Skip to main content
SpringerLink
Log in

Diseases and aging: Gender matters

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

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.

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

Abbreviations

ROS:

reactive oxygen species

References

  1. World Health Organization, Annual Report (2012).

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  9. Sandberg, K. (2008. Mechanisms underlying sex differences in progressive renal disease, Gend. Med., 5, 10–23.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  11. Harrison-Bernard, L. M., and Raij, L. (2000. Postmenopausal hypertension, Curr. Hypertens. Rep., 2, 202–207.

    Article  CAS  PubMed  Google Scholar 

  12. Rosen, C. J. (2005. Postmenopausal osteoporosis, Bone, 8, 595–603.

    Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  19. Aharon, A., Zandman-Goddard, G., and Shoenfeld, Y. (1994. Autoimmune multiorgan involvement in elderly men is it SLE? Clin. Rheumatol., 13, 631–634.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  21. Jimenez-Balderas, F. J., and Mintz, G. (1993. Ankylosing spondylitis: clinical course in women and men, J. Rheumatol., 20, 2069–2072.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

  25. Manigrasso, M. B., and Maric-Bilkan, C. (2013) Peptides, sex, diabetes, and the kidney, in Handbook in Biologically Active Peptides, pp. 1487–1493.

    Chapter  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  27. Beatty, W. W., and Aupperle, R. L. (2002. Sex differences in cognitive impairment in multiple sclerosis, Clin. Neuropsychol., 16, 472–480.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  30. Sheikh, K., and Bullock, C. M. (2007. Effect of measurement on sex difference in stroke mortality, Stroke, 38, 10851087.

    Article  Google Scholar 

  31. McHugh, J. C., and Delanty, N. (2008. Epidemiology and classification of epilepsy: gender comparisons, Int. Rev. Neurobiol., 83, 11–26.

    Article  PubMed  Google Scholar 

  32. Oertelt-Prigione, V., and Regitz-Zagrosek, V. (2012) Sex and Gender Aspects in Clinical Medicine, Springer-Verlag, London.

    Book  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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. 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  38. Glucksmann, A. (1981) Sexual Dimorphism in Human and Mammalian Biology and Pathology, Academic Press, London-New York.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  40. Neugarten, J., Kasiske, B., Silbiger, S. R., and Nyengaard, J. R. (2002. Effects of sex on renal structure, Nephron, 90, 139–144.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  45. Ankney, C. D. (1992. Sex differences in relative brain size: the mismeasure of woman, too? Intelligence, 16, 329–336.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  60. Lee, J., Giordano, S., and Zhang, J. (2011. Autophagy, mitochondria, and oxidative stress: cross-talk and redox signalling, Biochem. J., 441, 523–540.

    Article  PubMed Central  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  90. Graves, J. A. (2006. Sex chromosome specialization and degeneration in mammals, Cell, 124, 901–914.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  93. Hughes, I. A., and Deeb, A. (2006. Androgen resistance, Best Pract. Res. Clin. Endocrinol. Metab., 20, 577–598.

    Article  CAS  PubMed  Google Scholar 

  94. Greiner, S., Sobanski, J., and Bock, R. (2015. Why are most organelle genomes transmitted maternally? Bioessays, 37, 80–94.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  96. Woodson, J. D., and Chory, J. (2008. Coordination of gene expression between organellar and nuclear genomes, Nat. Rev. Genet., 9, 383–395.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  98. Wolff, J. N., and Gemmell, N. J. (2013. Mitochondria, maternal inheritance, and asymmetric fitness: why males die younger, BioEssays, 35, 93–99.

    Article  CAS  PubMed  Google Scholar 

  99. Wallace, D. C. (2010. Mitochondrial DNA mutations in disease and aging, Environ. Mol. Mutagen., 51, 440–450.

    CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  102. Greaves, L. C., Reeve, A. K., Taylor, R. W., and Turnbull, D. M. (2012. Mitochondrial DNA and disease, J. Pathol., 226, 274–286.

    Article  CAS  PubMed  Google Scholar 

  103. Schapira, A. H. (2012. Mitochondrial diseases, Lancet, 379, 1825–1834.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  107. Zeh, J. A., and Zeh, D. W. (2005. Maternal inheritance, sexual conflict, and the maladapted male, Trends Genet., 21, 281–286.

    Article  CAS  PubMed  Google Scholar 

  108. Gemmell, N. J., and Sin, F. Y. (2002. Mitochondrial mutations may drive Y chromosome evolution, BioEssays, 24, 275–279.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  112. Camus, M. F., Clancy, D. J., and Dowling, D. K. (2012. Mitochondria, maternal inheritance, and male aging, Curr. Biol., 22, 1717–1721.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  114. Schapira, A. H. (2012. Mitochondrial diseases, Lancet, 379, 1825–1834.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  117. Speakman, J. R. (2005. Body size, energy metabolism, and lifespan, J. Exp. Biol., 208, 1717–1730.

    Article  PubMed  Google Scholar 

  118. Fontana, L., Partridge, L., and Longo, V. D. (2010. Extending healthy life span–from yeast to humans, Science, 328, 321–326.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  119. Geodakian, V. A. (1991. Evolutionary theory of sex, Priroda, 8, 60–69.

    Google Scholar 

  120. Zahavi, A. (1975. Mate selection–a selection for a handicap, J. Theor. Biol., 53, 205–214.

    Article  CAS  PubMed  Google Scholar 

  121. Skulachev, V. P. (2004) Model Systems in Aging, Springer Berlin Heidelberg, Berlin, Heidelberg.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

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

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

  2. Lomonosov Moscow State University, International Laser Center, 119991, Moscow, Russia

    L. D. Zorova

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

    S. D. Zorov & V. A. Babenko

Authors
  1. V. A. Popkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Yu. Plotnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. N. Silachev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. D. Zorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. B. Pevzner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. S. Jankauskas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. D. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. V. A. Babenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. D. B. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Yu. Plotnikov.

Additional information

Original Russian Text © 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, 2015, published in Biokhimiya, 2015, Vol. 80, No. 12, pp. 1817-1829.

To whom correspondence should be addressed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popkov, V.A., Plotnikov, E.Y., Silachev, D.N. et al. Diseases and aging: Gender matters. Biochemistry Moscow 80, 1560–1570 (2015). https://doi.org/10.1134/S0006297915120032

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297915120032

Keywords

Search

Navigation