FROM CELLULAR ARCHITECTURE TO THE REGULATION OF MITOCHONDRIAL FUNCTION: THE ROLE OF VIMENTIN IN ENSURING CELLULAR MITOSTASIS

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Abstract

Mitochondria play a central role in cell physiology, and in addition to performing their primary function as an energy source, they are involved in processes such as regulating intracellular calcium levels, generating reactive oxygen species, synthesizing many critical compounds, regulating apoptosis, and more. In this regard, maintaining them in a normal state is of great importance, ensuring their transport, intracellular distribution, timely biogenesis, and removal of damaged mitochondria from cells. All of this is defined as cellular mitosis, the maintenance of which involves many cellular structures and, primarily, the cytoskeleton. This review summarizes data on the role of one component of the cytoskeleton, vimentin intermediate filaments, in these processes.

About the authors

R. Deeb

Institute of Protein Research of Russian Academy of Sciences; Moscow Institute of Physics and Technology (MIPT)

Pushchino, Russia; Dolgoprudny, Russia

A. S Shakhov

Institute of Protein Research of Russian Academy of Sciences; Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Pushchino, Russia; Moscow, Russia

A. S Churkina

Institute of Protein Research of Russian Academy of Sciences; Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Pushchino, Russia; Moscow, Russia

I. B Alieva

Institute of Protein Research of Russian Academy of Sciences; Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University

