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Biological Diversity and Remodeling of Cardiolipin in Oxidative Stress and Age-Related Pathologies

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Abstract

Age-related dysfunctions are accompanied by impairments in the mitochondrial morphology, activity of signaling pathway, and protein interactions. Cardiolipin is one of the most important phospholipids that maintains the curvature of the cristae and facilitates assembly and interaction of complexes and supercomplexes of the mitochondrial respiratory chain. The fatty acid composition of cardiolipin influences the biophysical properties of the membrane and, therefore, is crucial for the mitochondrial bioenergetics. The presence of unsaturated fatty acids in cardiolipin is the reason of its susceptibility to oxidative damage. Damaged cardiolipin undergoes remodeling by phospholipases, acyltransferases, and transacylases, creating a highly specific fatty acyl profile for each tissue. In this review, we discuss the variability of cardio-lipin fatty acid composition in various species and different tissues of the same species, both in the norm and at various pathologies (e.g., age-related diseases, oxidative and traumatic stresses, knockouts/knockdowns of enzymes of the cardio-lipin synthesis pathway). Progressive pathologies, including age-related ones, are accompanied by cardiolipin depletion and decrease in the efficiency of its remodeling, as well as the activation of an alternative way of pathological remodeling, which causes replacement of cardiolipin fatty acids with polyunsaturated ones (e.g., arachidonic or docosahexaenoic acids). Drugs or special diet can contribute to the partial restoration of the cardiolipin acyl profile to the one rich in fatty acids characteristic of an intact organ or tissue, thereby correcting the consequences of pathological or insufficient cardiolipin remodeling. In this regard, an urgent task of biomedicine is to study the mechanism of action of mitochondria-targeted antioxi-dants effective in the treatment of age-related pathologies and capable of accumulating not only in vitro, but also in vivo in the cardiolipin-enriched membrane fragments.

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Abbreviations

BTHS:

Barth syndrome

CL:

cardiolipin

DHA:

docosahexaenoic acid

FA:

fatty acid

MLCAT:

monolysocar-diolipin acyltransferase

MLCL:

monolysocardiolipin

PUFA:

polyunsaturated fatty acid

ROS:

reactive oxygen species

TAZ :

tafazzin gene

TLCL:

tetralinoleoylcardiolipin

TPP:

triphenyl-alkylphosphonium

References

  1. Feniouk, B. A., and Skulachev, V. P. (2017) Cellular and molecular mechanisms of action of mitochondria-targeted antioxidants, Curr. Aging. Sci., 10, 41–48, doi: 10.2174/ 1874609809666160921113706.

    Article  CAS  PubMed  Google Scholar 

  2. Skulachev, V. P., Anisimov, V. N., Antonenko, Y. N., Bakeeva, L. E., Chernyak, B. V., Erichev, V. P., Filenko, O. F., Kalinina, N. I., Kapelko, V. I., Kolosova, N. G., Kopnin, B. P., Korshunova, G. A., Lichinitser, M. R., Obukhova, L. A., Pasyukova, E. G., Pisarenko, O. I., Roginsky, V. A., Ruuge, E. K., Senin, I. I., Severina, I. I., Skulachev, M. V., Spivak, I. M., Tashlitsky, V. N., Tkachuk, V. A., Vyssokikh, M. Y., Yaguzhinsky, L. S., and Zorov, D. B. (2009) An attempt to prevent senescence: a mitochon-drial approach, Biochim. Biophys. Acta, 1787, 437–461, doi: 10.1016/j.bbabio.2008.12.008.

    Article  CAS  PubMed  Google Scholar 

  3. Ames, B. N., Shigenaga, M. K., and Hagen, T. M. (1995) Mitochondrial decay in aging, Biochim. Biophys. Acta, 1271, 165–170, doi: 10.1016/0925-4439(95)00024-x.

    Article  PubMed  Google Scholar 

  4. Kagan, V. E., Chu, C. T., Tyurina, Y. Y., Cheikhi, A., and Bayir, H. (2014) Cardiolipin asymmetry, oxidation and sig-naling, Chem. Phys. Lipids, 179, 64–69, doi: 10.1016/j.chemphyslip.2013.11.010.

    Article  CAS  PubMed  Google Scholar 

  5. Kagan, V. E., Tyurina, Y. Y., Tyurin, V. A., Mohammadyani, D., Angeli, J. P., Baranov, S. V., Klein-Seetharaman, J., Friedlander, R. M., Mallampalli, R. K., Conrad, M., and Bayir, H. (2015) Cardiolipin signaling mechanisms: collapse of asymmetry and oxidation, Antioxid. Redox Signal., 22, 1667–1680, doi: 10.1089/ars.2014.6219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Von Zglinicki, T. (1987) A mitochondrial membrane hypothesis of aging, J. Theor. Biol., 127, 127–132, doi: 10.1016/S0022-5193(87)80123-6.

    Article  Google Scholar 

  7. Ye, C., Shen, Z., and Greenberg, M. L. (2016) Cardiolipin remodeling: a regulatory hub for modulating cardiolipin metabolism and function, J. Bioenerg. Biomembr., 48, 113–123, doi: 10.1007/s10863-014-9591-7.

    Article  CAS  PubMed  Google Scholar 

  8. Laganiere, S., and Yu, B. P. (1993) Modulation of membrane phospholipid fatty acid composition by age and food restriction, Gerontology, 39, 7–18, doi: 10.1159/000213509.

    Article  CAS  PubMed  Google Scholar 

  9. Tyurina, Y. Y., Tyurin, V. A., Epperly, M. W., Greenberger, J. S., and Kagan, V. E. (2008) Oxidative lipidomics of gamma-irradiation-induced intestinal injury, Free Radic. Biol. Med., 44, 299–314, doi: 10.1016/j.freeradbiomed. 2007.08.021.

    Article  CAS  PubMed  Google Scholar 

  10. Tyurina, Y. Y., Tyurin, V. A., Kapralova, V. I., Amoscato, A. A., Epperly, M. W., Greenberger, J. S., and Kagan, V. E. (2009) Mass-spectrometric characterization of phospho-lipids and their hydroperoxide derivatives in vivo: effects of total body irradiation, Methods Mol. Biol., 580, 153–183, doi: 10.1007/978-1-60761-325-1_9.

