P. 9011–9027.
  52. Neves D., Salazar I.L., Almeida R.D., Silva R.M. // Life Sci. 2023. V. 328. P. 121814.
  53. Wu Q.J., Tymianski M. // Mol. Brain. 2018. V. 11. № 1. P. 15.
  54. Lobner D., Lipton P. // J. Neurosci. 1993. V. 13. № 11. P. 4861–4871.
  55. Chen H., Yoshioka H., Kim G.S., Jung J.E., Okami N., Sakata H., Maier C.M., Narasimhan P., Goeders C.E., Chan P.H. // Antioxid. Redox Signal. 2011. V. 14. № 8. P. 1505–1517.
  56. Yang C., Hawkins K.E., Doré S., Candelario-Jalil E. // Am. J. Physiol. Cell Physiol. 2019. V. 316. № 2. P. C135–C153.
  57. Hidetoshi T.-S., Makoto T., Inoue K. // Wiley Interdisciplinary Reviews: Membrane Transp. and Signal. 2012. V. 1. № 4. P. 493–501.
  58. Illes P., Xu G.-Y., Tang Y. // Neurosci. B. 2020. V. 36. № 11. P. 1239–1241.
  59. Territo P.R., Zarrinmayeh H. // Front. Cell. Neurosci. 2021. V. 15. P. 617036.
  60. Bai H.-Y., Li A.-P. // Neurosci. B. 2013. V. 29. № 3. P. 390–398.
  61. Challa S.R., Levingston H., Fornal C.A., Baker I.M., Boston J., Shanthappa N., Unnam P., Klopfenstein J.D., Veeravalli K.K. // Int. J. Mol. Sci. 2025. V. 26. № 6. P. 2379.
  62. Hirayama Y., Anzai N., Kinouchi H., Koizumi S. // Molecules. 2022. V. 27. № 12. P. 3655.
  63. Surprenant A., North R.A. // Annual Review of Physiology. 2009. V. 71. P. 333–359.
  64. Feuvre R.A.L., Brough D., Touzani O., Rothwell N.J. // J. Cereb. Blood Flow Metab. 2003. V. 23. №. 3. P. 381–384.
  65. Förster D., Reiser G. // Purinergic Signal. 2015. V. 11. № 4. P. 441–454.
  66. Melani A., Amadio S., Gianfriddo M., Vannucchi M.G., Volontè C., Bernardi G., Pedata F., Sancesario G. // J. of Cereb. Blood Flow Metab. 2006. V. 26. №. 7. P. 974–982
  67. Wang Y., Zhu Y., Wang J., Dong L., Liu S., Li S., Wu Q. // Front. Pharmacol. 2023. V. 14. P. 1112758.
  68. Ozaki T., Muramatsu R., Sasai M., Yamamoto M., Kubota Y., Fujinaka T., Yoshimine T., Yamashita T. // Sci.Rep. 2016. V. 6. № 1. P. 25893.
  69. Verma R., Cronin C.G., Hudobenko J., Venna V.R., McCullough L.D., Liang B.T. // Brain Behav. and Immun. 2017. V. 66. P. 302–312.
  70. Chu K., Yin B., Wang J., Peng G., Liang H., Xu Z., Du Y., Fang M., Xia Q., Luo B. // J. Neuroinflam. 2012. V. 9. № 1. P. 69.
  71. Wilmes M., Pinto Espinoza C., Ludewig P., Stabernack J., Liesz A., Nicke A., Gelderblom M., Gerloff C., Falzoni S., Tolosa E., Di Virgilio F., Rissiek B., Plesnilla N., Koch-Nolte F., Magnus T. // J. Neuroinflam. 2022. V. 19. № 1. P. 256.
  72. Chin Y., Kishi M., Sekino M., Nakajo F., Abe Y., Terazono Y., Hiroyuki O., Kato F., Koizumi S., Gachet C., Hisatsune T. // J. Neuroinflam. 2013. V. 10. № 1. P. 860.
  73. Kuboyama K., Harada H., Tozaki-Saitoh H., Tsuda M., Ushijima K., Inoue K. // J. of Cereb. Blood Flow Metab. 2011. V. 31. №. 9. P. 1930–1941.