Pushchino, Russia; Moscow, Russia

A. A Minin

Institute of Protein Research of Russian Academy of Sciences

Email: alexminin@gmail.com
Pushchino, Russia

References

  1. Walkon, L. L., Strubbe-Rivera, J. O., and Bazil, J. N. (2022) Calcium overload and mitochondrial metabolism, Biomolecules, 12, 1891, https://doi.org/10.3390/biom12121891.
  2. Melchinger, P., and Garcia, B. M. (2023) Mitochondria are midfield players in steroid synthesis, Int. J. Biochem. Cell Biol., 160, 106431, https://doi.org/10.1016/j.biocel.2023.106431.
  3. Gulbins, E., Dreschers, S., and Bock, J. (2003) Role of mitochondria in apoptosis, Exp. Physiol., 88, 85-90, https://doi.org/10.1113/eph8802503.
  4. Skulachev, V. P., Bakeeva, L. E., Chernyak, B. V., Domnina, L. V., Minin, A. A., Pletjushkina, O. Y., Saprunova, V. B., Skulachev, I. V., Tsyplenkova, V. G., Vasiliev, J. M., Yaguzhinsky, L. S., and Zorov, D. B. (2004) Thread-grain transition of mitochondrial reticulum as a step of mitoptosis and apoptosis, Mol. Cell. Biochem., 256-257, 341-358, https://doi.org/10.1023/b:mcbi.0000009880.94044.49.
  5. Godoy, J. A., Rios, J. A., Picón-Pagès, P., Herrera-Fernández, V., Swaby, B., Crepin, G., Vicente, R., Fernández-­Fernández, J. M., and Muñoz, F. J. (2021) Mitostasis, calcium and free radicals in health, aging and neurodegeneration, Biomolecules, 11, 1012, https://doi.org/10.3390/biom11071012.
  6. Misgeld, T., and Schwarz, T. L. (2017) Mitostasis in neurons: maintaining mitochondria in an extended cellular architecture, Neuron, 96, 651-666, https://doi.org/10.1016/j.neuron.2017.09.055.
  7. Sies, H., and Jones, D. P. (2020) Reactive oxygen species (ROS) as pleiotropic physiological signalling agents, Nat. Rev. Mol. Cell Biol., 21, 363-383, https://doi.org/10.1038/s41580-020-0230-3.
  8. Varesi, A., Chirumbolo, S., Campagnoli, L. I. M., Pierella, E., Piccini, G. B., Carrara, A., Ricevuti, G., Scassellati, C., Bonvicini, C., and Pascale, A. (2022) The role of antioxidants in the interplay between oxidative stress and senescence, Antioxidants, 11, 1224, https://doi.org/10.3390/antiox11071224.
  9. Guéraud, F., Atalay, M., Bresgen, N., Cipak, A., Eckl, P. M., Huc, L., Jouanin, I., Siems, W., and Uchida, K. (2010) Chemistry and biochemistry of lipid peroxidation products, Free Radic. Res., 44, 1098-1124, https://doi.org/10.3109/10715762.2010.498477.
  10. Viedma-Poyatos, Á., González-Jiménez, P., Langlois, O., Company-Marín, I., Spickett, C. M., and Pérez-Sala, D. (2021) Protein lipoxidation: Basic concepts and emerging roles, Antioxidants, 10, 295, https://doi.org/10.3390/antiox10020295.
  11. Di Lorenzo, R., Chimienti, G., Picca, A., Trisolini, L., Latronico, T., Liuzzi, G. M., Pesce, V., Leeuwenburgh, C., and Lezza, A. M. S. (2024) Resveratrol impinges on retrograde communication without inducing mitochondrial biogenesis in aged rat soleus muscle, Exp. Gerontol., 194, 112485, https://doi.org/10.1016/j.exger.2024.112485.
  12. Fernández Casafuz, A. B., De Rossi, M. C., and Bruno, L. (2023) Mitochondrial cellular organization and shape fluctuations are differentially modulated by cytoskeletal networks, Sci. Rep., 13, 4065, https://doi.org/10.1038/s41598-023-31121-w.
  13. Boldogh, I. R., and Pon, L. A. (2006) Interactions of mitochondria with the actin cytoskeleton, Biochim. Biophys. Acta, 1763, 450-462, https://doi.org/10.1016/j.bbamcr.2006.02.014.
  14. Saxton, W. M., and Hollenbeck, P. J. (2012) The axonal transport of mitochondria, J. Cell Sci., 125, 2095-2104, https://doi.org/10.1242/jcs.053850.
  15. Mooseker, M. S., and Cheney, R. E. (1995) Unconventional myosins, Annu. Rev. Cell Dev. Biol., 11, 633-675, https://doi.org/10.1146/annurev.cb.11.110195.003221.
