Melatonin as Potential Targets for Delaying Ovarian Aging

Author(s): Yanzhou Yang*, Hoi-Hung Cheung, Cheng Zhang, Ji Wu, Wai-Yee Chan.

Journal Name: Current Drug Targets

Volume 20 , Issue 1 , 2019

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Abstract:

In previous studies, oxidative stress damage has been solely considered to be the mechanism of ovarian aging, and several antioxidants have been used to delay ovarian aging. But recently, more reports have found that endoplasmic reticulum stress, autophagy, sirtuins, mitochondrial dysfunction, telomeres, gene mutation, premature ovarian failure, and polycystic ovary syndrome are all closely related to ovarian aging, and these factors all interact with oxidative stress. These novel insights on ovarian aging are summarized in this review. Furthermore, as a pleiotropic molecule, melatonin is an important antioxidant and used as drugs for several diseases treatment. Melatonin regulates not only oxidative stress, but also the various molecules, and normal and pathological processes interact with ovarian functions and aging. Hence, the mechanism of ovarian aging and the extensive role of melatonin in the ovarian aging process are described herein. This systematic review supply new insights into ovarian aging and the use of melatonin to delay its onset, further supply a novel drug of melatonin for ovarian aging treatment.

Keywords: Melatonin, oxidative stress, endoplasmic reticulum stress, autophagy, ovarian aging.

[1]
Steiner AZ, Jukic AM. Impact of female age and nulligravidity on fecundity in an older reproductive age cohort. Fertil Steril 2016; 05: 584-1588.
[2]
Suganuma N, Kitagawa T, Nawa A, Tomoda Y. Human ovarian aging and mitochondrial DNA deletion. Horm Res 1993; 39: 6-21.
[3]
Faddy MJ. Follicle dynamics during ovarian ageing. Mol Cell Endocrinol 2000; 163: 3-48.
[4]
Tamura H, Kawamoto M, Sato S, et al. Long-term melatonin treatment delays ovarian aging. J Pineal Res 2017; 62: 2381.
[5]
Handyside AH, Montag M, Magli MC, et al. Multiple meiotic errors caused by predivision of chromatids in women of advanced maternal age undergoing in vitro fertilisation. Eur J Hum Genet 2012; 20: 42-747.
[6]
Liu XJ. Targeting oocyte maturation to improve fertility in older women. Cell Tissue Res 2016; 363: 7-68.
[7]
Broekmans FJ, Soules MR, Fauser BC. Ovarian aging: mechanisms and clinical consequences. Endocr Rev 2009; 0: 65-493.
[8]
Li Q, Geng X, Zheng W, Tang J, Xu B, Shi Q. Current understanding of ovarian aging. Sci China Life Sci 2012; 55: 59-669.
[9]
Bancsi LF, Broekmans FJ, Eijkemans MJ, de Jong FH, Habbema JD, te Velde ER. Predictors of poor ovarian response in in vitro fertilization: a prospective study comparing basal markers of ovarian reserve. Fertil Steril 2002; 7: 28-336.
[10]
Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K. Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging (Albany NY) 2011; 3: 82-793.
[11]
Sükür YE, Kıvançl IB, Ozmen B. Ovarian aging and premature ovarian failure. J Turk Ger Gynecol Assoc 2014; 15: 90-196.
[12]
Reiter RJ, Tan DX, Galano A. Melatonin: exceeding expectations. Physiology (Bethesda) 2014; 29: 25-333.
[13]
Xie Z, Chen F, Li WA, et al. A review of sleep disorders and melatoninNeurol Res 2017. 1: -7
[14]
Li Y, Li S, Zhou Y, et al. Melatonin for the prevention and treatment of cancer. Oncotarget 2017; 8: 9896-39921.
[15]
Majidinia M, Sadeghpour A, Mehrzadi S, Reiter RJ, Khatami N, Yousefi B. Melatonin: a pleiotropic molecule that modulates DNA damage response and repair pathways. J Pineal Res 2017; 63: 2416.
