Biochemistry (Moscow)

, Volume 80, Issue 12, pp 1560–1570 | Cite as

Diseases and aging: Gender matters

  • V. A. Popkov
  • E. Yu. Plotnikov
  • D. N. Silachev
  • L. D. Zorova
  • I. B. Pevzner
  • S. S. Jankauskas
  • S. D. Zorov
  • V. A. Babenko
  • D. B. Zorov
Review

Abstract

At first glance, biological differences between male and female sex seem obvious, but, in fact, they affect a vast number of deeper levels apart from reproductive function and related physiological features. Such differences affect all organizational levels including features of cell physiology and even functioning of separate organelles, which, among other things, account for such global processes as resistance to diseases and aging. Understanding of mechanisms underlying resistance of one of the sexes to pathological processes and aging will allow taking into consideration gender differences while developing drugs and therapeutic approaches, and it will provide an opportunity to reproduce and enhance such resistance in the more vulnerable gender. Here we review physiological as well as cellular and biological features of disease course including aging that are affected by gender and discuss potential mechanisms behind these processes. Such mechanisms include features of oxidative metabolism and mitochondrial functioning.

Keywords

mortality aging females males myocardial infarction stroke hormones estrogen mitochondria 

Abbreviations

ROS

reactive oxygen species

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    World Health Organization, Annual Report (2012).Google Scholar
  2. 2.
    Anand, S. S., Islam, S., Rosengren, A., Franzosi, M. G., Steyn, K., Yusufali, A. H., Keltai, M., Diaz, R., Rangarajan, S., and Yusuf, S. (2008. Risk factors for myocardial infarction in women and men: insights from the INTERHEART study, Eur. Heart J., 29, 932–940.PubMedCrossRefGoogle Scholar
  3. 3.
    Hochman, J. S., McCabe, C. H., Stone, P. H., Becker, R. C., Cannon, C. P., Defeo-Fraulini, T., Thompson, B., Steingart, R., Knatterud, G., and Braunwald, E. (1997. Outcome and profile of women and men presenting with acute coronary syndromes: a report from TIMI IIIB, J. Am. Coll. Cardiol., 30, 141–148.PubMedCrossRefGoogle Scholar
  4. 4.
    Heer, T., Gitt, A. K., Juenger, C., Schiele, R., Wienbergen, H., Towae, F., Gottwitz, M., Zahn, R., Zeymer, U., and Senges, J. (2006. Gender differences in acute non-ST-segment elevation myocardial infarction, Am. J. Cardiol., 98, 160–166.PubMedCrossRefGoogle Scholar
  5. 5.
    Deswal, A., and Bozkurt, B. (2006. Comparison of morbidity in women versus men with heart failure and preserved ejection fraction, Am. J. Cardiol., 97, 1228–1231.PubMedCrossRefGoogle Scholar
  6. 6.
    Dimitrow, P., Czarnecka, D., Jaszcz, K., and Dubiel, J. (1997. Sex differences in age at onset of symptoms in patients with hypertrophic cardiomyopathy, J. Cardiovasc. Risk, 5, 33–35.CrossRefGoogle Scholar
  7. 7.
    Humphries, K. H., Kerr, C. R., Connolly, S. J., Klein, G., Boone, J. A., Green, M., Sheldon, R., Talajic, M., Dorian, P., and Newman, D. (2001. New-onset atrial fibrillation: sex differences in presentation, treatment, and outcome, Circulation, 103, 2365–2370.PubMedCrossRefGoogle Scholar
  8. 8.
    Costenbader, K. H., Feskanich, D., Stampfer, M. J., and Karlson, E. W. (2007. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women, Arthritis Rheum., 56, 1251–1262.PubMedCrossRefGoogle Scholar
  9. 9.
    Sandberg, K. (2008. Mechanisms underlying sex differences in progressive renal disease, Gend. Med., 5, 10–23.PubMedCrossRefGoogle Scholar
  10. 10.
    Grodstein, F., Stampfer, M. J., Manson, J. E., Colditz, G. A., Willett, W. C., Rosner, B., Speizer, F. E., and Hennekens, C. H. (1996. Postmenopausal estrogen and progestin use and the risk of cardiovascular disease, N. Engl. J. Med., 335, 453–461.PubMedCrossRefGoogle Scholar
  11. 11.
    Harrison-Bernard, L. M., and Raij, L. (2000. Postmenopausal hypertension, Curr. Hypertens. Rep., 2, 202–207.PubMedCrossRefGoogle Scholar
  12. 12.
    Rosen, C. J. (2005. Postmenopausal osteoporosis, Bone, 8, 595–603.Google Scholar
  13. 13.