    CAS  PubMed  Google Scholar 

  11. Tyurina, Y. Y., Tyurin, V. A., Kaynar, A. M., Kapralova, V. I., Wasserloos, K., Li, J., Mosher, M., Wright, L., Wipf, P., Watkins, S., Pitt, B. R., and Kagan, V. E. (2010) Oxidative lipidomics of hyperoxic acute lung injury: mass spectromet-ric characterization of cardiolipin and phosphatidylserine peroxidation, Am. J. Physiol. Lung Cell. Mol. Physiol., 299, 73–85, doi: 10.1152/ajplung.00035.2010.

    Article  CAS  Google Scholar 

  12. Mileykovskaya, E., Zhang, M., and Dowhan, W. (2005) Cardiolipin in energy transducing membranes, Biochemistry (Moscow), 70, 154–158, doi: 10.1007/s10541-005-0095-2.

    Article  CAS  Google Scholar 

  13. Schlame, M. (2008) Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes, J. Lipid Res., 49, 1607–1620, doi: 10.1194/jlr.R700018-JLR200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Corcelli, A. (2009) The cardiolipin analogues of Archaea, Biochim. Biophys. Acta, 1788, 2101–2106, doi: 10.1016/j.bbamem.2009.05.010.

    Article  CAS  PubMed  Google Scholar 

  15. Xu, Y., Sutachan, J. J., Plesken, H., Kelley, R. I., and Schlame, M. (2005) Characterization of lymphoblast mito-chondria from patients with Barth syndrome, Lab. Invest., 85, 823–830, doi: 10.1038/labinvest.3700274.

    Article  CAS  PubMed  Google Scholar 

  16. Acehan, D., Khuchua, Z., Houtkooper, R. H., Malhotra, A., Kaufman, J., Vaz, F. M., Ren, M., Rockman, H. A., Stokes, D. L., and Schlame, M. (2009) Distinct effects of tafazzin deletion in differentiated and undifferentiated mitochondria, Mitochondrion, 9, 86–95, doi: 10.1016/ j.mito.2008.12.001.

    Article  CAS  PubMed  Google Scholar 

  17. Xu, F. Y., McBride, H., Acehan, D., Vaz, F. M., Houtkooper, R. H., Lee, R. M., Mowat, M. A., and Hatch, G. M. (2010) The dynamics of cardiolipin synthesis post-mitochondrial fusion, Biochim. Biophys. Acta, 1798, 1577–1585, doi: 10.1016/j.bbamem.2010.04.007.

    Article  CAS  PubMed  Google Scholar 

  18. Claypool, S. M., Oktay, Y., Boontheung, P., Loo, J. A., and Koehler, C. M. (2008) Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane, J. Cell. Biol., 182, 937–950, doi: 10.1083/jcb.200801152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mileykovskaya, E., and Dowhan, W. (2014) Cardiolipin-dependent formation of mitochondrial respiratory super-complexes, Chem. Phys. Lipids, 179, 42–48, doi: 10.1016/ j.chemphyslip.2013.10.012.

    Article  CAS  PubMed  Google Scholar 

  20. Paradies, G., Paradies, V., Ruggiero, F. M., and Petrosillo, G. (2014) Cardiolipin and mitochondrial function in health and disease, Antioxid. Redox Signal., 20, 1925–1953, doi: 10.1089/ars.2013.5280.

    Article  CAS  PubMed  Google Scholar 

  21. Gebert, N., Joshi, A. S., Kutik, S., Becker, T., McKenzie, M., Guan, X. L., Mooga, V. P., Stroud, D. A., Kulkarni, G., Wenk, M. R., Rehling, P., Meisinger, C., Ryan, M. T., Wiedemann, N., Greenberg, M. L., and Pfanne, N. (2009) Mitochondrial cardiolipin involved in outer-membrane protein biogenesis: implications for Barth syndrome, Curr. Biol., 19, 2133–2139, doi: 10.1016/j.cub.2009.10.074.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Patil, V. A., Fox, J. L., Gohil, V. M., Winge, D. R., and Greenberg, M. L. (2013) Loss of cardiolipin leads to pertur-bation of mitochondrial and cellular iron homeostasis, J. Biol. Chem., 288, 1696–1705, doi: 10.1074/jbc.M112.428938.

    Article  CAS  PubMed  Google Scholar 

  23. Joshi, A. S., Zhou, J., Gohil, V. M., Chen, S., and Greenberg, M. L. (2009) Cellular functions of cardiolipin in yeast, Biochim. Biophys. Acta, 1793, 212–218, doi: 10.1016/j.bbamcr.2008.07.024.

    Article  CAS  PubMed  Google Scholar 

  24. Houtkooper, R. H., and Vaz, F. M. (2008) Cardiolipin, the heart of mitochondrial metabolism, Cell. Mol. Life Sci., 65, 2493–2506, doi: 10.1007/s00018-008-8030-5.

    Article  CAS  PubMed  Google Scholar 

  25. Cogliati, S., Frezza, C., Soriano, M. E., Varanita, T., Quintana-Cabrera, R., Corrado, M., Cipolat, S., Costa, V., Casarin, A., Gomes, L. C., Perales-Clemente, E., Salviati, L., Fernandez-Silva, P., Enriquez, J. A., and Scorrano, L. (2013) Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency, Cell, 155, 160–171, doi: 10.1016/j.cell.2013.08.032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Schlame, M. (2013) Cardiolipin remodeling and the function of tafazzin, Biochim. Biophys. Acta, 1831, 582–588, doi: 10.1016/j.bbalip.2012.11.007.

    Article  CAS  PubMed  Google Scholar 

  27. Kagan, V. E., Jiang, J., Huang, Z., Tyurina, Y. Y., Desbourdes, C., Cottet-Rousselle, C., Dar, H. H., Verma, M., Tyurin, V. A., Kapralov, A. A., Cheikhi, A., Mao, G., Stolz, D., St. Croix, C. M., Watkins, S., Shen, Z., Li, Y., Greenberg, M. L., Tokarska-Schlattner, M., Boissan, M., Lacombe, M. L., Epand, R. M., Chu, C. T., Mallampalli, R. K., Bayir, H., and Schlattner, U. (2016) NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy, Cell Death Differ., 23, 1140–1151, doi: 10.1038/cdd.2015.160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chu, C. T., Bayir, H., and Kagan, V. E. (2014) LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons: implications for Parkinson disease, Autophagy, 10, 376–378, doi: 10.4161/auto.27191.

