MITOCHONDRIAL DYSFUNCTION AS POSSIBLE CAUSE OF IMPAIRED FOLLICULAR DEVELOPMENT
Abstract
Mitochondria play leading role in senescence program realization. One of the early manifestations of this process is loss of reproductive function in female (menopause). In this review we discuss up-to-date data on basic mitochondria functions and their possible role in development of premature ovarian insufficienсy and morbid conditions associated with this state, that are typical for ageing organism. Besides performing function of conversion of free energy by cell respiration substrates oxidation mitochondria control survival and death of somatic cells and gametes maintaining optimal level of reactive oxygen species in cells. Oxidative stress results in selective death of specialized cells; organs and tissues functionality disturbance; leads to development of cardiovascular, locomotor and nervous disorders. The main reason of oxidative stress is mitochondrial disfunction induced by disbalance between reactive oxygen species production and their utilization by antioxidant system. On the other hand mitochondria play central role in intracellular signal transmission and maintain functional state and cellular structure of tissues, organs and systems of an organism controlling cell proliferation, differentiation and apoptosis. Finally mitochondria define largely immune response in case of infections and tumoral transformation and control sex hormones level taking part in steroidogenesis. It was found that high level of damaged mitochondrial DNA, decrease of its copy number and increase of reactive oxygen species production in ovarian tissue cells are typical for women suffering from premature ovarian insufficienсy. Chronic oxidative stress leads not only to oogenesis disturbance and decrease of oocyte maturation probability but promotes also cardiovascular diseases, osteoporosis and other delayed consequences of estrogen deficit development in case of this state.
About the Authors
A. A. Pozdnyakova
Research Center for Obstetrics, Gynecology and Perinatology of the Ministry of Healthcare of the Russian Federation
Russian Federation
the graduate student of office of gynecologic endocrinology
Russian Federation
the graduate student of office of gynecologic endocrinology
M. A. Volodina
Research Center for Obstetrics, Gynecology and Perinatology of the Ministry of Healthcare of the Russian Federation
Russian Federation
PhD, researcher at mitochondrial medicine research group
Russian Federation
PhD, researcher at mitochondrial medicine research group
S. J. Rshtuni
Research Center for Obstetrics, Gynecology and Perinatology of the Ministry of Healthcare of the Russian Federation
Russian Federation
the graduate student of office of gynecologic endocrinology
Russian Federation
the graduate student of office of gynecologic endocrinology
L. A. Marchenko
Research Center for Obstetrics, Gynecology and Perinatology of the Ministry of Healthcare of the Russian Federation
Russian Federation
the doctor of medical sciences, the professor, the leading researcher
Russian Federation
the doctor of medical sciences, the professor, the leading researcher
M. Yu. Vysokikh
Research Center for Obstetrics, Gynecology and Perinatology of the Ministry of Healthcare of the Russian Federation, Subdivision of Moscow State University "Scientific Research Institute of Physico-Chemical Biology named after AN Belozersky", Moscow
Russian Federation
PhD, Head of mitochondrial medicine research group
Russian Federation
PhD, Head of mitochondrial medicine research group
References
1. Weismann A. Lectures on theory of evolution: Held at the University of Freiburg in Breisgau. prof. August Weismann. Petrograd. 1918.
2. Galimov E.R. The role of p66shc in oxidative stress and apoptosis. Acta Naturae (In Russian). 2010; 2 (4): 49-57.
3. Rumyantseva S.A., Stupin V.A., Afanas'ev V.V. et al. Critical states in clinical practice (In Russian). Moscow. 2011; 752.
4. Skulachev V. P. Phenoptosis: programmed death of an organism. Biochemistry (In Russian). 1999; 64(12): 1418-26.
5. Skulachev V.P., Bogachev A.V., Kasparinsky F.O. Membrane Bioenergetics (In Russian). Moscow. 2010; 368.
6. Tagieva G.V. The role of the autoimmune process in the genesis of a premature ovarian insufficiency (In Russian). PhD Diss. Moscow. 2005; 178.
7. Berniakovich I., Trinei M., Stendardo M., Migliaccio E., Minucci S., Bernardi P., Pelicci P.G., Giorgio M. p66Shc-generated oxidative signal promotes fat accumulation. J. Biol. Chem. 2008; 283 (49): 34283-34293.
8. Boland N.I., Humpherson P.G., Leese H.J., Gosden R.G. Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro. Biol Reprod. 1993; 48: 798-806.
9. Bonomi M., Somigliana E., Cacciatore C., Busnelli M., Rossetti R. et al. Blood Cell Mitochondrial DNA Content and Premature Ovarian Aging. PLoS ONE. 2012; 7 (8): 42423.
10. Bormann J., Ferrero P., Guidotti A., Costa E. Neuropeptide modulation of GABA receptor C1-channels. Regulatory Peptides. 1985; 4: 33-38.