    Vaccarino, V., Parsons, L., Every, N. R., Barron, H. V., and Krumholz, H. M. (1999. Sex-based differences in early mortality after myocardial infarction. National Registry of Myocardial Infarction 2 Participants, N. Engl. J. Med., 341, 217–225.PubMedCrossRefGoogle Scholar
  14. 14.
    Lundblad, D., Holmgren, L., Jansson, J.-H., Naslund, U., and Eliasson, M. (2008. Gender differences in trends of acute myocardial infarction events: the Northern Sweden MONICA study 1985-2004, BMC Cardiovasc. Disord., 8, 17.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Cavasin, M. A., Tao, Z.-Y., Yu, A.-L., and Yang, X.-P. (2006. Testosterone enhances early cardiac remodeling after myocardial infarction, causing rupture and degrading cardiac function, Am. J. Physiol. Heart Circ. Physiol., 290, 2043–2050.CrossRefGoogle Scholar
  16. 16.
    Pajunen, P., Taskinen, M. R., Nieminen, M. S., and Syvanne, M. (2000. Angiographic severity and extent of coronary artery disease in patients with type 1 diabetes mellitus, Am. J. Cardiol., 86, 1080–1085.PubMedCrossRefGoogle Scholar
  17. 17.
    Donahue, R. P., Rejman, K., Rafalson, L. B., Dmochowski, J., Stranges, S., and Trevisan, M. (2007. Sex differences in endothelial function markers before conversion to pre-diabetes: does the clock start ticking earlier among women? The Western New York study, Diabetes Care, 30, 354–359.PubMedCrossRefGoogle Scholar
  18. 18.
    Carlsson, A. C., Wandell, P. E., De Faire, U., and Hellenius, M. L. (2008. Risk factors associated with newly diagnosed high blood pressure in men and women, Am. J. Hypertens., 21, 771–777.PubMedCrossRefGoogle Scholar
  19. 19.
    Aharon, A., Zandman-Goddard, G., and Shoenfeld, Y. (1994. Autoimmune multiorgan involvement in elderly men is it SLE? Clin. Rheumatol., 13, 631–634.PubMedCrossRefGoogle Scholar
  20. 20.
    Prete, P. E., Majlessi, A., Gilman, S., and Hamideh, F. (2001. Systemic lupus erythematosus in men: a retrospective analysis in a Veterans Administration Healthcare System population, J. Clin. Rheumatol., 7, 142–150.PubMedCrossRefGoogle Scholar
  21. 21.
    Jimenez-Balderas, F. J., and Mintz, G. (1993. Ankylosing spondylitis: clinical course in women and men, J. Rheumatol., 20, 2069–2072.PubMedGoogle Scholar
  22. 22.
    Hannedouche, T., Chauveau, P., Kalou, F., Albouze, G., Lacour, B., and Jungers, P. (1993. Factors affecting progression in advanced chronic renal failure, Clin. Nephrol., 39, 312–320.PubMedGoogle Scholar
  23. 23.
    Neugarten, J., Acharya, A., and Silbiger, S. R. (2000. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis, J. Am. Soc. Nephrol., 11, 319–329.PubMedGoogle Scholar
  24. 24.
    National Institutes of Health, National Institutes of Diabetes and Digestive and Kidney Disease, D. of K.U. and H.D. (2011) USRDS 2011 Annual Data Report: Atlas of Chronic Kidney Disease and End-Stage Renal Disease in the United States, 2011.Google Scholar
  25. 25.
    Manigrasso, M. B., and Maric-Bilkan, C. (2013) Peptides, sex, diabetes, and the kidney, in Handbook in Biologically Active Peptides, pp. 1487–1493.CrossRefGoogle Scholar
  26. 26.
    Sellner, J., Kraus, J., Awad, A., Milo, R., Hemmer, B., and Stuve, O. (2011. The increasing incidence and prevalence of female multiple sclerosis. A critical analysis of potential environmental factors, Autoimmun. Rev., 10, 495–502.PubMedCrossRefGoogle Scholar
  27. 27.
    Beatty, W. W., and Aupperle, R. L. (2002. Sex differences in cognitive impairment in multiple sclerosis, Clin. Neuropsychol., 16, 472–480.PubMedCrossRefGoogle Scholar
  28. 28.
    Howard, V. J., Cushman, M., Pulley, L., Gomez, C. R., Go, R. C., Prineas, R. J., Graham, A., Moy, C. S., and Howard, G. (2005. The reasons for geographic and racial differences in stroke study: objectives and design, Neuroepidemiology, 25, 135–143.PubMedCrossRefGoogle Scholar
  29. 29.