  74. Milde S., Brown G.C. // Int. J. Mol. Sci. 2022. V. 23. № 4. P. 2304.
  75. Webster C.M., Hokari M., McManus A., Tang X.N., Ma H., Kacimi R., Yenari M.A. // PLOS ONE. 2013. V. 8. № 8. P. e70927.
  76. Chu S., Xiong W., Zhang D., Soylu H., Sun C., Albensi B.C., Parkinson F.E. // Acta Pharmacologica Sin. 2013. V. 34. № 1. P. 60–66.
  77. Liu B., Liao M., Mielke J.G., Ning K., Chen Y., Li L., El-Hayek Y.H., Gomez E., Zukin R.S., Fehlings M.G., Wan Q. // J. Neurosci. 2006. V. 26. № 20. P. 5309–5319.
  78. Lewerenz A., Hentschel S., Vissiennon Z., Michael S., Nieber K. // Drug Dev. Res. 2003. V. 58. № 4. P. 420–427.
  79. Pugliese A.M., Coppi E., Spalluto G., Corradetti R., Pedata F. // Br. J. Pharmacol. 2006. V. 147. № 5. P. 524–532.
  80. Pugliese A.M., Coppi E., Volpini R., Cristalli G., Corradetti R., Jeong L.S., Jacobson K.A., Pedata F. // Biochem. Pharmacol. 2007. V. 74. № 5. P. 768–779.
  81. Coppi E., Cherchi F., Venturini M., Lucarini E., Corradetti R., Di Cesare Mannelli L., Ghelardini C., Pedata F., Pugliese A.M. // Molecules. 2022. V. 27. № 6. P. 1890.
  82. Cavaliere F., Florenzano F., Amadio S., Fusco F.R., Viscomi M.T., D’Ambrosi N., Vacca F., Sancesario G., Bernardi G., Molinari M., Volontè C. // Neuroscience. 2003. V. 120. № 1. P. 85–98.
  83. Montilla A., Mata G.P., Matute C., Domercq M. // Int. J. Mol. Sci. 2020. V. 21. № 15. P. 5562.
  84. Domercq M., Vazquez N., Matute C. // Front. Cell. Neurosci. 2013. V. 7. P. 49.
  85. Xiang Z., Jiang X., Ji R., Yuan H. // Purinergic Signal. 2021. V. 17. № 3. P. 425–438.
  86. Sluyter R. // ed. M. Z. Atassi. Singapore: Springer, 2017. P. 17–53.
  87. Miras-Portugal M.T., Sebastián-Serrano Á., De Diego García L., Díaz-Hernández M. // Journal Neurosci. 2017. V. 37. № 30. P. 7063–7072.
  88. Arbeloa J., Pérez-Samartín A., Gottlieb M., Matute C. // Neurobiol. Dis. 2012. V. 45. № 3. P. 954–961.
  89. Cisneros-Mejorado A., Gottlieb M., Cavaliere F., Magnus T., Koch-Nolte F., Scemes E., Pérez-Samartín A., Matute C. // J. Cereb. Blood Flow Metab. 2015. V. 35. № 5. P. 843–850.
  90. Cavaliere F., Amadio S., Sancesario G., Bernardi G., Volonté C. // J. Cereb. Blood Flow Metab. 2004. V. 24. №. 4. P. 392–398.
  91. Milius D., Sperlagh B., Illes P. // Neurosci. Letters. 2008. V. 446. № 1. P. 45–50.
  92. Kaczmarek-Hajek K., Zhang J., Kopp R., Grosche A., Rissiek B., Saul A., Bruzzone S., Engel T., Jooss T., Krautloher A., Schuster S., Magnus T., Stadelmann C., Sirko S., Koch-Nolte F., Eulenburg V., Nicke A. // eLife. 2018. V. 7. P. e36217.
  93. Rubini P., Pagel G., Mehri S., Marquardt P., Riedel T., Illes P. // Naunyn Schmiedebergs Arch. Pharmacol. 2014. V. 387. № 10. P. 943–954.
  94. Fujita T., Tozaki-Saitoh H., Inoue K. // Glia. 2009. V. 57. № 3. P. 244–257.
  95. Traini C., Pedata F., Cipriani S., Mello T., Galli A., Giovannini M.G., Cerbai F., Volpini R., Cristalli G., Pugliese A.M. // Eur. J. Neurosci. 2011. V. 33. № 12. P. 2203–2215.