  16. Taunton, J., Rowning, B. A., Coughlin, M. L., Wu, M., Moon, R. T., Mitchison, T. J., and Larabell, C. A. (2000) Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP, J. Cell Biol., 148, 519-530, https://doi.org/10.1083/jcb.148.3.519.
  17. Кулик А. В., Гиоева Ф. К., Минин А. А. (2002) Видео-микроскопическое изучение подвижности митохондрий, Онтогенез, 33, 366-373.
  18. Некрасова О. Е., Минин Ан. А., Кулик А. В., Минин А. А. (2005) Регуляция фибронектином формы и внутриклеточного распределения митохондрий, Биол. Мембр., 22, 105-112.
  19. Кулик А. В., Некрасова О. Е., Минин А. А. (2006) Фибриллярный актин регулирует подвижность митохондрий, Биол. Мембр., 23, 42-51.
  20. Minin, A. A., Kulik, A.V., Gyoeva, F. K., Li, Y., Goshima, G., and Gelfand, V. I. (2006) Regulation of mitochondria distribution by RhoA and formins, J. Cell Sci., 119, 659-670, https://doi.org/10.1242/jcs.02762.
  21. Некрасова О. Е., Кулик А. В., Минин А. А. (2007) Протеинкиназа С регулирует подвижность митохондрий, Биол. Мембр., 24, 126-132.
  22. Nekrasova, O. E., Mendez, M. G., Chernoivanenko, I. S., Tyurin-Kuzmin, P. A., Kuczmarski, E. R., Gelfand, V. I., Goldman, R. D., and Minin, A. A. (2011) Vimentin intermediate filaments modulate the motility of mitochondria, Mol. Biol. Cell, 22, 2282-2289, https://doi.org/10.1091/mbc.E10-09-0766.
  23. Rapaport, D. (2003) Finding the right organelle Targeting signals in mitochondrial outer-membrane proteins, EMBO Rep., 4, 948-952, https://doi.org/10.1038/sj.embor.embor937.
  24. Araiso, Y., Imai, K., and Endo, T. (2022) Role of the TOM complex in protein import into mitochondria: structural views, Annu. Rev. Biochem., 91, 679-703, https://doi.org/10.1146/annurev-biochem-032620-104527.
  25. Schwarz, N., and Leube, R. E. (2016) Intermediate filaments as organizers of cellular space: how they affect mitochondrial structure and function, Cells, 5, 30, https://doi.org/10.3390/cells5030030.
  26. Etienne-Manneville, S. (2018) Cytoplasmic intermediate filaments in cell biology, Annu. Rev. Cell Dev. Biol., 34, 1-28, https://doi.org/10.1146/annurev-cellbio-100617-062534.
  27. Gilbert, S., Loranger, A., Daigle, N., and Marceau, N. (2001) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation, J. Cell Biol., 154, 763-773, https://doi.org/10.1083/jcb.200102130.
  28. Capetanaki, Y. (2002) Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function, Trends Cardiovasc. Med., 12, 339-348, https://doi.org/10.1016/S1050-1738(02)00184-6.
  29. Uttam, J., Hutton, E., Coulombe, P. A., Anton-Lamprecht, I., Yu, Q. C., Gedde-Dahl, T., Jr., Fine, J. D., and Fuchs, E. (1996) The genetic basis of epidermolysis bullosa simplex with mottled pigmentation, Proc. Natl. Acad. Sci. USA, 93, 9079-9084, https://doi.org/10.1073/pnas.93.17.9079.
  30. Brownlees, J., Ackerley, S., Grierson, A. J., Jacobsen, N. J., Shea, K., Anderton, B. H., Leigh, P. N., Shaw, C. E., and Miller, C. C. (2002) Charcot-Marie-Tooth disease neurofilament mutations disrupt neurofilament assembly and axonal transport, Hum. Mol. Genet., 11, 2837-2844, https://doi.org/10.1093/hmg/11.23.2837.
  31. Milner, D. J., Mavroidis, M., Weisleder, N., and Capetanaki, Y. (2000) Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function, J. Cell Biol., 150, 1283-1298, https://doi.org/10.1083/jcb.150.6.1283.
  32. Wagner, O. I., Lifshitz, J., Janmey, P. A., Linden, M., McIntosh, T. K., and Leterrier, J. F. (2003) Mechanisms of mitochondria-neurofilament interactions, J. Neurosci., 23, 9046-9058, https://doi.org/10.1523/JNEUROSCI.23-27-09046.2003.
  33. Tolstonog, G. V., Belichenko-Weitzmann, I. V., Lu, J. P., Hartig, R., Shoeman, R. L., Traub, U., and Traub, P. (2005) Spontaneously immortalized mouse embryo fibroblasts: growth behavior of wild-type and vimentin-deficient cells in relation to mitochondrial structure and activity, DNA Cell Biol., 24, 680-709, https://doi.org/10.1089/dna.2005.24.680.