    Article  CAS  PubMed  Google Scholar 

  29. Mulkidjanian, A. Y., Shalaeva, D. N., Lyamzaev, K. G., and Chernyak, B. V. (2018) Does oxidation of mitochon-drial cardiolipin trigger a chain of antiapoptotic reactions? Biochemistry (Moscow), 83, 1263–1278, doi: 10.1134/ S0006297918100115.

    Article  CAS  Google Scholar 

  30. Petrosillo, G., Casanova, G., Matera, M., Ruggiero, F. M., and Paradies, G. (2006) Interaction of peroxidized cardio-lipin with rat heart mitochondrial membranes: induction of permeability transition and cytochrome c release, FEBS Lett., 580, 6311–6316, doi: 10.1016/j.febslet.2006.10.036.

    Article  CAS  PubMed  Google Scholar 

  31. Wang, Z., Ying, Z., Bosy-Westphal, A., Zhang, J., Schautz, B., Later, W., Heymsfield, S. B., and Muller, M. J. (2010) Specific metabolic rates of major organs and tissues across adulthood: evaluation by mechanistic model of resting energy expenditure, Am. J. Clin. Nutr., 92, 1369–1377, doi: 10.3945/ajcn.2010.29885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Rocquelin, G., Guenot, L., Astorg, P. O., and David, M. (1989) Phospholipid content and fatty acid composition of human heart, Lipids, 24, 775–780, doi: 10.1007/ bf02544583.

    Article  CAS  PubMed  Google Scholar 

  33. Ristic, V., Tepsic, V., De Luka, S. R., and Vrbaski, S. R. (1998) Phospholipid content and fatty acid composition in the rat heart after chronic diazepam treatment, Physiol. Res., 47, 115–118.

    CAS  PubMed  Google Scholar 

  34. Tepsic, V., Ristic, V., Ristic, D., Vasiljevic, N., and Pecelj-Gec, M. (1998) Heart phospholipid content and fatty acid composition in the rat after feeding different lipid supple-mented diets, Physiol. Res., 47, 413–418.

    CAS  PubMed  Google Scholar 

  35. Schlame, M., Ren, M., Xu, Y., Greenberg, M. L., and Haller, I. (2005) Molecular symmetry in mitochondrial cardiolipins, Chem. Phys. Lipids, 138, 38–49, doi: 10.1016/j.chemphyslip.2005.08.002.

    Article  CAS  PubMed  Google Scholar 

  36. Claypool, S. M., and Koehler, C. M. (2012) The complexity of cardiolipin in health and disease, Trends Biochem. Sci., 37, 32–41, doi: 10.1016/j.tibs.2011.09.003.

    Article  CAS  PubMed  Google Scholar 

  37. Saric, A., Andreau, K., Armand, A S., Moller, I. M., and Petit, P. X. (2016) Barth syndrome: from mitochondrial dysfunctions associated with aberrant production of reactive oxygen species to pluripotent stem cell studies, Front. Genet., 6, 359, doi: 10.3389/fgene.2015.00359.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Shen, Z., Ye, C., McCain, K., and Greenberg, M. L. (2015) The role of cardiolipin in cardiovascular health, Biomed. Res. Int., 2015, 891707, doi: 10.1155/2015/ 891707.

    Google Scholar 

  39. Maguire, J. J., Tyurina, Y. Y, Mohammadyani, D., Kapralov, A. A, Anthonymuthu, T. S., Qu, F., Amoscato, A. A., Sparvero, L. J., Tyurin, V. A., Planas-Iglesias, J., He, R. R., Klein-Seetharaman, J., Bayir, H., and Kagan, V. E. (2017) Known unknowns of cardiolipin signaling: the best is yet to come, Biochim. Biophys. Acta Mol. Cell. Biol. Lipids, 1862, 8–24, doi: 10.1016/j.bbalip.2016.08.001.

    Article  CAS  PubMed  Google Scholar 

  40. Guan, Z. Z., Soderberg, M., Sindelar, P., and Edlund, C. (1994) Content and fatty acid composition of cardiolipin in the brain of patients with Alzheimer’s disease, Neurochem. Int., 25, 295–300, doi: 10.1016/0197-0186(94)90073-6.

    Article  CAS  PubMed  Google Scholar 

  41. Divakaran, P., and Venkataraman, A. (1977) Effect of dietary fats on oxidative phosphorylation and fatty acid profile of rat liver mitochondria, J. Nutr., 107, 1621–1631, doi: 10.1093/jn/107.9.1621.

    Article  CAS  PubMed  Google Scholar 

  42. Kraffe, E., Soudant, P., Marty, Y., Kervarec, N., and Jehan, P. (2002) Evidence of a tetradocosahexaenoic cardiolipin in some marine bivalves, Lipids, 37, 507–514, doi: 10.1007/s11745-002-0925-z.

    Article  CAS  PubMed  Google Scholar 

  43. Kraffe, E., Soudant, P., Marty, Y., and Kervarec, N. (2005) Docosahexaenoic acid- and eicosapentaenoic acid-enriched cardiolipin in the Manila clam. Ruditapes philippinarum, Lipids, 40, 619–625, doi: 10.1007/s11745-005-1423-z.

    Article  CAS  PubMed  Google Scholar 

  44. Fajardo, V. A., Mikhaeil, J. S., Leveille, C. F., Saint, C., and LeBlanc, P. J. (2017) Cardiolipin content, linoleic acid composition, and tafazzin expression in response to skeletal muscle overload and unload stimuli, Sci Rep., 7, 2060, doi: 10.1038/s41598-017-02089-1.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Diagne, A., Fauvel, J., Record, M., Chap, H., and Douste-Blazy L. (1984) Studies on ether phospholipids. II. Comparative composition of various tissues from human, rat and guinea pig, Biochim. Biophys. Acta, 793, 221–231, doi: 10.1016/0005-2760(84)90324-2.

    Article  CAS  PubMed  Google Scholar 

  46. Courtade, S., Marinetti, G. V., and Stotz, E. (1967) The struc-ture and abundance of rat tissue cardiolipins, Biochim. Biophys. Acta, 137, 121–134, doi: 10.1016/0005-2760(67)90015-x.

    Article  CAS  PubMed  Google Scholar 

  47. Sparagna, G. C., and Lesnefsky E. J. (2009) Cardiolipin remodeling in the heart, J. Cardiovasc. Pharmacol., 53, 290–301, doi: 10.1097/FJC.0b013e31819b5461.