[16]
Reiter RJ, Rosales-Corral SA, Tan DX, et al. Melatonin, a Full Service Anti-Cancer Agent: Inhibition of Initiation, Progression and Metastasis. Int J Mol Sci 2017; 18: E843.
[17]
Su SC, Hsieh MJ, Yang WE, Chung WH, Reiter RJ, Yang SF. Cancer metastasis: Mechanisms of inhibition by melatonin. J Pineal Res 2017; 62: 2370.
[18]
Farez MF, Calandri IL, Correale J, Quintana FJ. Anti-inflammatory effects of melatonin in multiple sclerosis. Bioessays 2016. 38: 016- 1026
[19]
Calvo JR, González-Yanes C, Maldonado MD. The role of melatonin in the cells of the innate immunity: a review. J Pineal Res 2013. 55: 03-120
[20]
Radogna F, Diederich M, Ghibelli L. Melatonin: a pleiotropic molecule regulating inflammation. Biochem Pharmacol 2010; 80: 844-1852.
[21]
Esposito E, Cuzzocrea S. Antiinflammatory activity of melatonin in central nervous system. Curr Neuropharmacol 2010; 8: 28-242.
[22]
Kalpakcioglu B, Senel K. The role of melatonin in rheumatic diseases. Infect Disord Drug Targets 2009; 9: 53-456.
[23]
Srinivasan V, Ohta Y, Espino J, et al. Metabolic syndrome, its pathophysiology and the role of melatonin. Recent Pat Endocr Metab Immune Drug Discov 2013; 7: 1-25.
[24]
Hardeland R. Melatonin and the theories of aging: a critical appraisal of melatonin’s role in antiaging mechanisms. J Pineal Res 2013; 55: 25-356.
[25]
Chen Q, Wang Q, Zhu J, Xiao Q, Zhang L. Reactive Oxygen Species: Key Regulators in Vascular Health and Diseases. Br J Pharmacol 2018; 175: 279-1292.
[26]
Wang XN, Zhang CJ, Diao HL, Zhang Y. Protective Effects of Curcumin against Sodium Arsenite-induced Ovarian Oxidative Injury in a Mouse Model. Chin Med J (Engl) 2017. 130: 026-1032.
[27]
Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: A review. Reprod Biol Endocrinol 2012; 10: 9.
[28]
Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005; 3: 8.
[29]
Pertynska-Marczewska M, Diamanti-Kandarakis E. Aging ovary and the role for advanced glycation end products. Menopause 2017; 24: 45-351.
[30]
Shi L, Zhang J, Lai Z, et al. Long-Term Moderate Oxidative Stress Decreased Ovarian Reproductive Function by Reducing Follicle Quality and Progesterone Production. PLoS One 2016; 11: e0162194.
[31]
Yeh J, Bowman MJ, Browne RW, Chen N. Reproductive aging results in a reconfigured ovarian antioxidant defense profile in rats. Fertil Steril 2005; 84: 109-1113.
[32]
Lim J, Luderer U. Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol Reprod 2011; 84: 75-782.
[33]
Elizur SE, Lebovitz O, Orvieto R, Dor J, Zan-Bar T. Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. Gynecol Endocrinol 2014. 30: 05-707.
[34]
Liang LF, Qi ST, Xian YX, Huang L, Sun XF, Wang WH. Protective effect of antioxidants on the pre-maturation aging of mouse oocytes. Sci Rep 2017; 7: 434.
[35]
Stefanatos R, Sanz A. The role of mitochondrial ROS in the aging brain. FEBS Lett 2018; 92: 43-758.
[36]
Wang S, Ge W, Harns C, Meng X, Zhang Y, Ren J. Ablation of toll-like receptor 4 attenuates aging-induced myocardial remodeling and contractile dysfunction through NCoRI-HDAC1-mediated regulation of autophagy. J Mol Cell Cardiol 192018; : 0-50.