    Niewada, M., Kobayashi, A., Sandercock, P. A., Kaminski, B., and Czlonkowska, A. (2005. Influence of gender on baseline features and clinical outcomes among 17,370 patients with confirmed ischaemic stroke in the international stroke trial, Neuroepidemiology, 24, 123–128.PubMedCrossRefGoogle Scholar
  30. 30.
    Sheikh, K., and Bullock, C. M. (2007. Effect of measurement on sex difference in stroke mortality, Stroke, 38, 10851087.CrossRefGoogle Scholar
  31. 31.
    McHugh, J. C., and Delanty, N. (2008. Epidemiology and classification of epilepsy: gender comparisons, Int. Rev. Neurobiol., 83, 11–26.PubMedCrossRefGoogle Scholar
  32. 32.
    Oertelt-Prigione, V., and Regitz-Zagrosek, V. (2012) Sex and Gender Aspects in Clinical Medicine, Springer-Verlag, London.CrossRefGoogle Scholar
  33. 33.
    Miller, J. A., Anacta, L. A., and Cattran, D. C. (1999. Impact of gender on the renal response to angiotensin II, Kidney Int., 55, 278–285.PubMedCrossRefGoogle Scholar
  34. 34.
    Ogden, C. L., Fryar, C. D., Carroll, M. D., and Flegal, K. M. (2004. Mean body weight, height, and body mass index, United States 1960-2002, Adv. Data, 1–17.Google Scholar
  35. 35.
    Benjamin, M., Toumi, H., Ralphs, J. R., Bydder, G., Best, T. M., and Milz, S. (2006. Where tendons and ligaments meet bone: attachment sites (“entheses”) in relation to exercise and/or mechanical load, J. Anat., 208, 471–490.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Janssen, I., Heymsfield, S. B., Wang, Z. M., and Ross, R. (2000. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr, J. Appl. Physiol., 89, 81–88.PubMedGoogle Scholar
  37. 37.
    Miller, A. E. J., MacDougall, J. D., Tarnopolsky, M. A., and Sale, D. G. (1993. Gender differences in strength and muscle fiber characteristics, Eur. J. Appl. Physiol. Occup. Physiol., 66, 254–262.PubMedCrossRefGoogle Scholar
  38. 38.
    Glucksmann, A. (1981) Sexual Dimorphism in Human and Mammalian Biology and Pathology, Academic Press, London-New York.Google Scholar
  39. 39.
    Salton, C. J., Chuang, M. L., O’Donnell, C. J., Kupka, M. J., Larson, M. G., Kissinger, K. V., Edelman, R. R., Levy, D., and Manning, W. J. (2002. Gender differences and normal left ventricular anatomy in an adult population free of hypertension, J. Am. Coll. Cardiol., 39, 1055–1060.PubMedCrossRefGoogle Scholar
  40. 40.
    Neugarten, J., Kasiske, B., Silbiger, S. R., and Nyengaard, J. R. (2002. Effects of sex on renal structure, Nephron, 90, 139–144.PubMedCrossRefGoogle Scholar
  41. 41.
    Nyengaard, J. R., and Bendtsen, T. F. (1992. Glomerular number and size in relation to age, kidney weight, and body surface in normal man, Anat. Rec., 232, 194–201.PubMedCrossRefGoogle Scholar
  42. 42.
    Jean-Faucher, C., Berger, M., Gallon, C., De Turckheim, M., Veyssiere, G., and Jean, C. (1987. Sex-related differences in renal size in mice: ontogeny and influence of neonatal androgens, J. Endocrinol., 115, 241–246.PubMedCrossRefGoogle Scholar
  43. 43.
    Oudar, O., Elger, M., Bankir, L., Ganten, D., Ganten, U., and Kriz, W. (1991. Differences in rat kidney morphology between males, females, and testosterone-treated females, Ren. Physiol. Biochem., 14, 92–102.PubMedGoogle Scholar
  44. 44.
    Blantz, R. C., Peterson, O. W., Blantz, E. R., and Wilson, C. B. (1988. Sexual differences in glomerular ultrafiltration: effect of androgen administration in ovariectomized rats, Endocrinology, 122, 767–773.PubMedCrossRefGoogle Scholar
  45. 45.
    Ankney, C. D. (1992. Sex differences in relative brain size: the mismeasure of woman, too? Intelligence, 16, 329–336.CrossRefGoogle Scholar
  46. 46.
    Marner, L., Nyengaard, J. R., Tang, Y., and Pakkenberg, B. (2003. Marked loss of myelinated nerve fibers in the human brain with age, J. Comp. Neurol., 462, 144–152.PubMedCrossRefGoogle Scholar
  47. 47.