    Article  CAS  PubMed  Google Scholar 

  48. Lee, H., Mayette, J., Rapoport, S. I., and Bazinet, R. P. (2006) Selective remodeling of cardiolipin fatty acids in the aged rat heart, Lipids Health Dis., 5, 2, doi: 10.1186/1476-511X-5-2.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Schlame, M., and Otten, D. (1991) Analysis of cardiolipin molecular species by high-performance liquid chromatography of its derivative 1,3-bisphosphatidyl-2-benzoyl-sn-glyceroldimethyl ester, Anal. Biochem., 195, 290–295, doi: 10.1016/0003-2697(91)90332-n.

    Article  CAS  PubMed  Google Scholar 

  50. Han, X., Yang, K., Yang, J., Cheng, H., and Gross, R. W (2006) Shotgun lipidomics of cardiolipin molecular species in lipid extracts of biological samples, J. Lipid Res., 47, 864–879, doi: 10.1194/jlr.D500044-JLR200.

    Article  CAS  PubMed  Google Scholar 

  51. Portero-Otin, M., Bellmunt, M. J., Ruiz, M. C., Barja, G., and Pamplona, R. (2001) Correlation of fatty acid unsaturation of the major liver mitochondrial phospholipid classes in mammals to their maximum life span potential, Lipids, 36, 491–498, doi: 10.1007/s11745-001-0748-y.

    Article  CAS  PubMed  Google Scholar 

  52. Wang, H. Y., Jackson, S. N., and Woods, A. S. (2007) Direct MALDI-MS analysis of cardiolipin from rat organs sections, J. Am. Soc. Mass Spectrom., 18, 567–577, doi: 10.1016/j.jasms.2006.10.023.

    Article  CAS  PubMed  Google Scholar 

  53. Xu, Y., Malhotra, A., Ren, M., and Schlame, M. (2006) The enzymatic function of tafazzin, J. Biol. Chem., 281, 39217–39224, doi: 10.1074/jbc.M606100200.

    Article  CAS  PubMed  Google Scholar 

  54. Chicco, A. J., Sparagna, G. C., McCune, S. A., Johnson, C. A., Murphy, R. C., Bolden, D. A., Rees, M. L., Gardner, R. T., and Moore, R. L. (2008) Linoleate-rich high-fat diet decreases mortality in hypertensive heart failure rats com-pared with lard and low-fat diets, Hypertension, 52, 549–555, doi: 10.1161/HYPERTENSIONAHA.108.114264.

    Article  CAS  PubMed  Google Scholar 

  55. He, Q., and Han, X. (2014) Cardiolipin remodeling in diabetic heart, Chem. Phys. Lipids, 179, 75–81, doi: 10.1016/j.chemphyslip.2013.10.007.

    Article  CAS  PubMed  Google Scholar 

  56. Wahjudi, P. N., Yee, J. K., Martinez, S. R., Zhang, J., Teitell, M., Nikolaenko, L., Swerdloff, R., Wang, C., and Lee, W. N. (2011) Turnover of nonessential fatty acids in cardiolipin from the rat heart, J. Lipid Res., 52, 2226–2233, doi: 10.1194/jlr.M015966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Bayir, H., Tyurin, V. A., Tyurina, Y. Y., Viner, R., Ritov, V., Amoscato, A. A., Zhao, Q., Zhang, X. J., Janesko-Feldman, K. L., Alexander, H., Basova, L. V., Clark, R. S., Kochanek, P. M., and Kagan, V. E. (2007) Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis, Ann. Neurol., 62, 154–169, doi: 10.1002/ana.21168.

    Article  CAS  PubMed  Google Scholar 

  58. Cheng, H., Mancuso, D. J., Jiang, X., Guan, S., Yang, J., Yang, K., Sun, G., Gross, R. W., and Han, X. (2008) Shotgun lipidomics reveals the temporally dependent, highly diversified cardiolipin profile in the mammalian brain: temporally coordinated postnatal diversification of cardiolipin molecular species with neuronal remodeling, Biochemistry, 47, 5869–5880, doi: 10.1021/bi7023282.

    Article  CAS  PubMed  Google Scholar 

  59. Ji, J., Kline, A. E., Amoscato, A., Samhan-Arias, A. K., Sparvero, L. J., Tyurin, V. A., Tyurina, Y. Y., Fink, B., Manole, M. D., Puccio, A. M., Okonkwo, D. O., Cheng, J. P., Alexander, H., Clark, R. S., Kochanek, P. M., Wipf, P., Kagan, V. E., and Bayir, H. (2012) Lipidomics identifies cardiolipin oxidation as a mitochondrial target for redox therapy of brain injury, Nat. Neurosci., 15, 1407–1413, doi: 10.1038/nn.3195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kiebish, M. A., Han, X., Cheng, H., Chuang, J. H., and Seyfried, T. N. (2008) Cardiolipin and electron transport chain abnormalities in mouse brain tumor mitochondria: lipidomic evidence supporting the Warburg theory of cancer, J. Lipid Res., 49, 2545–2556, doi: 10.1194/jlr.M800319-JLR200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Yabuuchi, H., and O’Brien, J. (1968) Brain cardiolipin: isolation and fatty acid positions, J. Neurochem., 15, 1383–1390, doi: 10.1111/j.1471-4159.1968.tb05920.x.

    Article  CAS  PubMed  Google Scholar 

  62. Li, J., Romestaing, C., Han, X., Li, Y., Hao, X., Wu, Y., Sun, C., Liu, X., Jefferson, L. S., Xiong, J., Lanoue, K. F., Chang, Z., Lynch, C. J., Wang, H., and Shi, Y. (2010) Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity, Cell Metab., 12, 154–165, doi: 10.1016/j.cmet.2010.07.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Maddalena, L. A., Ghelfi, M., Atkinson, J., and Stuart, J. A. (2017) The mitochondria-targeted imidazole substituted oleic acid ‘TPP-IOA’ affects mitochondrial bioenergetics and its protective efficacy in cells is influenced by cellular dependence on aerobic metabolism, Biochim. Biophys. Acta, 1858, 73–85, doi: 10.1016/j.bbabio.2016.11.005.