11. Camici G.G., Schiavoni M., Francia P., Bachschmid M., Martin-Padura I., Hersberger M., Tanner F.C., Pelicci P., Volpe M., Anversa P., Lüscher T.F., Cosentino F. Genetic deletion of p66(Shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc. Natl. Acad. Sci. USA. 2007; 104: 5217-5222.
12. Chelli B., Lena A., Vanacore R. et al. Peripheral benzodiazepine receptor ligands: mitochondrial transmembrane potential depolarization and apoptosis induction in rat C6 glioma cells. Biochem. Pharmacol. 2004; 68: 125-134.
13. Cutler R.G., Rodriguez H. Critical reviews of oxidative stress and aging: advances in basic science, diagnostics and intervention. World Scientific. 2003; 1523.
14. Dimmer K., Scorrano S.L. (De)constructing mitochondria: what for? Physiology. 2006; 21: 233-241.
15. Dolder M., Wendt S., Wallimann T. Mitochondrial creatine kinase in contact sites: interaction with porin and adenine nucleotide translocase, role in permeability transition and sensitivity to oxidative damage. Biol. Signals Recept. 2001; 10: 93-111.
16. Dumollard R., Duchen M., Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007; 77: 21-49.
17. Evans M.D., Cooke M.S. Oxidative damage to nucleic acids. New York: Springer Science & Business. LLS 2007; 228.
18. Fagiani E., Giardina G., Luzi L., Cesaroni M., Quarto M., Capra M., Germano G., Bono M., Capillo M., Pelicci P., Lanfrancone L. RaLP, a new member of the Src homology and collagen family, regulates cell migration and tumor growth of metastatic melanomas. Cancer Res. 2007; 67 (7): 3064-3073.
19. Ferzaz B., Brault E., Bourliaud G. et al. SSR180575 (7-chloro-N,N,5-trimethyl-4-oxo-3-phenyl-3,5-dihydro-4H-pyridazino[4,5-b] indole-1-acetamide), a peripheral benzodiazepine receptor ligand, promotes neuronal survival and repair. J. Pharmacol. Experim. Therapeuts. 2002; 301: 1067-1078.
20. File S.E., Pellow S. Ro5-4864, a ligand for benzodiazepine micromolar and peripheral binding sites: antagonism and enhancement of behavioural effects. Psychopharmacol. 1983; 80: 166-170
21. Friedman J.R., Nunnar J. Mitochondrial form and function. Nature. 2014; 505: 335-43.
22. Fu X.D., Simoncini T. Extra-nuclear signaling of estrogen receptors. IUBMB Life. 2008; 60: 502-510.
23. Galiègue S., Casellas P., Kramar A. et al. Immunohistochemical assessment of the peripheral benzodiazepine receptor in breast cancer and its relationship with survival. Clin. Cancer Res. 2004; 10: 2058-2064.
24. Gavish M., Bachman I., Shoukrun R. et al. Enigma of the peripheral benzodiazepine receptor. Pharmacol. Rev. 1999; 51: 629-650.
25. Giorgio M., Migliaccio E., Orsini F., Paolucci D., Moroni M., Contursi C., Pelliccia G., Luzi L., Minucci S., Marcaccio M., Pinton P., Rizzuto R., Bernardi P., Paolucci F., Pelicci P.G. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell. 2005; 122: 221-233.
26. Guevara R., Gianotti M., Oliver J., Roca P. Age and sex-related changes in rat brain mitochondrial oxidative status. Exp. Gerontol. 2011; 46: 923-928.
27. Halliwell B., Gutteridge J.М.С. Free Radicals in Biology and Medicine. 4th ed. Oxford: Oxford University Press. 2007; 851.
28. Harris S.E., Leese H.J., Gosden R.G., Picton H.M. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes. Mol Reprod Dev. 2009; 76: 231-238.
29. Harman D. Aging: A theory based on free radicals and radiation chemistry. J. Gerontol. 1956; 11: 298-300.
30. Hicsonmez G. The effect of steroid on myeloid leukemic cells: the potential of short-course highdose methylprednisolone treatment in inducing differentiation, apoptosis and in stimulating myelopoiesis. Leuk. Res. 2006; 30: 60-68.
31. Jansen R.P., de Boer K. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol. 1998; 145: 81-88.
32. Kancheva V.D., Kasaikina O.T. Bio-antioxidants – a chemical base of their antioxidant activity and beneficial effect on human health. Curr Med Chem. 2013; 20 (37): 4784-805.
33. Keanely J.F. Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham study. Arterioscler Thromb Vasc Biol. 2003; 23: 434-9.
34. Kolesnikova L.I., Darenskaya M.A., Grebenkina L.A., et al. Activity of lipid peroxidation in infertile women from different populations. Bull Exp Bio Med. 2012; 154 (2): 203-5.