    Alonso-Nanclares, L., Gonzalez-Soriano, J., Rodriguez, J. R., and De Felipe, J. (2008. Gender differences in human cortical synaptic density, Proc. Natl. Acad. Sci. USA, 105, 14615–14619.PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Dongworth, R. K., Hall, A. R., Burke, N., and Hausenloy, D. J. (2014. Targeting mitochondria for cardioprotection: examining the benefit for patients, Future Cardiol., 10, 255–272.PubMedCrossRefGoogle Scholar
  49. 49.
    Garaulet, M., Perez-Llamas, F., Fuente, T., Zamora, S., and Tebar, F. J. (2000. Anthropometric, computed tomography, and fat cell data in an obese population: relationship with insulin, leptin, tumor necrosis factor-alpha, sex hormone-binding globulin and sex hormones, Eur. J. Endocrinol., 143, 657–666.PubMedCrossRefGoogle Scholar
  50. 50.
    Ferraro, R., Lillioja, S., Fontvieille, A. M., Rising, R., Bogardus, C., and Ravussin, E. (1992. Lower sedentary metabolic rate in women compared with men, J. Clin. Invest., 90, 780–784.PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Buchholz, A. C., Rafii, M., and Pencharz, P. B. (2001. Is resting metabolic rate different between men and women? Br. J. Nutr., 86, 641–646.PubMedCrossRefGoogle Scholar
  52. 52.
    Arciero, P. J., Goran, M. I., and Poehlman, E. T. (1993. Resting metabolic rate is lower in women than in men, J. Appl. Physiol., 75, 2514–2520.PubMedGoogle Scholar
  53. 53.
    Humpeler, E., Vogel, S., Schobersberger, W., and Mairbaurl, H. (1989. Red cell oxygen transport in man in relation to gender and age, Mech. Ageing Dev., 47, 229–239.PubMedCrossRefGoogle Scholar
  54. 54.
    Straface, E., Vona, R., Gambardella, L., Ascione, B., Marino, M., Bulzomi, P., Canu, S., Coinu, R., Rosano, G., Malorni, W., and Franconi, F. (2009. Cell sex determines anoikis resistance in vascular smooth muscle cells, FEBS Lett., 583, 3448–3454.PubMedCrossRefGoogle Scholar
  55. 55.
    Matarrese, P., Colasanti, T., Ascione, B., Margutti, P., Franconi, F., Alessandri, C., Conti, F., Riccieri, V., Rosano, G., Ortona, E., and Malorni, W. (2011. Gender disparity in susceptibility to oxidative stress and apoptosis induced by autoantibodies specific to RLIP76 in vascular cells, Antioxid. Redox Signal., 15, 2825–2836.PubMedCrossRefGoogle Scholar
  56. 56.
    Malorni, W., Campesi, I., Straface, E., Vella, S., and Franconi, F. (2007. Redox features of the cell: a gender perspective, Antioxid. Redox Signal., 9, 1779–1801.PubMedCrossRefGoogle Scholar
  57. 57.
    Valle, A., Guevara, R., Garcia-Palmer, F. J., Roca, P., and Oliver, J. (2007. Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions, Am. J. Physiol. Cell Physiol., 293, 1302–1308.CrossRefGoogle Scholar
  58. 58.
    Guevara, R., Santandreu, F. M., Valle, A., Gianotti, M., Oliver, J., and Roca, P. (2009. Sex-dependent differences in aged rat brain mitochondrial function and oxidative stress, Free Radic. Biol. Med., 46, 169–175.PubMedCrossRefGoogle Scholar
  59. 59.
    Wang, E. Y., Biala, A. K., Gordon, J. W., and Kirshenbaum, L. A. (2012. Autophagy in the heart, J. Cardiovasc. Pharmacol., 60, 110–117.PubMedCrossRefGoogle Scholar
  60. 60.
    Lee, J., Giordano, S., and Zhang, J. (2011. Autophagy, mitochondria, and oxidative stress: cross-talk and redox signalling, Biochem. J., 441, 523–540.PubMedCentralCrossRefGoogle Scholar
  61. 61.
    Campesi, I., Straface, E., Occhioni, S., Montella, A., and Franconi, F. (2013. Protein oxidation seems to be linked to constitutive autophagy: a sex study, Life Sci., 93, 145–152.PubMedCrossRefGoogle Scholar
  62. 62.