    Article  CAS  Google Scholar 

  64. Daiyasu, H., Kuma, K., Yokoi, T., Morii, H., Koga, Y., and Toh, H. (2005) A study of archaeal enzymes involved in polar lipid synthesis linking amino acid sequence information, genomic contexts and lipid composition, Archaea, 1, 399–410, doi: 10.1155/2005/452563.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gu, Z., Valianpou, F., Chen, S., Vaz, F. M., Hakkaart, G. A., Wanders, R. J., and Greenberg, M. L. (2004) Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome, Mol. Microbiol., 51, 149–158, doi: 10.1046/j.1365-2958.2003.03802.x.

    Article  CAS  PubMed  Google Scholar 

  66. Cao, J., Liu, Y., Lockwood, J., Burn, P., and Shi, Y. (2004) A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA: lysocardiolipin acyltransferase (ALCAT1) in mouse, J. Biol. Chem., 279, 31727–31734, doi: 10.1074/jbc.M402930200.

    Article  CAS  PubMed  Google Scholar 

  67. Ren, M., Phoon, C. K., and Schlame, M. (2014) Metabolism and function of mitochondrial cardiolipin, Prog. Lipid Res., 55, 1–16, doi: 10.1016/j.plipres.2014.04.001.

    Article  CAS  PubMed  Google Scholar 

  68. Sullivan, E. M., Pennington, E. R., Sparagna, G. C., Torres, M. J., Neufer, P. D., Harris, M., Washington, J., Anderson, E. J., Zeczycki, T. N., Brown, D. A., and Shaikh, S. R. (2018) Docosahexaenoic acid lowers cardiac mitochondrial enzyme activity by replacing linoleic acid in the phospholipidome, J. Biol. Chem., 293, 466–483, doi: 10.1074/jbc.M117.812834.

    Article  CAS  PubMed  Google Scholar 

  69. Barth, P. G., Scholte, H. R., Berden, J. A., Van der Klei-Van Moorsel, J. M., Luyt-Houwen, I. E., Van’t Veer-Korthof, E. T., Van der Harten, J. J., and Sobotka-Plojhar, M. A. (1983) An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes, J. Neurol. Sci., 62, 327–355, doi: 10.1016/0022-510x(83)90209-5.

    Article  CAS  PubMed  Google Scholar 

  70. Bione, S., D’Adamo, P., Maestrini, E., Gedeon, A. K., Bolhuis, P. A., and Toniolo, D. (1996) A novel X-linked gene, G4.5, is responsible for Barth syndrome, Nat. Genet., 12, 385–389, doi: 10.1038/ng0496-385.

    Article  CAS  PubMed  Google Scholar 

  71. Schlame, M., Kelley, R. I., Feigenbaum, A., Towbin, J. A., Heerdt, P. M., Schieble, T., Wanders, R. J. A., DiMauro, S., and Blanck, T. J. J. (2003) Phospholipid abnormalities in children with Barth syndrome, J. Am. Coll. Cardiol., 42, 1994–1999, doi: 10.1016/j.jacc.2003.06.015.

    Article  CAS  PubMed  Google Scholar 

  72. Vreken, P., Valianpour, F., Nijtmans, L. G., Grivell, L. A., Plecko, B., Wanders, R. J., and Barth, P. G. (2000) Defective remodeling of cardiolipin and phosphatidylglyc-erol in Barth syndrome, Biochem. Biophys. Res. Commun., 279, 378–382, doi: 10.1006/bbrc.2000.3952.

    Article  CAS  PubMed  Google Scholar 

  73. Acehan, D., Vaz, F., Houtkooper, R. H., James, J., Moore, V., Tokunaga, C., Kulik, W., Wansapura, J., Toth, M. J., Strauss, A., and Khuchua, Z. (2011) Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome, J. Biol. Chem., 286, 899–908, doi: 10.1074/ jbc.M110.171439.

    Article  CAS  PubMed  Google Scholar 

  74. Shilovsky, G. A., Zverkov, O. A., Seliverstov, A. V., Ashapkin, V. V., Putyatina, T. S., Rubanov, L. I., and Lyubetsky, V. A. (2019) New C-terminal conserved regions of tafazzin, a catalyst of cardiolipin remodeling, Oxid. Med. Cell. Longev., 2019, 2901057, doi: 10.1155/2019/2901057.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Tocchi, A., Quarles, E. K., Basisty, N., Gitari, L., and Rabinovitch, P. S. (2015) Mitochondrial dysfunction in cardiac aging, Biochim. Biophys. Acta, 1847, 1424–1433, doi: 10.1016/j.bbabio.2015.07.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Kirwin, S. M., Manolakos, A., Barnett, S. S., and Gonzalez, I. L. (2014) Tafazzin splice variants and mutations in Barth syndrome, Mol. Genet. Metab., 111, 26–32, doi: 10.1016/j.ymgme.2013.11.006.

    Article  CAS  PubMed  Google Scholar 

  77. Xu, Y., Zhang, S., Malhotra, A., Edelman-Novemsky, I., Ma, J., Kruppa, A., Cernicica, C., Blais, S., Neubert, T. A., Ren, M., and Schlame, M. (2009) Characterization of tafazzin splice variants from humans and fruit flies, J. Biol. Chem., 284, 29230–29239, doi: 10.1074/jbc.M109.016642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Ronvelia, D., Greenwood, J., Platt, J., Hakim, S., and Zaragoza, M. V. (2012) Intrafamilial variability for novel TAZ gene mutation: Barth syndrome with dilated car-diomyopathy and heart failure in an infant and left ventricular noncompaction in his great-uncle, Mol. Genet. Metab., 107, 428–432, doi: 10.1016/j.ymgme.2012.09.013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Acehan, D., Xu, Y., Stokes, D. L., and Schlame, M. (2007) Comparison of lymphoblast mitochondria from normal subjects and patients with Barth syndrome using electron microscopic tomography, Lab. Invest., 87, 40–48, doi: 10.1038/labinvest.3700480.

    Article  CAS  PubMed  Google Scholar 

  80. Bissler, J. J., Tsorads, M., Goring, H. H., Hug, P., Chuck, G., Tombragel, E., McGraw, C., Schlotman, J., Ralston, M. A., and Hug, G. (2002) Infantile dilated X-linked car-diomyopathy, G4.5 mutations, altered lipids, and ultra-structural malformations of mitochondria in heart, liver, and skeletal muscle, Lab. Invest., 82, 335–344, doi: 10.1038/labinvest.3780427.