35. Kumar M., D. Pathak, S. Venkatesh, A. Kriplani, A.C. Ammini, Rima Dada. Chromosomal abnormalities & oxidative stress in women with premature ovarian failure (POF). Indian J Med Res. 2012 Jan; 135 (1): 92-97.
36. Kwang-Yul Cha, Sook-Hwan Lee, Hyung-Min Chung, Kwang-Hyun Baek, Sung-Won Cho, Kyu-Bum Kwack. RETRACTED: Quantification of mitochondrial DNA using real-time polymerase chain reaction in patients with premature ovarian failure. Fertility and Sterility. 2005; 84 (6): 1712-1718.
37. Lebiedzinska M., Karkucinska-Wieckowska A., Giorgi C., Karczmarewicz E., Pronicka E., Pinton P., Duszynski J., Pronicki M., Wieckowski M.R. Biochim. Biophys. Acta. 2010; 1797 (6-7): 952-960.
38. Leneveu-Jenvrin C, Connil N, Bouffartigues E, Papadopoulos V, Feuilloley M.G.J., Chevalier S. Structure-to-function relationships of bacterial translocator protein (TSPO): a focus on Pseudomonas. Front. Microbiol. 2014; 5: 631.
39. Li W., Hardwick M.J., Rosenthal D. et al. Peripheral-type benzodiazepine receptor overexpression and knockdown in human breast cancer cells indicate its prominent role in tumor cell proliferation. Biochem. Pharmacol. 2007; 73: 491-503.
40. Liu H., Pedram A., Kim J.K. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38α-mediated activation of p53 and by down-regulating p53 inhibition on p38β. Cardiovasc. Res. 2011; 1: 119-128.
41. Lizcano F., Guzman G. Estrogen deficiency and the origin of obesity during menopause. Biomed Res Int. 2014; ID 757461.
42. Longo V.D., Mitteldorf J., Skulachev V.P. Programmed and altruistic ageing. Nature Review Genetics. 2005; 3: 866-872.
43. Luoma P., Melberg A., Rinne J.O., Kaukonen J.A., Nupponen N.N. et al. Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet. 2004; 364: 875-882.
44. Luzi L., Confalonieri S., Di Fiore P.P., Pelicci P.G. Evolution of Shc functions from nematode to human. Curr. Opin. Genet. Dev. 2000; 10 (6): 668-674.
45. Maaser K., Grabowski P., Sutter A.P. et al. Overexpression of the peripheral benzodiazepine receptor is a relevant prognostic factor in stage III colorectal cancer. Clin. Cancer Res. 2002; 8: 3205-3209.
46. Maclaran K., Panay N. Current concepts in premature ovarian insufficiency. Womens Health (Lond Engl). 2015 Mar; 11 (2): 169-82.
47. Mastorakos G., Pavlatou M., Diamanti-Kandarakis E., Chrousos G.P. Exercise and the stress system. Hormones (Athens). 2005; 4: 73-89.
48. May-Panloup P., Chretien M.F., Jacques C., Vasseur C., Malthiery Y. et al. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod. 2005; 20: 593-597.
49. May-Panloup P., Chretien M.F., Malthiery Y., Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol. 2007; 77: 51-83.
50. Migliaccio E., Giorgio M., Mele S., Pelicci G., Reboldi P., Pandolfi P.P., Lanfrancone L., Pelicci P.G. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 1999; 402: 309-313.
51. Miller L., Hunt J.S. Sex steroid hormones and macrophage function. Life Sci. 1996; 59: 1-14.
52. Miquel J., Ramirez-Bosca A., Ramirez-Bosca J.V., Alperi J.D. Menopause: a review on the role of oxygen stress and favorable effects of dietary antioxidants. Arch Geron Geriat. 2006; 42: 289-306.
53. Morohaku K., Phuong N.S., Selvaraj V. Developmental Expression of Translocator Protein/Peripheral Benzodiazepine Receptor in Reproductive Tissues. PLoS ONE. 2013; 8 (9): e74509.
54. Napoli C., Martin-Padura I., de Nigris F., Giorgio M., Mansueto G., Somma P., Condorelli M., Sica G., De Rosa G., Pelicci P. Proc. Natl. Acad. Sci. USA. 2003; 100 (4): 2112-2116.
55. Nemoto S., Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science. 2002; 295 (5564): 2450-2452.
56. Niizuma K., Endo H., Chan P. Oxidative stress and mitochondrial dysfunction as determinants of ischemic neuronal death and survival. J Neurochem. 2009; 109: 133-138.
57. Ogunro P.S., Bolarinde A.A., Owa O.O., Salawu A.A., Oshodi A.A. Antioxidant status and reproductive hormones in women during reproductive, perimenopausal and postmenopausal phase of life. Afr J Med Sci. 2014; 43 (1): 49-57.