[37]
Ren J, Yang L, Zhu L, et al. Akt2 ablation prolongs life span and improves myocardial contractile function with adaptive cardiac remodeling: role of Sirt1-mediated autophagy regulation. Aging Cell 2017; 6: 76-987.
[38]
El Assar M, Fernández A, Sánchez-Ferrer A, Angulo J, Rodríguez-Mañas L. Multivessel analysis of progressive vascular aging in the rat: Asynchronous vulnerability among vascular territories. Mech Ageing Dev 2018 S0047-6374:: 0257-30259..
[39]
Sultana Z, Maiti K, Aitken J, Morris J, Dedman L, Smith R. Oxidative stress, placental ageing-related pathologies and adverse pregnancy outcomes. Am J Reprod Immunol 2017; 7: 2653.
[40]
Niemann J, Johne C, Schröder S, et al. An mtDNA mutation accelerates liver aging by interfering with the ROS response and mitochondrial life cycle. Free Radic Biol Med 2017; 02: 74-187.
[41]
Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290: 717-1721.
[42]
Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 63-477.
[43]
Lim HJ, Song H. Evolving tales of autophagy in early reproductive events. Int J Dev Biol 2014; 58: 83-187.
[44]
Yang Y, Cheung HH, Law WN, et al. New Insights into the Role of Autophagy in Ovarian Cryopreservation by Vitrification. Biol Reprod 2016; 94: 37.
[45]
Findlay JK, Hutt KJ, Hickey M, Anderson RA. How Is the Number of Primordial Follicles in the Ovarian Reserve Established? Biol Reprod 2015; 93: 11.
[46]
Klinger FG, Rossi V, De Felici M. Multifaceted programmed cell death in the mammalian fetal ovary. Int J Dev Biol 2015; 59: 1-54.
[47]
Yuan J, Zhang Y, Sheng Y, Fu X, Cheng H, Zhou R. MYBL2 guides autophagy suppressor VDAC2 in the developing ovary to inhibit autophagy through a complex of VDAC2-BECN1-BCL2L1 in mammals. Autophagy 112015; : 081-1098..
[48]
Sugiyama M, Kawahara-Miki R, Kawana H, Shirasuna K, Kuwayama T, Iwata H. Resveratrol-induced mitochondrial synthesis and autophagy in oocytes derived from early antral follicles of aged cows. J Reprod Dev 2015; 61: 51-259.
[49]
Hurst PR, Mora JM, Fenwick MA. Caspase-3, TUNEL and ultrastructural studies of small follicles in adult human ovarian biopsis. Hum Reprod 2006; 21: 974-1980.
[50]
Li L, Fu YC, Xu JJ, et al. Caloric Restriction Promotes the Reserve of Follicle Pool in Adult Female Rats by Inhibiting the Activation of Mammalian Target of Rapamycin Signaling. Reprod Sci 222015; : 0-67.
[51]
Gawriluk TR, Hale AN, Flaws JA, Dillon CP, Green DR, Rucker EB III. Autophagy is a cell survival program for female germ cells in the murine ovary. Reproduction 2011; 141: 59-765.
[52]
Song ZH, Yu HY, Wang P, et al. Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice. Cell Death Dis 2015; 6: e1589.
[53]
Reddy P, Liu L, Adhikari D, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008; 319: 11-613.
[54]
Banerjee S, Banerjee S, Saraswat G, Bandyopadhyay SA, Kabir SN. Female reproductive aging is master-planned at the level of ovary. PLoS One 2014; 9: e96210.
[55]
Yuan S, Wen J, Cheng J, et al. Age-associated up-regulation of EGR1 promotes granulosa cell apoptosis during follicle atresia in mice through the NF-κB pathway. Cell Cycle 2016; 15: 895-2905.
[56]
Luo LL, Xu JJ, Fu YC. Rapamycin prolongs female reproductive lifespan. Cell Cycle 2013; 12: 353-3354.
[57]
Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13: 211-1233.
[58]
Koumenis C. ER stress, hypoxia tolerance and tumor progression. Curr Mol Med 2006; 6: 55-69.
