FROM CELLULAR ARCHITECTURE TO THE REGULATION OF MITOCHONDRIAL FUNCTION: THE ROLE OF VIMENTIN IN ENSURING CELLULAR MITOSTASIS
- Authors: Deeb R.1,2, Shakhov A.S1,3, Churkina A.S1,3, Alieva I.B1,3, Minin A.A1
-
Affiliations:
- Institute of Protein Research of Russian Academy of Sciences
- Moscow Institute of Physics and Technology (MIPT)
- Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University
- Issue: Vol 90, No 12 (2025)
- Pages: 2012—2020
- Section: Articles
- URL: https://ogarev-online.ru/0320-9725/article/view/376121
- DOI: https://doi.org/10.7868/S3034529425120078
- ID: 376121
Cite item
Abstract
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 UniversityPushchino, Russia; Moscow, Russia
A. S Churkina
Institute of Protein Research of Russian Academy of Sciences; Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityPushchino, Russia; Moscow, Russia
I. B Alieva
Institute of Protein Research of Russian Academy of Sciences; Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State UniversityPushchino, Russia; Moscow, Russia
A. A Minin
Institute of Protein Research of Russian Academy of Sciences
Email: alexminin@gmail.com
Pushchino, Russia
References
- 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.
- 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.
- Gulbins, E., Dreschers, S., and Bock, J. (2003) Role of mitochondria in apoptosis, Exp. Physiol., 88, 85-90, https://doi.org/10.1113/eph8802503.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- Кулик А. В., Гиоева Ф. К., Минин А. А. (2002) Видео-микроскопическое изучение подвижности митохондрий, Онтогенез, 33, 366-373.
- 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.
- Кулик А. В., Некрасова О. Е., Минин А. А. (2006) Фибриллярный актин регулирует подвижность митохондрий, Биол. Мембр., 23, 42-51.
- 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.
- Некрасова О. Е., Кулик А. В., Минин А. А. (2007) Протеинкиназа С регулирует подвижность митохондрий, Биол. Мембр., 24, 126-132.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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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