    Cosper, P. F., and Leinwand, L. A. (2011. Cancer causes cardiac atrophy and autophagy in a sexually dimorphic manner, Cancer Res., 71, 1710–1720.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Du, L., Hickey, R. W., Bayir, H., Watkins, S. C., Tyurin, V. A., Guo, F., Kochanek, P. M., Jenkins, L. W., Ren, J., Gibson, G., Chu, C. T., Kagan, V. E., and Clark, R. S. (2009. Starving neurons show sex difference in autophagy, J. Biol. Chem., 284, 2383–2396.PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Czubryt, M. P., McAnally, J., Fishman, G. I., and Olson, E. N. (2003. Regulation of peroxisome proliferator-activated receptor ? coactivator 1a (PGC-1a) and mitochondrial function by MEF2 and HDAC5, Proc. Natl. Acad. Sci. USA, 100, 1711–1716.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Singh, H., Cheng, J., Deng, H., Kemp, R., Ishizuka, T., Nasjletti, A., and Schwartzman, M. L. (2007. Vascular cytochrome P450 4A expression and 20-hydroxyeicosatetraenoic acid synthesis contribute to endothelial dysfunction in androgen-induced hypertension, Hypertension, 50, 123–129.PubMedCrossRefGoogle Scholar
  66. 66.
    Reckelhoff, J. F., Zhang, H., Srivastava, K., and Granger, J. P. (1999. Gender differences in hypertension in spontaneously hypertensive rats: role of androgens and androgen receptor, Hypertension, 34, 920–923.PubMedCrossRefGoogle Scholar
  67. 67.
    Szekacs, B., Vajo, Z., Varbiro, S., Kakucs, R., Vaslaki, L., Acs, N., Mucsi, I., and Brinton, E. A. (2000. Postmenopausal hormone replacement improves proteinuria and impaired creatinine clearance in type 2 diabetes mellitus and hypertension, BJOG, 107, 1017–1021.PubMedCrossRefGoogle Scholar
  68. 68.
    Hsieh, Y.-C., Choudhry, M. A., Yu, H.-P., Shimizu, T., Yang, S., Suzuki, T., Chen, J., Bland, K. I., and Chaudry, I. H. (2006. Inhibition of cardiac PGC-1a expression abolishes ERß agonist-mediated cardioprotection following trauma-hemorrhage, FASEB J., 20, 1109–1117.PubMedCrossRefGoogle Scholar
  69. 69.
    Lopez-Ruiz, A., Sartori-Valinotti, J., Yanes, L. L., Iliescu, R., and Reckelhoff, J. F. (2008. Sex differences in control of blood pressure: role of oxidative stress in hypertension in females, Am. J. Physiol. Heart Circ. Physiol., 295, 466–474.CrossRefGoogle Scholar
  70. 70.
    Sullivan, J. C., Sasser, J. M., and Pollock, J. S. (2007. Sexual dimorphism in oxidant status in spontaneously hypertensive rats, Am. J. Physiol. Regul. Integr. Comp. Physiol., 292, 764–768.CrossRefGoogle Scholar
  71. 71.
    Giordano, G., Tait, L., Furlong, C. E., Cole, T. B., Kavanagh, T. J., and Costa, L. G. (2013. Gender differences in brain susceptibility to oxidative stress are mediated by levels of paraoxonase-2 expression, Free Radic. Biol. Med., 58, 98–108.PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Haq, S., Choukroun, G., Kang, Z. B., Ranu, H., Matsui, T., Rosenzweig, A., Molkentin, J. D., Alessandrini, A., Woodgett, J., Hajjar, R., Michael, A., and Force, T. (2000. Glycogen synthase kinase-3ß is a negative regulator of cardiomyocyte hypertrophy, J. Cell Biol., 151, 117–130.PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Antos, C. L., McKinsey, T. A., Frey, N., Kutschke, W., McAnally, J., Shelton, J. M., Richardson, J. A., Hill, J. A., and Olson, E. N. (2002. Activated glycogen synthase-3ß suppresses cardiac hypertrophy in vivo, Proc. Natl. Acad. Sci. USA, 99, 907–912.PubMedCentralPubMedCrossRefGoogle Scholar
  74. 74.
    Kadokami, T., McTiernan, C. F., Kubota, T., Frye, C. S., and Feldman, A. M. (2000. Sex-related survival differences in murine cardiomyopathy are associated with differences in TNF-receptor expression, J. Clin. Invest., 106, 589–597.PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Janczewski, A. M., Kadokami, T., Lemster, B., Frye, C. S., McTiernan, C. F., and Feldman, A. M. (2003. Morphological and functional changes in cardiac myocytes isolated from mice overexpressing TNF-a, Am. J. Physiol. Heart Circ. Physiol., 284, 960–969.CrossRefGoogle Scholar
  76. 76.
