Skip to main content

Advertisement

SpringerLink
Log in

Do mitochondria have an immune system?

  • Hypothesis
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The question if mitochondria have some kind of immune system is not trivial. The basis for raising this question is the fact that bacteria, which are progenitors of mitochondria, do have an immune system. The CRISPR system in bacteria based on the principle of RNA interference serves as an organized mechanism for destroying alien nucleic acids, primarily those of viral origin. We have shown that mitochondria are also a target for viral attacks, probably due to a related organization of genomes in these organelles and bacteria. Bioinformatic analysis performed in this study has not given a clear answer if there is a CRISPR-like immune system in mitochondria. However, this does not preclude the possibility of mitochondrial immunity that can be difficult to decipher or that is based on some principles other than those of CRISPR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., and Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes, Science, 315, 1709–1712.

    Article  CAS  PubMed  Google Scholar 

  2. Price, W. H. (1952) Bacterial viruses, Annu. Rev. Microbiol., 6, 333–348.

    Article  CAS  PubMed  Google Scholar 

  3. Anand, S. K., and Tikoo, S. K. (2013) Viruses as modulators of mitochondrial functions, Adv. Virol., 2013, 738–794.

    Article  Google Scholar 

  4. Zhdanov, V. M., Tikhonenko, T. I., Bocharov, A. F., and Naroditsky, B. A. (1971) Reproduction of tobacco mosaic virus in isolated rat liver mitochondria, DAN SSSR, 199, 944–947.

    CAS  Google Scholar 

  5. Zhdanov, V. M. (1972) Functioning of viral genome in isolated mitochondria, Vest. Akad. Med. Nauk, 27, 86–91.

    CAS  Google Scholar 

  6. Macho, A., Castedo, M., Marchetti, P., Aguilar, J. J., Decaudin, D., Zamzami, N., Girard, P. M., Uriel, J., and Kroemer, G. (1995) Mitochondrial dysfunctions in circulating T-lymphocytes from human immunodeficiency virus-1 carriers, Blood, 86, 2481–2487.

    CAS  PubMed  Google Scholar 

  7. Tollefson, A. E., Ryerse, J. S., Scaria, A., Hermiston, T. W., and Wold, W. S. (1996) The E3-11.6-kDa adenovirus death protein (ADP) is required for efficient cell death: characterization of cells infected with adp mutants, Virology, 220, 152–162.

    Article  CAS  PubMed  Google Scholar 

  8. Alandijany, T., Kammouni, W., Roy Chowdhury, S. K., Fernyhough, P., and Jackson, A. C. (2013) Mitochondrial dysfunction in rabies virus infection of neurons, J. Neurovirol., 19, 537–549.

    Article  CAS  PubMed  Google Scholar 

  9. Kruman, I. I., Nath, A., and Mattson, M. P. (1998) HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress, Exp. Neurol., 154, 276–288.

    Article  CAS  PubMed  Google Scholar 

  10. Lassoued, S., Ben Ameur, R., Ayadi, W., Gargouri, B., Ben Mansour, R., and Attia, H. (2008) Epstein–Barr virus induces an oxidative stress during the early stages of infection in B-lymphocytes, epithelial, and lymphoblastoid cell lines, Mol. Cell. Biochem., 313, 179–186.

    Article  CAS  PubMed  Google Scholar 

  11. Monne, M., Robinson, A. J., Boes, C., Harbour, M. E., Fearnley, I. M., and Kunji, E. R. S. (2007) The mimivirus genome encodes a mitochondrial carrier that transports dATP and dTTP, J. Virol., 81, 3181–3186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim, Y.-J., Jung, J. K., Lee, S. Y., and Jang, K. L. (2010) Hepatitis B virus X protein overcomes stress-induced premature senescence by repressing p16(INK4a) expression via DNA methylation, Cancer Lett., 288, 226–235.

    Article  CAS  PubMed  Google Scholar 

  13. Lund, K., and Ziola, B. (1985) Cell sonicates used in the analysis of how measles and herpes simplex type 1 virus infections influence Vero cell mitochondrial calcium uptake, Can. J. Biochem. Cell Biol., 63, 1194–1197.

    Article  CAS  PubMed  Google Scholar 

  14. Foti, M., Cartier, L., Piguet, V., Lew, D. P., Carpentier, J. L., Trono, D., and Krause, K. H. (1999) The HIV Nef protein alters Ca2+ signaling in myelomonocytic cells through SH3-mediated protein–protein interactions, J. Biol. Chem., 274, 34765–34772.