    Article  CAS  PubMed  Google Scholar 

  81. Huang, Y., Powers, C., Madala, S. K., Greis, K. D., Haffey, W. D., Towbin, J. A., Purevjav, E., Javadov, S., Strauss, A. W., and Khuchua, Z. (2015) Cardiac metabolic pathways affected in the mouse model of Barth syndrome, PLoS One, 10, e0128561, doi: 10.1371/journal.pone.0128561.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Kiebish, M. A., Yang, K., Liu, X., Mancuso, D. J., Guan, S., Zhao, Z., Sims, H. F., Cerqua, R., Cade, W. T., Han, X., and Gross, R. W. (2013) Dysfunctional cardiac mitochon-drial bioenergetic, lipidomic, and signaling in a murine model of Barth syndrome, J. Lipid Res., 54, 1312–1325, doi: 10.1194/jlr.M034728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Gawrisch, K. (2012) Tafazzin senses curvature, Nat. Chem. Biol., 8, 811–812, doi: 10.1038/nchembio.1068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Chicco, A. J., and Sparagna, G. C. (2007) Role of cardio-lipin alterations in mitochondrial dysfunction and disease, Am. J. Physiol., 292, 33–44, doi: 10.1152/ajpcell.00243.2006.

    Article  CAS  Google Scholar 

  85. Han, X., Yang, J., Yang, K., Zhao, Z., Abendschein, D. R., and Gross, R. W. (2007) Alterations in myocardial cardio-lipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study, Biochemistry, 46, 6417–6428, doi: 10.1021/bi7004015.

    Article  CAS  PubMed  Google Scholar 

  86. Sparagna, G. C., Chicco, A. J., Murphy, R. C., Bristow, M. R., Johnson, C. A., Rees, M. L., Maxey, M. L., McCune, S. A., and Moore, R. L. (2007) Loss of cardiac tetralinoleoyl-cardiolipin in human and experimental heart failure, J. Lipid Res., 48, 1559–1570, doi: 10.1194/jlr.M600551-JLR200.

    Article  CAS  PubMed  Google Scholar 

  87. Almaida-Pagan, P. F., Lucas-Sanchez, A., and Tocher, D. R. (2014) Changes in mitochondrial membrane composition and oxidative status during rapid growth, maturation and aging in zebrafish, Danio rerio, Biochim. Biophys. Acta, 1841, 1003–1011, doi: 10.1016/j.bbalip.2014.04.004.

    Article  CAS  PubMed  Google Scholar 

  88. Aluri, H. S., Simpson, D. C., Allegood, J. C., Hu, Y., Szczepanek, K., Gronert, S., Chen, Q., and Lesnefsky, E. J. (2014) Electron flow into cytochrome c coupled with reactive oxygen species from the electron transport chain converts cytochrome c to a cardiolipin peroxidase: role during ischemia-reperfusion, Biochim. Biophys. Acta, 1840, 3199–3207, doi: 10.1016/j.bbagen.2014.07.017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Modi, H. R., Katyare, S. S., and Patel, M. A. (2008) Ageing-induced alterations in lipid/phospholipid profiles of rat brain and liver mitochondria: implications for mito-chondrial energy linked functions, J. Membr. Biol., 221, 51–60, doi: 10.1007/s00232-007-9086-0.

    Article  CAS  PubMed  Google Scholar 

  90. Liu, X., Ye, B., Miller, S., Yuan, H., Zhang, H., Tian, L., Nie, J., Imae, R., Arai, H., Li, Y., Cheng, Z., and Shi, Y. (2012) Ablation of ALCAT1 mitigates hypertrophic car-diomyopathy through effects on oxidative stress and mitophagy, Mol. Cell. Biol., 32, 4493–4504, doi: 10.1128/ MCB.01092-12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Paradies, G., Petrosillo, G., Gadaleta, M. N., and Ruggiero, F. M. (1999) The effect of aging and acetyl-L-carnitine on the pyruvate transport and oxidation in rat heart mitochondria, FEBS Lett., 454, 207–209, doi: 10.1016/s0014-5793(99)00809-1.

    Article  CAS  PubMed  Google Scholar 

  92. Pepe, S., Tsuchiya, N., Lakatta, E. G., and Hansford, R. G. (1999) PUFA and aging modulate cardiac mitochondri-al membrane lipid composition and Ca2+ activation of PDH, Am. J. Physiol., 276, 149–158, doi: 10.1152/ajpheart. 1999.276.1.H149.

    Google Scholar 

  93. Tamburini, I., Quartacci, M. F., Izzo, R., and Bergamini, E. (2004) Effects of dietary restriction on age-related changes in the phospholipid fatty acid composition of various rat tissues, Aging Clin. Exp. Res., 16, 425–431, doi: https://doi.org/10.1007/BF03327396.

    Article  CAS  PubMed  Google Scholar 

  94. Paradies, G., Ruggiero, F. M., Petrosillo, G., and Quagliariello, E. (1997) Age-dependent decline in the cytochrome c oxidase activity in rat heart mitochondria, FEBS Lett., 406, 136–138, doi: 10.1016/s0014-5793(97)00264-0.

    Article  CAS  PubMed  Google Scholar 

  95. McMillin, J. B., Taffet, G. E., Taegtmeyer, H., Hudson, E. K., and Tate, C. A. (1993) Mitochondrial metabolism and substrate competition in the aging Fischer rat heart, Cardiovasc. Res., 27, 2222–2228, doi: 10.1093/cvr/27.12.2222.

    Article  CAS  PubMed  Google Scholar 

  96. Moghaddas, S., Stoll, M. S., Minkler, P. E., Salomon, R. G., Hoppel, C. L., and Lesnefsky, E. J. (2002) Preservation of cardiolipin content during aging in rat heart interfibrillar mitochondria, J. Gerontol. A. Biol. Sci. Med. Sci., 57, 22–28, doi: 10.1093/gerona/57.1.b22.

    Article  Google Scholar 

  97. Coleman, G. L., Barthold, S. W., Osbaldiston, G. W., Foster, S. J., and Jonas, A. M. (1977) Pathological changes during aging in barrier-reared Fischer 344 male rats, J. Gerontol., 32, 258–278, doi: 10.1093/geronj/32.3.258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Semba, R. D., Moaddel, R., Zhang, P., Ramsden, C. E., and Ferrucci, L. (2019) Tetralinoleoyl cardiolipin depletion plays a major role in the pathogenesis of sarcopenia, Med. Hypotheses, 127, 142–149, doi: 10.1016/j.mehy.2019. 04.015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Paradies, G., Ruggiero, F. M., Gadaleta, M. N., and Quagliariello, E. (1992) The effect of aging and acetyl-L-carnitine on the activity of the phosphate carrier and on the phospholipid composition in rat heart mitochondria, Biochim. Biophys. Acta, 1103, 324–326, doi: 10.1016/0005-2736(92)90103-s.