    Wang, C., Chiari, P. C., Weihrauch, D., Krolikowski, J. G., Warltier, D. C., Kersten, J. R., Pratt, P. F., and Pagel, P. S. (2006. Gender-specificity of delayed preconditioning by isoflurane in rabbits: potential role of endothelial nitric oxide synthase, Anesth. Analg., 103, 274–280.PubMedCrossRefGoogle Scholar
  77. 77.
    Cross, H. R., Kranias, E. G., Murphy, E., and Steenbergen, C. (2003. Ablation of PLB exacerbates ischemic injury to a lesser extent in female than male mice: protective role of NO, Am. J. Physiol. Heart Circ. Physiol., 284, 683–690.CrossRefGoogle Scholar
  78. 78.
    Vijay, V., Han, T., Moland, C. L., Kwekel, J. C., Fuscoe, J. C., and Desai, V. G. (2015. Sexual dimorphism in the expression of mitochondria-related genes in rat heart at different ages, PLoS One, 10, e0117047.Google Scholar
  79. 79.
    Foryst-Ludwig, A., Kreissl, M. C., Sprang, C., Thalke, B., Bohm, C., Benz, V., Gurgen, D., Dragun, D., Schubert, C., Mai, K., Stawowy, P., Spranger, J., Regitz-Zagrosek, V., Unger, T., and Kintscher, U. (2011. Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability, Am. J. Physiol. Heart Circ. Physiol., 301, 115–122.CrossRefGoogle Scholar
  80. 80.
    Foryst-Ludwig, A., and Kintscher, U. (2010. Metabolic impact of estrogen signalling through ERa and ERß, J. Steroid Biochem. Mol. Biol., 122, 74–81.PubMedCrossRefGoogle Scholar
  81. 81.
    Yao, J., Hamilton, R. T., Cadenas, E., and Brinton, R. D. (2010. Decline in mitochondrial bioenergetics and shift to ketogenic profile in brain during reproductive senescence, Biochim. Biophys. Acta, 1800, 1121–1126.PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Ding, F., Yao, J., Zhao, L., Mao, Z., Chen, S., and Brinton, R. D. (2013. Ovariectomy induces a shift in fuel availability and metabolism in the hippocampus of the female transgenic model of familial Alzheimer’s, PLoS One, 8, 13–15.Google Scholar
  83. 83.
    Ciana, P., Raviscioni, M., Mussi, P., Vegeto, E., Que, I., Parker, M. G., Lowik, C., and Maggi, A. (2003. In vivo imaging of transcriptionally active estrogen receptors, Nat. Med., 9, 82–86.PubMedCrossRefGoogle Scholar
  84. 84.
    Mikkola, A., Aro, J., Rannikko, S., Oksanen, H., and Ruutu, M. (2005. Cardiovascular complications in patients with advanced prostatic cancer treated by means of orchiectomy or polyestradiol phosphate, Scand. J. Urol. Nephrol., 39, 294–300.PubMedCrossRefGoogle Scholar
  85. 85.
    Hamilton, E. J., Gianatti, E., Strauss, B. J., Wentworth, J., Lim-Joon, D., Bolton, D., Zajac, J. D., and Grossmann, M. (2011. Increase in visceral and subcutaneous abdominal fat in men with prostate cancer treated with androgen deprivation therapy, Clin. Endocrinol. (Oxford), 74, 377–383.CrossRefGoogle Scholar
  86. 86.
    Langley, R. E., Cafferty, F. H., Alhasso, A. A., Rosen, S. D., Sundaram, S. K., Freeman, S. C., Pollock, P., Jinks, R. C., Godsland, I. F., Kockelbergh, R., Clarke, N. W., Kynaston, H. G., Parmar, M. K., and Abel, P. D. (2013. Cardiovascular outcomes in patients with locally advanced and metastatic prostate cancer treated with luteinizing hormone-releasing hormone agonists or transdermal oestrogen: the randomised, phase 2 MRC PATCH trial (PR09), Lancet Oncol., 14, 306–316.PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Haring, R., John, U., Volzke, H., Nauck, M., Dorr, M., Felix, S. B., and Wallaschofski, H. (2012. Low testosterone concentrations in men contribute to the gender gap in cardiovascular morbidity and mortality, Gend. Med., 9, 557–568.PubMedCrossRefGoogle Scholar
  88. 88.
    Gooren, L. J., Wierckx, K., and Giltay, E. J. (2014. Cardiovascular disease in transsexual persons treated with cross-sex hormones: reversal of the traditional sex difference in cardiovascular disease pattern, Eur. J. Endocrinol., 170, 809–819.PubMedCrossRefGoogle Scholar
  89. 89.