    Article  CAS  PubMed  Google Scholar 

  15. Campbell, R. V., Yang, Y., Wang, T., Rachamallu, A., Li, Y., Watowich, S. J., and Weinman, S. A. (2009) Chapter 20. Effects of hepatitis C core protein on mitochondrial electron transport and production of reactive oxygen species, Methods Enzymol., 456, 363–380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Diaz, Y., Chemello, M. E., Pena, F., Aristimuno, O. C., Zambrano, J. L., Rojas, H., Bartoli, F., Salazar, L., Chwetzoff, S., Sapin, C., Trugnan, G., Michelangeli, F., and Ruiz, M. C. (2008) Expression of nonstructural rotavirus protein NSP4 mimics Ca2+ homeostasis changes induced by rotavirus infection in cultured cells, J. Virol., 82, 11331–11343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Aldabe, R., Irurzun, A., and Carrasco, L. (1997) Poliovirus protein 2BC increases cytosolic free calcium concentrations, J. Virol., 71, 6214–6217.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Moise, A. R., Grant, J. R., Vitalis, T. Z., and Jefferies, W. A. (2002) Adenovirus E3-6.7K maintains calcium homeostasis and prevents apoptosis and arachidonic acid release, J. Virol., 76, 1578–1587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Van Kuppeveld, F. J. M., De Jong, A. S., Melchers, W. J., and Willems, P. H. (2005) Enterovirus protein 2B po(u)res out the calcium: a viral strategy to survive? Trends Microbiol., 13, 41–44.

    Article  PubMed  Google Scholar 

  20. Bozidis, P., Williamson, C. D., Wong, D. S., and ColbergPoley, A. M. (2010) Trafficking of UL37 proteins into mitochondrion-associated membranes during permissive human cytomegalovirus infection, J. Virol., 84, 7898–7903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. McGuire, K. A., Barlan, A. U., Griffin, T. M., and Wiethoff, C. M. (2011) Adenovirus type 5 rupture of lysosomes leads to cathepsin B-dependent mitochondrial stress and production of reactive oxygen species, J. Virol., 85, 10806–10813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nishina, S., Hino, K., Korenaga, M., Vecchi, C., Pietrangelo, A., Mizukami, Y., Furutani, T., Sakai, A., Okuda, M., Hidaka, I., Okita, K., and Sakaida, I. (2008) Hepatitis C virus-induced reactive oxygen species raise hepatic iron level in mice by reducing hepcidin transcription, Gastroenterology, 134, 226–238.

    Article  CAS  PubMed  Google Scholar 

  23. Gil, L., Tarinas, A., Hernandez, D., Riveron, B. V., Perez, D., Tapanes, R., Capo, V., and Perez, J. (2011) Altered oxidative stress indexes related to disease progression marker in human immunodeficiency virus infected patients with antiretroviral therapy, Biomed. Aging Pathol., 1, 8–15.

    Article  CAS  Google Scholar 

  24. Lassoued, S., Gargouri, B., El Feki Ael F., Attia, H., and Van Pelt, J. (2010) Transcription of the Epstein–Barr virus lytic cycle activator BZLF-1 during oxidative stress induction, Biol. Trace Elem. Res., 137, 13–22.

    Article  CAS  PubMed  Google Scholar 

  25. Hu, L., Chen, L., Yang, G., Li, L., Sun, H., Chang, Y., Tu, Q., Wu, M., and Wang, H. (2011) HBx sensitizes cells to oxidative stress-induced apoptosis by accelerating the loss of Mcl-1 protein via caspase-3 cascade, Mol. Cancer, 10, 43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Srisuttee, R., Koh, S. S., Park, E. H., Cho, I.-R., Min, H. J., Jhun, B. H., Yu, D.-Y., Park, S., Park, D. Y., Lee, M. O., Castrillon, D. H., Johnston, R. N., and Chung, Y.-H. (2011) Up-regulation of Foxo4 mediated by hepatitis B virus X protein confers resistance to oxidative stressinduced cell death, Int. J. Mol. Med., 28, 255–260.