    Article  CAS  PubMed  Google Scholar 

  100. Monteiro-Cardoso, V. F., Oliveira, M. M., Melo, T., Domingues, M. R., Moreira, P. I., Ferreiro, E., Peixoto, F., and Videira, R. A. (2015) Cardiolipin profile changes are associated to the early synaptic mitochondrial dysfunction in Alzheimer’s disease, J. Alzheimers Dis., 43, 1375–1392, doi: 10.3233/JAD-141002.

    Article  CAS  PubMed  Google Scholar 

  101. Petrosillo, G., Ruggiero, F. M., Di Venosa, N., and Paradies, G. (2003) Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin, FASEB J., 17, 714–716, doi: 10.1096/fj.02-0729fje.

    Article  CAS  PubMed  Google Scholar 

  102. Chan, R. B., and Di Paolo, G. (2012) Knockout punch: cardiolipin oxidation in trauma, Nat. Neurosci., 15, 1325–1327, doi: 10.1038/nn.3222.

    Article  CAS  PubMed  Google Scholar 

  103. Ting, H. C., Chao, Y. J., and Hsu, Y. H. (2015) Polyunsaturated fatty acids incorporation into cardiolipin in H9c2 cardiac myoblast, J. Nutr. Biochem., 26, 769–775, doi: 10.1016/j.jnutbio.2015.02.005.

    Article  CAS  PubMed  Google Scholar 

  104. Chao, Y. J., Chan, J. F., and Hsu, Y. H. (2016) Chemotherapy drug induced discoordination of mitochon-drial life cycle detected by cardiolipin fluctuation, PLoS One, 11, e0162457, doi: 10.1371/journal.pone.0162457.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Petrosillo, G., Fattoretti, P., Matera, M., Ruggiero, F. M., Bertoni-Freddari, C., and Paradies, G. (2008) Melatonin prevents age-related mitochondrial dysfunction in rat brain via cardiolipin protection, Rejuvenation Res., 11, 935–943, doi: 10.1089/rej.2008.0772.

    Article  CAS  PubMed  Google Scholar 

  106. Fink, M. P., Macias, C. A., Xiao, J., Tyurina, Y. Y., Jiang, J., Belikova, N., Delude, R. L., Greenberger, J. S., Kagan, V. E., and Wipf, P. (2007) Hemigramicidin-TEMPO con-jugates: novel mitochondria-targeted antioxidants, Biochem. Pharmacol., 74, 801–809, doi: 10.1016/j.bcp. 2007.05.019.

    Article  CAS  PubMed  Google Scholar 

  107. Szeto, H. H., and Birk, A. V. (2014) Serendipity and the discovery of novel compounds that restore mitochondrial plasticity, Clin. Pharmacol. Ther., 96, 672–683, doi: 10.1038/clpt.2014.174.

    Article  CAS  PubMed  Google Scholar 

  108. Kelso, G. F., Porteous, C. M., Coulter, C. V., Hughes, G., Porteous, W. K., Ledgerwood, E. C., Smith, R. A., and Murphy, M. P. (2001) Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties, J. Biol. Chem., 276, 4588–4596, doi: 10.1074/jbc.M009093200.

    Article  CAS  PubMed  Google Scholar 

  109. Antonenko, Y. N., Avetisyan, A. V., Bakeeva, L. E., Chernyak, B. V., Chertkov, V. A., Domnina, L. V., Ivanova, O. Y., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Muntyan, M. S., Nepryakhina, O. K., Pashkovskaya, A. A., Pletjushkina, O. Y., Pustovidko, A. V., Roginsky, V. A., Rokitskaya, T. I., Ruuge, E. K., Saprunova, V. B., Severina, I. I., Simonyan, R. A., Skulachev, I. V., Skulachev, M. V., Sumbatyan, N. V., Sviryaeva, I. V., Tashlitsky, V. N., Vassiliev, J. M., Vyssokikh, M. Y., Yaguzhinsky, L. S., Zamyatnin, A. A., Jr., and Skulachev, V. P. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies, Biochemistry (Moscow), 73, 1273–1287, doi: 10.1134/s0006297908120018.

    Article  CAS  Google Scholar 

  110. Anisimov, V. N., Egorov, M. V., Krasilshchikova, M. S., Lyamzaev, K. G., Manskikh, V. N., Moshkin, M. P., Novikov, E. A., Popovich, I. G., Rogovin, K. A., Shabalina, I. G., Shekarova, O. N., Skulachev, M. V., Titova, T. V., Vygodin, V. A., Vyssokikh, M. Y., Yurova, M. N., Zabezhinsky, M. A., and Skulachev, V. P. (2011) Effects of the mitochondria-targeted antioxidant SkQ1 on lifespan of rodents, Aging (Albany N. Y.), 3, 1110–1119, doi: 10.18632/aging.100404.

    CAS  Google Scholar 

  111. Lyamzaev, K. G., Pustovidko, A. V., Simonyan, R. A., Rokitskaya, T. I., Domnina, L. V., Ivanova, O. Y., Severina, I. I., Sumbatyan, N. V., Korshunova, G. A., Tashlitsky, V. N., Roginsky, V. A., Antonenko, Y. N., Skulachev, M. V., Chernyak, B. V., and Skulachev, V. P. (2011) Novel mitochondria-targeted antioxidants: plasto-quinone conjugated with cationic plant alkaloids berberine and palmatine, Pharm. Res., 28, 2883–2895, doi: 10.1007/s11095-011-0504-8.

    Article  CAS  PubMed  Google Scholar 

  112. Skulachev, V. P. (2012) Mitochondria-targeted antioxi-dants as promising drugs for treatment of age-related brain diseases, J. Alzheimer’s Dis., 28, 283–289, doi: 10.3233/JAD-2011-111391.