    Barrett-Connor, E. (2003. Clinical review 162: cardiovascular endocrinology 3: an epidemiologist looks at hormones and heart disease in women, J. Clin. Endocrinol. Metab., 88, 4031–4042.PubMedCrossRefGoogle Scholar
  90. 90.
    Graves, J. A. (2006. Sex chromosome specialization and degeneration in mammals, Cell, 124, 901–914.PubMedCrossRefGoogle Scholar
  91. 91.
    Arakawa, Y., Nishida-Umehara, C., Matsuda, Y., Sutou, S., and Suzuki, H. (2002. X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat, Cytogenet. Genome Res., 99, 303–309.PubMedCrossRefGoogle Scholar
  92. 92.
    Forsberg, L. A., Rasi, C., Malmqvist, N., Davies, H., Pasupulati, S., Pakalapati, G., Sandgren, J., Diaz de Stahl, T., Zaghlool, A., Giedraitis, V., Lannfelt, L., Score, J., Cross, N. C., Absher, D., Janson, E. T., Lindgren, C. M., Morris, A. P., Ingelsson, E., Lind, L., and Dumanski, J. P. (2014. Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer, Nat. Genet., 46, 624–628.PubMedCrossRefGoogle Scholar
  93. 93.
    Hughes, I. A., and Deeb, A. (2006. Androgen resistance, Best Pract. Res. Clin. Endocrinol. Metab., 20, 577–598.PubMedCrossRefGoogle Scholar
  94. 94.
    Greiner, S., Sobanski, J., and Bock, R. (2015. Why are most organelle genomes transmitted maternally? Bioessays, 37, 80–94.PubMedCentralPubMedCrossRefGoogle Scholar
  95. 95.
    Gregersen, N., Hansen, J., and Palmfeldt, J. (2012. Mitochondrial proteomics–a tool for the study of metabolic disorders, J. Inherit. Metab. Dis., 35, 715–726.PubMedCrossRefGoogle Scholar
  96. 96.
    Woodson, J. D., and Chory, J. (2008. Coordination of gene expression between organellar and nuclear genomes, Nat. Rev. Genet., 9, 383–395.PubMedCrossRefGoogle Scholar
  97. 97.
    Gemmell, N. J., Metcalf, V. J., and Allendorf, F. W. (2004. Mother’s curse: the effect of mtDNA on individual fitness and population viability, Trends Ecol. Evol., 19, 238–244.PubMedCrossRefGoogle Scholar
  98. 98.
    Wolff, J. N., and Gemmell, N. J. (2013. Mitochondria, maternal inheritance, and asymmetric fitness: why males die younger, BioEssays, 35, 93–99.PubMedCrossRefGoogle Scholar
  99. 99.
    Wallace, D. C. (2010. Mitochondrial DNA mutations in disease and aging, Environ. Mol. Mutagen., 51, 440–450.PubMedGoogle Scholar
  100. 100.
    Ruiz-Pesini, E., Lapena, A. C., Diez-Sanchez, C., PerezMartos, A., Montoya, J., Alvarez, E., Diaz, M., Urries, A., Montoro, L., Lopez-Perez, M. J., and Enriquez, J. A. (2000. Human mtDNA haplogroups associated with high or reduced spermatozoa motility, Am. J. Hum. Genet., 67, 682–696.PubMedCentralPubMedCrossRefGoogle Scholar
  101. 101.
    Wallace, D. C., Singh, G., Lott, M. T., Hodge, J. A., Schurr, T. G., Lezza, A. M., Elsas, L. J., and Nikoskelainen, E. K. (1988. Mitochondrial DNA mutation associated with Leber’s hereditary optic neuropathy, Science, 242, 1427–1430.PubMedCrossRefGoogle Scholar
  102. 102.
    Greaves, L. C., Reeve, A. K., Taylor, R. W., and Turnbull, D. M. (2012. Mitochondrial DNA and disease, J. Pathol., 226, 274–286.PubMedCrossRefGoogle Scholar
  103. 103.
    Schapira, A. H. (2012. Mitochondrial diseases, Lancet, 379, 1825–1834.PubMedCrossRefGoogle Scholar
  104. 104.
    Ieremiadou, F., and Rodakis, G. C. (2009. Correlation of the 4977 bp mitochondrial DNA deletion with human sperm dysfunction, BMC Res. Notes, 2, 18.PubMedCentralPubMedCrossRefGoogle Scholar
  105. 105.