    CAS  PubMed  Google Scholar 

  27. Ano, Y., Sakudo, A., Kimata, T., Uraki, R., Sugiura, K., and Onodera, T. (2010) Oxidative damage to neurons caused by the induction of microglial NADPH oxidase in encephalomyocarditis virus infection, Neurosci. Lett., 469, 39–43.

    Article  CAS  PubMed  Google Scholar 

  28. Gonzalez, M. E., and Carrasco, L. (2003) Viroporins, FEBS Lett., 552, 28–34.

    Article  CAS  PubMed  Google Scholar 

  29. Deniaud, A., Brenner, C., and Kroemer, G. (2004) Mitochondrial membrane permeabilization by HIV-1 Vpr, Mitochondrion, 4, 223–233.

    Article  CAS  PubMed  Google Scholar 

  30. Everett, H., Barry, M., Sun, X., Lee, S. F., Frantz, C., Berthiaume, L. G., McFadden, G., and Bleackley, R. C. (2002) The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore, J. Exp. Med., 196, 1127–1139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gibbs, J. S., Malide, D., Hornung, F., Bennink, J. R., and Yewdell, J. W. (2003) The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function, J. Virol., 77, 7214–7224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Biasiotto, R., Aguiari, P., Rizzuto, R., Pinton, P., D’ Agostino, D. M., and Ciminale, V. (2010) The p13 protein of human T-cell leukemia virus type 1 (HTLV-1) modulates mitochondrial membrane potential and calcium uptake, Biochim. Biophys. Acta, 1797, 945–951.

    Article  CAS  PubMed  Google Scholar 

  33. Nudson, W. A., Rovnak, J., Buechner, M., and Quackenbush, S. L. (2003) Walleye dermal sarcoma virus Orf C is targeted to the mitochondria, J. Gen. Virol., 84, 375–381.

    Article  CAS  PubMed  Google Scholar 

  34. Nieva, J. L., Agirre, A., Nir, S., and Carrasco, L. (2003) Mechanisms of membrane permeabilization by picornavirus 2B viroporin, FEBS Lett., 552, 68–73.

    Article  CAS  PubMed  Google Scholar 

  35. Matthews, D. A., and Russell, W. C. (1998) Adenovirus core protein V interacts with p32–a protein, which is associated with both the mitochondria and the nucleus, J. Gen. Virol., 79, 1677–1685.

    Article  CAS  PubMed  Google Scholar 

  36. Kaminska, M., Shalak, V., Francin, M., and Mirande, M. (2007) Viral hijacking of mitochondrial lysyl-tRNA synthetase, J. Virol., 81, 68–73.

    Article  CAS  PubMed  Google Scholar 

  37. Seo, J.-Y., Yaneva, R., Hinson, E. R., and Cresswell, P. (2011) Human cytomegalovirus directly induces the antiviral protein viperin to enhance infectivity, Science, 332, 1093–1097.

    Article  CAS  PubMed  Google Scholar 

  38. Kim, S., Kim, H.-Y., Lee, S., Kim, S. W., Sohn, S., Kim, K., and Cho, H. (2007) Hepatitis B virus X protein induces perinuclear mitochondrial clustering in microtubuleand dynein-dependent manners, J. Virol., 81, 1714–1726.

    Article  CAS  PubMed  Google Scholar 

  39. Nomura-Takigawa, Y., Nagano-Fujii, M., Deng, L., Kitazawa, S., Ishido, S., Sada, K., and Hotta, H. (2006) Non-structural protein 4A of hepatitis C virus accumulates on mitochondria and renders the cells prone to undergoing mitochondria-mediated apoptosis, J. Gen. Virol., 87, 1935–1945.

    Article  CAS  PubMed  Google Scholar 

  40. Radovanovic, J., Todorovic, V., Boricic, I., JankovicHladni, M., and Korac, A. (1999) Comparative ultrastructural studies on mitochondrial pathology in the liver of AIDS patients: clusters of mitochondria, protuberances, minimitochondria, vacuoles, and virus-like particles, Ultrastruct. Pathol., 23, 19–24.

    Article  CAS  PubMed  Google Scholar 

  41. Rojo, G., Chamorro, M., Salas, M. L., Vinuela, E., Cuezva, J. M., and Salas, J. (1998) Migration of mitochondria to viral assembly sites in African swine fever virusinfected cells, J. Virol., 72, 7583–7588.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Kelly, D. C. (1975) Frog virus 3 replication: electron microscope observations on the sequence of infection in chick embryo fibroblasts, J. Gen. Virol., 26, 71–86.