[59]
Yang Y, Pei X, Jin Y, Wang Y, Zhang C. The roles of endoplasmic reticulum stress response in female mammalian reproduction. Cell Tissue Res 2016; 363: 89-597.
[60]
Tatone C, Amicarelli F. The aging ovary--the poor granulosa cells. Fertil Steril 2013; 99: 2-17.
[61]
Guzel E, Arlier S, Guzeloglu-Kayisli O, et al. Endoplasmic Reticulum Stress and Homeostasis in Reproductive Physiology and Pathology. Int J Mol Sci 2017; 18: E792.
[62]
Lin P, Yang Y, Li X, et al. Endoplasmic reticulum stress is involved in granulosa cell apoptosis during follicular atresia in goat ovaries. Mol Reprod Dev 2012; 79: 23-432.
[63]
Yang Y, Lin P, Chen F, et al. Luman recruiting factor regulates endoplasmic reticulum stress in mouse ovarian granulosa cell apoptosis. Theriogenology 2013; 79: 33-639.
[64]
Zeng Y, Sun H, Li Y, et al. Exposure to triptolide affects follicle development in NIH mice: Role of endoplasmic reticulum stress in granulosa cell apoptosis. Hum Exp Toxicol In press
[65]
Huang N, Yu Y, Qiao J. Dual role for the unfolded protein response in the ovary: adaption and apoptosis. Protein Cell 2017; 8: 4-24.
[66]
Martínez G, Duran-Aniotz C, Cabral-Miranda F, Vivar JP, Hetz C. Endoplasmic reticulum proteostasis impairment in aging. Aging Cell 2017; 16: 15-623.
[67]
Taylor RC. Aging and the UPR(ER). Brain Res 2016; 1648: 88-593.
[68]
Matos L, Gouveia AM, Almeida H. ER Stress Response in Human Cellular Models of Senescence. J Gerontol A Biol Sci Med Sci 2015; 7: 24-935.
[69]
Brown MK, Chan MT, Zimmerman JE, Pack AI, Jackson NE, Naidoo N. Aging induced endoplasmic reticulum stress alters sleep and sleep homeostasis. Neurobiol Aging 2014; 35: 431-1441.
[70]
Labunskyy VM, Gerashchenko MV, Delaney JR, et al. Lifespan extension conferred by endoplasmic reticulum secretory pathway deficiency requires induction of the unfolded protein response. PLoS Genet 2014; 10: e1004019.
[71]
Sontag EM, Samant RS, Frydman J. Mechanisms and Functions of Spatial Protein Quality Control. Annu Rev Biochem 2017; 86: 7-122.
[72]
Höhn A, Weber D, Jung T, et al. Happily (n)ever after: Aging in the context of oxidative stress, proteostasis loss and cellular senescence. Redox Biol 2017; 11: 82-501.
[73]
Miller BF, Drake JC, Naylor B, Price JC, Hamilton KL. The measurement of protein synthesis for assessing proteostasis in studies of slowed aging. Ageing Res Rev 182014; : 06-111.
[74]
Hetz C, Chevet E, Oakes SA. Proteostasis control by the unfolded protein response. Nat Cell Biol 2015; 17: 29-838.
[75]
Jęśko H, Wencel P, Strosznajder RP, Strosznajder JB. Sirtuins and Their Roles in Brain Aging and Neurodegenerative Disorders. Neurochem Res 2017; 42: 76-890.
[76]
Carafa V, Rotili D, Forgione M, et al. Sirtuin functions and modulation: from chemistry to the clinic. Clin Epigenetics 2016; 8: 1.
[77]
Kida Y, Goligorsky MS. Sirtuins, Cell Senescence, and Vascular Aging. Can J Cardiol 2016; 32: 34-641.
[78]
Masri S. Sirtuin-dependent clock control: new advances in metabolism, aging and cancer. Curr Opin Clin Nutr Metab Care 2015; 18: 21-527.