    Holyoake, A. J., McHugh, P., Wu, M., O’ Carroll, S., Benny, P., Sin, I. L., and Sin, F. Y. (2001. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men, Int. J. Androl., 24, 175–182.PubMedCrossRefGoogle Scholar
  106. 106.
    White, D. J., Wolff, J. N., Pierson, M., and Gemmell, N. J. (2008. Revealing the hidden complexities of mtDNA inheritance, Mol. Ecol., 17, 4925–4942.PubMedCrossRefGoogle Scholar
  107. 107.
    Zeh, J. A., and Zeh, D. W. (2005. Maternal inheritance, sexual conflict, and the maladapted male, Trends Genet., 21, 281–286.PubMedCrossRefGoogle Scholar
  108. 108.
    Gemmell, N. J., and Sin, F. Y. (2002. Mitochondrial mutations may drive Y chromosome evolution, BioEssays, 24, 275–279.PubMedCrossRefGoogle Scholar
  109. 109.
    Innocenti, P., Morrow, E. H., and Dowling, D. K. (2011. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution, Science, 332, 845–848.PubMedCrossRefGoogle Scholar
  110. 110.
    Clancy, D. J. (2008. Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background, Aging Cell, 7, 795–804.PubMedCrossRefGoogle Scholar
  111. 111.
    Golob, M. J., Tian, L., Wang, Z., Zimmerman, T., Caneba, C., Hacker, T., Song, G., and Chesler, N. C. (2015. Mitochondria DNA mutations cause sex-dependent development of hypertension and alterations in cardiovascular function, J. Biomech., 48, 405–412.PubMedCrossRefGoogle Scholar
  112. 112.
    Camus, M. F., Clancy, D. J., and Dowling, D. K. (2012. Mitochondria, maternal inheritance, and male aging, Curr. Biol., 22, 1717–1721.PubMedCrossRefGoogle Scholar
  113. 113.
    Kujoth, G. C., Bradshaw, P. C., Haroon, S., and Prolla, T. A. (2007. The role of mitochondrial DNA mutations in mammalian aging, PLoS Genet., 3, 161–173.CrossRefGoogle Scholar
  114. 114.
    Schapira, A. H. (2012. Mitochondrial diseases, Lancet, 379, 1825–1834.PubMedCrossRefGoogle Scholar
  115. 115.
    Sekirov, I., Russell, S. L., Antunes, L. C., and Finlay, B. B. (2010. Gut microbiota in health and disease, Physiol. Rev., 90, 859–904.PubMedCrossRefGoogle Scholar
  116. 116.
    Zorov, D. B., Plotnikov, E. Y., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Zorov, S. D., Babenko, V. A., Jankauskas, S. S., Popkov, V. A., and Savina, P. S. (2014. Microbiota and mitobiota. Putting an equal sign between mitochondria and bacteria, Biochemistry (Moscow), 79, 1017–1031.CrossRefGoogle Scholar
  117. 117.
    Speakman, J. R. (2005. Body size, energy metabolism, and lifespan, J. Exp. Biol., 208, 1717–1730.PubMedCrossRefGoogle Scholar
  118. 118.
    Fontana, L., Partridge, L., and Longo, V. D. (2010. Extending healthy life span–from yeast to humans, Science, 328, 321–326.PubMedCentralPubMedCrossRefGoogle Scholar
  119. 119.
    Geodakian, V. A. (1991. Evolutionary theory of sex, Priroda, 8, 60–69.Google Scholar
  120. 120.
    Zahavi, A. (1975. Mate selection–a selection for a handicap, J. Theor. Biol., 53, 205–214.PubMedCrossRefGoogle Scholar
  121. 121.
    Skulachev, V. P. (2004) Model Systems in Aging, Springer Berlin Heidelberg, Berlin, Heidelberg.Google Scholar
  122. 122.
    Croft, D. P., Brent, L. J., Franks, D. W., and Cant, M. A. (2015. The evolution of prolonged life after reproduction, Trends Ecol. Evol., 30, 407–416.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • V. A. Popkov
    • 1
  • E. Yu. Plotnikov
    • 1
  • D. N. Silachev
    • 1
  • L. D. Zorova
    • 2
  • I. B. Pevzner
    • 1
  • S. S. Jankauskas
    • 1
  • S. D. Zorov
    • 3
  • V. A. Babenko
    • 3
  • D. B. Zorov
    • 1
  1. 1.Lomonosov Moscow State UniversityBelozersky Institute of Physico-Chemical BiologyMoscowRussia
  2. 2.Lomonosov Moscow State UniversityInternational Laser CenterMoscowRussia
  3. 3.Lomonosov Moscow State UniversityFaculty of Bioengineering and BioinformaticsMoscowRussia

Personalised recommendations