  96. Peterson T.S., Camden J.M., Wang Y., Seye C.I., Wood W.G., Sun G.Y., Erb L., Petris M.J., Weisman G.A. // Mol. Neurobiol. 2010. V. 41. № 2. P. 356–366.
  97. Горбачева Л.Р., Помыткин И.А., Сурин А.М., Абрамов Е.А., Пинелис В.Г. // Рос. пед. журнал. 2018. V. 21. № 1. P. 46–53.
  98. Sofroniew M.V. // Trends in Neurosci. 2009. V. 32. № 12. P. 638–647.
  99. Sofroniew M.V., Vinters H.V. // Acta Neuropathol. 2010. V. 119. № 1. P. 7–35.
  100. Brambilla R., Neary J.T., Cattabeni F., Cottini L., D’Ippolito G., Schiller P.C., Abbracchio M.P. // J. Neurochem. 2002. V. 83. № 6. P. 1285–1296.
  101. Washburn K.B., Neary J.T. // Neuroscience. 2006. V. 142. № 2. P. 411–423.
  102. Franke H., Sauer C., Rudolph C., Krügel U., Hengstler J.G., Illes P. // Glia. 2009. V. 57. № 10. P. 1031–1045.
  103. Sun J.-J., Liu Y., Ye Z.-R. // Neurosci. Bulletin. 2008. V. 24. № 4. P. 231–243.
  104. Lämmer A.B., Beck A., Grummich B., Förschler A., Krügel T., Kahn T., Schneider D., Illes P., Franke H., Krügel U. // PloS One. 2011. V. 6. № 5. P. e19983.
  105. Förster D., Reiser G. // Neurochem. Int. 2016. V. 94. P. 57–66.
  106. Wixey J.A., Reinebrant H.E., Carty M.L., Buller K.M. // J. Neuroimmunol. 2009. V. 212. № 1. P. 35–43.
  107. Lai A.Y., Todd K.G. // Can. J. Physiol. and Pharmacol. 2006. V. 84. № 1. P. 49–59.
  108. Weinstein J.R., Koerner I.P, Möller T. // Future Neurology. 2009. V. 5. № 2. P. 227–246.
  109. Block M.L., Zecca L., Hong J.-S. // Nat. Rev. Neurosci. 2007. V. 8. № 1. P. 57–69.
  110. Egan T.M., Khakh B.S. // J. Neurosci. 2004. V. 24. № 13. P. 3413–3420.
  111. Skaper S.D. // CNS Neurol. Disord. Drug Targets. 2011. V. 10. № 1. P. 44–56.
  112. Raouf R., Chabot-Doré A.-J., Ase A.R., Blais D., Séguéla P. // Neuropharmacol. 2007. V. 53. № 4. P. 496–504.
  113. Kaiser M., Penk A., Franke H., Krügel U., Nörenberg W., Huster D., Schaefer M. // Purinergic Signal. 2016. V. 12. № 3. P. 453–463.
  114. Fukumoto Y., Tanaka K.F., Parajuli B., Shibata K., Yoshioka H., Kanemaru K., Gachet C., Ikenaka K., Koizumi S., Kinouchi H. // J. Cereb. Blood Flow Metab. 2019. V. 39. №. 11. P. 2144–2156.
  115. Wen R.-X., Shen H., Huang S.-X., Wang L.-P., Li Z.-W., Peng P., Mamtilahun M., Tang Y.-H., Shen F.-X., Tian H.-L., Yang G.-Y., Zhang Z.-J. // CNS Neurosci. Ther. 2020. V. 26. № 4. P. 416–429.
  116. Amadio S., Parisi C., Montilli C., Carrubba A.S., Apolloni S., Volonté C. // Mediators Inflamm. 2014. V. 2014. P. 975849.
  117. Gelosa P., Lecca D., Fumagalli M., Wypych D., Pignieri A., Cimino M., Verderio C., Enerbäck M., Nikookhesal E., Tremoli E., Abbracchio M.P., Sironi L. // J. Cereb. Blood Flow Metab. 2014. V. 34. № 6. P. 979–988.
  118. Gómez Morillas A., Besson V.C., Lerouet D. // Int. J. Mol. Sci. 2021. V. 22. № 4. P. 1636.

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