  34. Fuchs, E., and Weber, K. (1994) Intermediate filaments: structure, dynamics, function and disease, Annu. Rev. Biochem., 63, 345-382, https://doi.org/10.1146/annurev.bi.63.070194.002021.
  35. Alieva, I. B., Shakhov, A. S., Dayal, A. A., Parfenteva, O. I., and Minin, A. A. (2024) Unique role of vimentin in the intermediate filament proteins family, Biochemistry (Moscow), 89, 726-736, https://doi.org/10.1134/S0006297924040114.
  36. Dayal, A. A., Medvedeva, N. V., and Minin, A. A. (2022) N-Terminal fragment of vimentin is responsible for binding of mitochondria in vitro, Membr. Cell Biol., 5, 21-28.
  37. Dayal, A. A., Medvedeva, N. V., Nekrasova, T. M., Duhalin, S. D., Surin, A. K., and Minin, A. A. (2020) Desmin interacts directly with mitochondria, Int. J. Mol. Sci., 21, 8122, https://doi.org/10.3390/ijms21218122.
  38. Chernoivanenko, I. S., Matveeva, E. A., Gelfand, V. I., Goldman, R. D., and Minin, A. A. (2015) Mitochondrial membrane potential is regulated by vimentin intermediate filaments, FASEB J., 29, 820-827, https://doi.org/10.1096/fj.14-259903.
  39. Matveeva, E. A., Venkova, L. S., Chernoivanenko, I. S., and Minin, A. A. (2015) Vimentin is involved in regulation of mitochondrial motility and membrane potential by Rac1, Biol. Open., 4, 1290-1297, https://doi.org/10.1242/bio.013326.
  40. Huynh, T. N., Toperzer, J., Scherer, A., Gumina, A., Brunetti, T., Mansour, M. K., Markovitz, D. M., and Russo, B. C. (2024) Vimentin regulates mitochondrial ROS production and inflammatory responses of neutrophils, Front. Immunol., 15, 1416275, https://doi.org/10.3389/fimmu.2024.1416275.
  41. San Martín, A., and Griendling, K. K. (2010) Redox control of vascular smooth muscle migration, Antioxid. Redox Signal., 12, 625-640, https://doi.org/10.1089/ars.2009.2852.
  42. Venkova, L. S., Chernoivanenko, I. S., and Minin, A. A. (2014) Hydrogen peroxide stimulating migration of fibroblasts is formed in mitochondria, Membr. Cell Biol., 8, 309-313, https://doi.org/10.1134/S1990747814050080.
  43. Matveeva, E. A., Chernoivanenko, I. S., and Minin, A. A. (2010) Vimentin intermediate filaments protect mitochondria from oxidative stress, Membr. Cell Biol., 4, 321-331, https://doi.org/10.1134/S199074781004001X.
  44. Venkova, L. S., Zerkalenkova, E. A., and Minin, A. A. (2018) Vimentin protects cells against doxorubicin and vincristine, Membr. Cell Biol., 12, 255-260, https://doi.org/10.1134/S1990747818030091.
  45. Hemel, I. M. G. M., Steen, C., Denil, S. L. I. J., Ertaylan, G., Kutmon, M., Adriaens, M., and Gerards, M. (2025) The unusual suspect: A novel role for intermediate filament proteins in mitochondrial morphology, Mitochondrion, 81, 102008, https://doi.org/10.1016/j.mito.2025.102008.
  46. Winter, L., Abrahamsberg, C., and Wiche, G. (2008) Plectin isoform 1b mediates mitochondrion-intermediate filament network linkage and controls organelle shape, J. Cell Biol., 181, 903-911, https://doi.org/10.1083/jcb.200710151.
  47. Yardeni, T., Fine, R., Joshi, Y., Gradus-Pery, T., Kozer, N., Reichenstein, I., Yanowski, E., Nevo, S., Weiss-Tishler, H., Eisenberg-Bord, M., Shalit, T., Plotnikov, A., Barr, H. M., Perlson, E., and Hornstein, E. (2018) High content image analysis reveals function of miR-124 upstream of Vimentin in regulating motor neuron mitochondria, Sci. Rep., 8, 59, https://doi.org/10.1038/s41598-017-17878-x.
  48. Eibauer, M., Weber, M. S., Kronenberg-Tenga, R., Beales, C. T., Boujemaa Paterski, R., Turgay, Y., Sivagurunathan, S., Kraxner, J., Koster, S., Goldman, R. D., and Medalia, O. (2024) Vimentin filaments integrate low complexity domains in a complex helical structure, Nat. Struct. Mol. Biol., 31, 939-949, https://doi.org/10.1038/s41594-024-01261-2.

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