    Article  CAS  PubMed  Google Scholar 

  43. Kim, Y.-J., Jung, J. K., Lee, S. Y., and Jang, K. L. (2010) Hepatitis B virus X protein overcomes stress-induced premature senescence by repressing p16INK4a expression via DNA methylation, Cancer Lett., 288, 226–235.

    Article  CAS  PubMed  Google Scholar 

  44. Wiedmer, A., Wang, P., Zhou, J., Rennekamp, A. J., Tiranti, V., Zeviani, M., and Lieberman, P. M. (2008) Epstein–Barr virus immediate-early protein Zta co-opts mitochondrial single-stranded DNA binding protein to promote viral and inhibit mitochondrial DNA replication, J. Virol., 82, 4647–4655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Machida, K., Cheng, K. T.-H., Lai, C.-K., Jeng, K.-S., Sung, V. M.-H., and Lai, M. M. (2006) Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation, J. Virol., 80, 7199–7207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. De Mendoza, C., Martin-Carbonero, L., Barreiro, P., De Baar, M., Zahonero, N., Rodriguez-Novoa, S., Benito, J. M., Gonzalez-Lahoz, J., and Soriano, V. (2007) Mitochondrial DNA depletion in HIV-infected patients with chronic hepatitis C and effect of pegylated interferon plus ribavirin therapy, AIDS, 21, 583–588.

    Article  PubMed  Google Scholar 

  47. Saffran, H. A., Pare, J. M., Corcoran, J. A., Weller, S. K., and Smiley, J. R. (2007) Herpes simplex virus eliminates host mitochondrial DNA, EMBO Rep., 8, 188–193.

    Article  CAS  PubMed  Google Scholar 

  48. Koshiba, T. (2013) Mitochondrial-mediated antiviral immunity, Biochim. Biophys. Acta, 1833, 225–232.

    Article  CAS  PubMed  Google Scholar 

  49. Seth, R. B., Sun, L., Ea, C.-K., and Chen, Z. J. (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3, Cell, 122, 669–682.

    Article  CAS  PubMed  Google Scholar 

  50. Sun, Q., Sun, L., Liu, H.-H., Chen, X., Seth, R. B., Forman, J., and Chen, Z. J. (2006) The specific and essential role of MAVS in antiviral innate immune responses, Immunity, 24, 633–642.

    Article  CAS  PubMed  Google Scholar 

  51. Li, X.-D., Sun, L., Seth, R. B., Pineda, G., and Chen, Z. J. (2005) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity, Proc. Natl. Acad. Sci. USA, 102, 17717–17722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Yang, Y., Liang, Y., Qu, L., Chen, Z., Yi, M., Li, K., and Lemon, S. M. (2007) Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor, Proc. Natl. Acad. Sci. USA, 104, 7253–7258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Wei, C., Ni, C., Song, T., Liu, Y., Yang, X., Zheng, Z., Jia, Y., Yuan, Y., Guan, K., Xu, Y., Cheng, X., Zhang, Y., Yang, X., Wang, Y., Wen, C., Wu, Q., Shi, W., and Zhong, H. (2010) The hepatitis B virus X protein disrupts innate immunity by downregulating mitochondrial antiviral signaling protein, J. Immunol., 185, 1158–1168.

    Article  CAS  PubMed  Google Scholar 

  54. Castanier, C., Garcin, D., Vazquez, A., and Arnoult, D. (2010) Mitochondrial dynamics regulate the RIG-Ilike receptor antiviral pathway, EMBO Rep., 11, 133–138.

    Article  CAS  PubMed  Google Scholar 

  55. Koshiba, T., Yasukawa, K., Yanagi, Y., and Kawabata, S. (2011) Mitochondrial membrane potential is required for MAVS-mediated antiviral signaling, Sci. Signal., 4, ra7.

  56. Marraffini, L. A. (2015) CRISPR-Cas immunity in prokaryotes, Nature, 526, 55–61.

    Article  CAS  PubMed  Google Scholar 

  57. Bagasra, O., and Prilliman, K. R. (2004) RNA interference: the molecular immune system, J. Mol. Histol., 35, 545–553.

    CAS  PubMed  Google Scholar 

  58. Westra, E. R., Buckling, A., and Fineran, P. C. (2014) CRISPR-Cas systems: beyond adaptive immunity, Nat. Rev. Microbiol., 12, 317–326.