58. Orsini F., Migliaccio E., Moroni M., Contursi C., Raker V.A., Piccini D., Martin-Padura I., Pelliccia G., Trinei M., Bono M., Puri C., Tacchetti C., Ferrini M., Mannucci R., Nicoletti I., Lanfrancone L., Giorgio M., Pelicci P.G. J. Biol. Chem. 2004; 279 (24): 25689-25695.
59. Pagnamenta A.T., Taanman J.W., Wilson C.J., Anderson N.E., Marotta R., et al. Dominant inheritance of premature ovarian failure associated with mutant mitochondrial DNA polymerase gamma. Hum Reprod. 2006; 21: 2467-2473.
60. Papadopoulos V. In search of the function of the peripheral-type benzodiazepine receptor. Endocr. Res. 2004; 30: 677-684.
61. Papadopoulos V., Baraldi M., Guilarte T.R. et al. Translocator protein (18kDa): new nomenclature for the peripheraltype benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol. Sci. 2006; 27: 402-409.
62. Papadopoulos V., Boujrad N., Ikonomovic M.D. et al. Topography of the Leydig cell mitochondrial peripheraltype benzodiazepine receptor. Mol. Cell Endocrinol. 1994; 104: 5-9.
63. Qin Y., Jiao X., Simpson J.L., Chen Z.J. Genetics of primary ovarian insufficiency: new developments and opportunities. Hum Reprod Update. 2015 Nov; 21 (6): 787-808.
64. Ramalho-Santos J., Varum S., Amaral S., Mota P.C., Sousa A.P., Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum. Reprod. Update. 2009; 15: 553-72.
65. Simpson E.R., Waterman M.R. Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can. J. Biochem. Cell Biol. 1983; 61: 692-707.
66. Shoubridge E.A., Wai T. Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol. 2007; 77: 87-111.
67. Smith W.W., Norton D.D., Gorospe M., Jiang H., Nemoto S., Holbrook N.J., Finkel T., Kusiak J.W. Phosphorylation of p66Shc and forkhead proteins mediates Abeta toxicity. J. Cell Biol. 2005; 169 (2): 331-339.
68. Stirone, C., Duckles S.P., Krause D.N., Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol. Pharmacol. 2005; (68): 959-965.
69. Tatone C., Carbone M.C., Falone S., Aimola P., Giardinelli A. et al. Agedependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod. 2006; 12: 655-660.
70. van Blerkom J., Davis P.W., Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod. 1995; 10: 415-424.
71. Veenman L., Gavish M. The peripheral-type benzodiazepine receptor and the cardiovascular system. Implications for drug development. Pharmacol. Ther. 2006; 110: 503-524.
72. Veenman L., Leschiner S., Spanier I. et al. PK11195 attenuates kainic acid-induced seizures and alterations in peripheral-type benzodiazepine receptor (PBR) components in the rat brain. J. Neurochem. 2002; 80: 917-927.
73. Veenman L., Papadopoulos V., Gavish M. Channel-Like Functions of the 18-kDa Translocator Protein (TSPO): Regulation of Apoptosis and Steroidogenesis as Part of the Host-Defense Response. Curr. Pharm. Des. 2007; 13: 2385-2405.
74. Venkatesh S., Kumar M., Sharma A., Kriplani A., Ammin A. C., Talwar P., Agarwal A., Rima Dada. Oxidative stress and ATPase6 mutation is associated with primary ovarian insufficiency. Arch Gynecol Obstet. 2010; 282: 313-318.
75. Viña J., Sastre J., Pallardó F.V., Gambini J., Borrás C. Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic. 2006 Dec; 40: 1359-1365.
76. Vyssokikh M.Y., Brdiczka D. The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism andapoptosis. Acta. Biochim. Pol. 2003; 50: 389-404.
77. Wai T., Ao A., Zhang X., Cyr D., Dufort D. et al. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod. 2010; 83: 52-62.
78. West L.A., Horvat R.D., Roess D.A. et al. Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology. 2001; 142: 502-505.
79. Wycherley G., Kane M.T., Hynes A.C. Oxidative phosphorylation and the tricarboxylic acid cycle are essential for normal development of mouse ovarian follicles. Hum Reprod. 2005; 20: 2757-2763.
80.
For citation:
Pozdnyakova A.A., Volodina M.A., Rshtuni S.J., Marchenko L.A., Vysokikh M.Yu. MITOCHONDRIAL DYSFUNCTION AS POSSIBLE CAUSE OF IMPAIRED FOLLICULAR DEVELOPMENT. Obstetrics, Gynecology and Reproduction. 2015;9(4):55-65. (In Russ.) https://doi.org/10.17749/2070-4968.2015.9.4.055-065
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