    Article  CAS  Google Scholar 

  113. Jiang, J., Bakan, A., Kapralov, A. A., Silva, K. I., Huang, Z., Amoscato, A. A., Peterson, J., Garapati, V. K., Saxena, S., Bayir, H., Atkinson, J., Bahar, I., and Kagan, V. E. (2014) Designing inhibitors of cytochrome c/cardiolipin peroxidase complexes: mitochondria-targeted imidazole-substituted fatty acids, Free Radic. Biol. Med., 71, 221–230, doi: 10.1016/j.freeradbiomed.2014.02.029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Kloner, R. A., Hale, S. L., Dai, W., Gorman, R. C., Shuto, T., Koomalsingh, K. J., Gorman, J. H., 3rd, Sloan, R. C., Frasier, C. R., Watson, C. A., Bostian, P. A., Kypson, A. P., and Brown, D. A. (2012) Reduction of ischemia/reperfu-sion injury with Bendavia, a mitochondria-targeting cyto-protective peptide, J. Am. Heart Assoc., 1, e001644, doi: 10.1161/JAHA.112.001644.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Szeto, H. H. (2018) Stealth peptides target cellular power-houses to fight rare and common age-related diseases, Protein Pept. Lett., 25, 1108–1123, doi: 10.2174/0929866525666181101105209.

    Article  CAS  PubMed  Google Scholar 

  116. Szeto, H. H. (2014) First-in-class cardiolipin-protective compound as a therapeutic agent to restore mitochondrial bioenergetics, Br. J. Pharmacol., 171, 2029–2050, doi: 10.1111/bph.12461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. McLachlan, J., Beattie, E., Murphy, M. P., Koh-Tan, C. H., Olson, E., Beattie, W., Dominiczak, A. F., Nicklin, S. A., and Graham, D. (2014) Combined therapeutic benefit of mitochondria-targeted antioxidant, MitoQ10, and angiotensin receptor blocker, losartan, on cardiovascular function, J. Hypertens., 32, 555–564, doi: 10.1097/HJH.0000000000000054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Adlam, V. J., Harrison, J. C., Porteous, C. M., James, A. M., Smith, R. A., Murphy, M. P., and Sammut, I. A. (2005) Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury, FASEB J., 19, 1088–1095, doi: 10.1096/fj.05-3718com.

    Article  CAS  PubMed  Google Scholar 

  119. Skulachev, V. P., Antonenko, Y. N., Cherepanov, D. A., Chernyak, B. V., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Pletjushkina, O. Y., Roginsky, V. A., Rokitskaya, T. I., Severin, F. F., Severina, I. I., Simonyan, R. A., Skulachev, M. V., Sumbatyan, N. V., Sukhanova, E. I., Tashlitsky, V. N., Trendeleva, T. A., Vyssokikh, M. Y., and Zvyagilskaya, R. A. (2010) Prevention of cardiolipin oxidation and fatty acid cycling as two antioxidant mechanisms of cationic derivatives of plastoquinone (SkQs), Biochim. Biophys. Acta, 1797, 878–889, doi: 10.1016/j.bbabio. 2010.03.015.

    Article  CAS  PubMed  Google Scholar 

  120. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J. N., Rovio, A. T., Bruder, C. E., Bohlooly, Y. M., Gidlof, S., Oldfors, A., Wibom, R., Tornell, J., Jacobs, H. T., and Larsson, N. G. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase, Nature, 429, 417–423, doi: 10.1038/nature02517.

    Article  CAS  PubMed  Google Scholar 

  121. Shabalina, I. G., Vyssokikh, M. Y., Gibanova, N., Csikasz, R. I., Edgar, D., Hallden-Waldemarson, A., Rozhdestvenskaya, Z., Bakeeva, L. E., Vays, V. B., Pustovidko, A. V., Skulachev, M. V., Cannon, B., Skulachev, V. P., and Nedergaard, J. (2017) Improved health-span and lifespan in mtDNA mutator mice treated with the mitochondrially targeted antioxi-dant SkQ1, Aging (Albany NY), 9, 315–339, doi: 10.18632/aging.101174.

    Article  CAS  Google Scholar 

  122. Lokhmatikov, A. V., Voskoboynikova, N., Cherepanov, D. A., Skulachev, M. V., Steinhoff, H. J., Skulachev, V. P., and Mulkidjanian, A. Y. (2016) Impact of antioxidants on car-diolipin oxidation in liposomes: why mitochondrial cardio-lipin serves as an apoptotic signal? Oxid. Med. Cell Longev., 2016, 8679469, doi: 10.1155/2016/8679469.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Mileykovskaya, E., and Dowhan, W. (2009) Cardiolipin membrane domains in prokaryotes and eukaryotes, Biochim. Biophys. Acta, 1788, 2084–2091, doi: 10.1016/ j.bbamem.2009.04.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Bradley, R. M., Stark, K. D., and Duncan, R. E. (2016) Influence of tissue, diet, and enzymatic remodeling on cardiolipin fatty acyl profile, Mol. Nutr. Food Res., 60, 1804–1818, doi: 10.1002/mnfr.201500966.

    Article  CAS  PubMed  Google Scholar 

  125. Broadhurst, C. L., Wang, Y., Crawford, M. A., Cunnane, S. C., Parkington, J. E., and Schmidt, W. F. (2002) Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 131, 653–673, doi: 10.1016/s1096-4959(02)00002-7.

    Article  PubMed  Google Scholar 

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Funding

The study was supported by the Russian Foundation for Basic Research (project 18-29-13037).

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Authors and Affiliations

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

    G. A. Shilovsky, V. V. Ashapkin & M. Y. Vyssokikh

  2. Faculty of Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    G. A. Shilovsky, T. S. Putyatina, E. V. Sorokina & A. V. Markov

  3. Institute for Information Transmission Problems, Russian Academy of Sciences, 127051, Moscow, Russia

    G. A. Shilovsky & V. A. Lyubetsky

  4. Nesmeyanov Institute of Organoelement Compounds, Russian Academy of Sciences, 119991, Moscow, Russia

    O. V. Yamskova

  5. Institute of Molecular Genetics, Russian Academy of Sciences, 123182, Moscow, Russia

    S. I. Shram

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  1. G. A. Shilovsky
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Correspondence to G. A. Shilovsky.

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Conflict of interest. The authors declare no conflict of interest.

Compliance with ethical standards. No people or animals were used as objects for studies in this work.

Published in Russian in Biokhimiya, 2019, Vol. 84, No. 12, pp. 1815–1831.

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Shilovsky, G.A., Putyatina, T.S., Ashapkin, V.V. et al. Biological Diversity and Remodeling of Cardiolipin in Oxidative Stress and Age-Related Pathologies. Biochemistry Moscow 84, 1469–1483 (2019). https://doi.org/10.1134/S000629791912006X

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