    Article  CAS  PubMed  Google Scholar 

  59. Jaag, H. M., Lu, Q., Schmitt, M. E., and Nagy, P. D. (2011) Role of RNase MRP in viral RNA degradation and RNA recombination, J. Virol., 85, 243–253.

    Article  CAS  PubMed  Google Scholar 

  60. Xia, C., Chen, Y.-C., Gong, H., Zeng, W., Vu, G.-P., Trang, P., Lu, S., Wu, J., and Liu, F. (2013) Inhibition of hepatitis B virus gene expression and replication by ribonuclease P, Mol. Ther., 21, 995–1003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Borralho, P. M., Rodrigues, C. M., and Steer, C. J. (2015) microRNAs in mitochondria: an unexplored niche, Adv. Exp. Med. Biol., 887, 31–51.

    Article  PubMed  Google Scholar 

  62. Mojica, F. J., Diez-Villasenor, C., Soria, E., and Juez, G. (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria, Mol. Microbiol., 36, 244–246.

    Article  CAS  Google Scholar 

  63. Voinnet, O. (2001) RNA silencing as a plant immune system against viruses, Trends Genet., 17, 449–459.

    Article  CAS  PubMed  Google Scholar 

  64. Kuzminova, A. E., Zhuravlyova, A. V., Vyssokikh, M. Yu., V., Zorova, L. D., Krasnikov, B. F., and Zorov, D. B. (1998) The permeability transition pore induced under anaerobic conditions in mitochondria energized with ATP, FEBS Lett., 434, 313–316.

    Article  CAS  PubMed  Google Scholar 

  65. Zorova, L. D., Krasnikov, B. F., Kuzminova, A. E., Polyakova, I. A., Dobrov, E. N., and Zorov, D. B. (2000) Virus-induced permeability transition in mitochondria, FEBS Lett., 466, 305–309.

    Article  CAS  PubMed  Google Scholar 

  66. Edgar, R. C. (2007) PILER-CR: fast and accurate identification of CRISPR repeats, BMC Bioinformatics, 8, 18.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Rice, P., Longden, I., and Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite, Trends Genet., 16, 276–277.

    Article  CAS  PubMed  Google Scholar 

  68. Rahmani, Z., Huh, K. W., Lasher, R., and Siddiqui, A. (2000) Hepatitis B virus X protein colocalizes to mitochondria with a human voltage-dependent anion channel, HVDAC3, and alters its transmembrane potential, J. Virol., 74, 2840–2846.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zorov, D. B. (1996) Mitochondrial transport of nucleic acids. Involvement of the benzodiazepine receptor, Biochemistry (Moscow), 61, 939–946.

    Google Scholar 

  70. Zorov, D. B. (1996) Mitochondrial damage as a source of diseases and aging: a strategy of how to fight these, Biochim. Biophys. Acta, 1275, 10–15.

    Article  PubMed  Google Scholar 

  71. Simon, L. D., and Anderson, T. F. (1967) The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration, Virology, 32, 279–297.

    Article  CAS  PubMed  Google Scholar 

  72. Harrison, B. D., and Roberts, I. M. (1968) Association of tobacco rattle virus with mitochondria, J. Gen. Virol., 3, 121–124.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. A. Popkov, D. N. Silachev, S. S. Jankauskas, V. A. Babenko, I. B. Pevzner, E. Y. Plotnikov & D. B. Zorov

  2. Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. A. Popkov, V. A. Babenko, T. I. Danilina & S. D. Zorov

  3. International Laser Research Center, Lomonosov Moscow State University, 119991, Moscow, Russia

    L. D. Zorova

  4. Moscow Institute of Physics and Technology, 141701, Dolgoprudny, Russia

    I. O. Korvigo

Authors
  1. V. A. Popkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. D. Zorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. O. Korvigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. N. Silachev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. S. Jankauskas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. A. Babenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. B. Pevzner
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. T. I. Danilina
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. D. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. E. Y. Plotnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. D. B. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. B. Zorov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popkov, V.A., Zorova, L.D., Korvigo, I.O. et al. Do mitochondria have an immune system?. Biochemistry Moscow 81, 1229–1236 (2016). https://doi.org/10.1134/S0006297916100217

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297916100217

Key words

Search

Navigation