[79]
Zhang J, Fang L, Lu Z, et al. Are sirtuins markers of ovarian aging? Gene 2016; 575: 80-686.
[80]
Wang N, Luo LL, Xu JJ, et al. Obesity accelerates ovarian follicle development and follicle loss in rats. Metabolism 2014; 63: 4-103.
[81]
Sirotkin AV. The Role and Application of Sirtuins and mTOR Signaling in the Control of Ovarian Functions. Cells 2016; 5: E42.
[82]
Cinco R, Digman MA, Gratton E, Luderer U. Spatial Characterization of Bioenergetics and Metabolism of Primordial to Preovulatory Follicles in Whole Ex Vivo Murine Ovary. Biol Reprod 2016; 95: 29.
[83]
Tao X, Zhang X, Ge SQ, Zhang EH, Zhang B. Expression of SIRT1 in the ovaries of rats with polycystic ovary syndrome before and after therapeutic intervention with exenatide. Int J Clin Exp Pathol 2015; 8: 276-8283.
[84]
Zhang L, Ma R, Hu J, Ding X, Xu Y. Sirtuin Inhibition Adversely Affects Porcine Oocyte Meiosis. PLoS One 2015; 10: e0132941.
[85]
Tatone C, Di Emidio G, Vitti M, et al. Sirtuin Functions in Female Fertility: Possible Role in Oxidative Stress and Aging. Oxid Med Cell Longev 2015; 2015: 59687.
[86]
Liu WJ, Zhang XM, Wang N, Zhou XL, Fu YC, Luo LL. Calorie restriction inhibits ovarian follicle development and follicle loss through activating SIRT1 signaling in mice. Eur J Med Res 2015; 20: 2.
[87]
Itami N, Shirasuna K, Kuwayama T, Iwata H. Resveratrol improves the quality of pig oocytes derived from early antral follicles through sirtuin 1 activation. Theriogenology 2015; 83: 360-1367.
[88]
Zhao F, Zhao W, Ren S, et al. Roles of SIRT1 in granulosa cell apoptosis during the process of follicular atresia in porcine ovary. Anim Reprod Sci 2014; 151: 4-41.
[89]
Zhou XL, Xu JJ, Ni YH, et al. SIRT1 activator (SRT1720) improves the follicle reserve and prolongs the ovarian lifespan of diet-induced obesity in female mice via activating SIRT1 and suppressing mTOR signaling. J Ovarian Res 2014; 7: 7.
[90]
Pacella-Ince L, Zander-Fox DL, Lan M. Mitochondrial SIRT3 and its target glutamate dehydrogenase are altered in follicular cells of women with reduced ovarian reserve or advanced maternal age. Hum Reprod 2014; 29: 490-1499.
[91]
Pavlová S, Klucska K, Vašíček D, et al. The involvement of SIRT1 and transcription factor NF-κB (p50/p65) in regulation of porcine ovarian cell function. Anim Reprod Sci 2013; 140: 80-188.
[92]
Zhang XM, Li L, Xu JJ, et al. Rapamycin preserves the follicle pool reserve and prolongs the ovarian lifespan of female rats via modulating mTOR activation and sirtuin expression. Gene 2013; 523: 2-87.
[93]
Luo LL, Chen XC, Fu YC, et al. The effects of caloric restriction and a high-fat diet on ovarian lifespan and the expression of SIRT1 and SIRT6 proteins in rats. Aging Clin Exp Res 2012; 24: 25-133.
[94]
Jia G, Su L, Singhal S, Liu X. Emerging roles of SIRT6 on telomere maintenance, DNA repair, metabolism and mammalian aging. Mol Cell Biochem 2012; 364: 45-350.
[95]
Brownlee M, Cerami A, Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 1988; 318: 315-1321.
[96]
Biswas SK. Soluble receptor for advanced glycation end products and insulin resistance during development of type 2 diabetes mellitus. J Diabetes Complications 2015; 29: 11.
[97]
Galì A, Mucciardi G, Butticè S, et al. Correlation Between Advanced Glycation End-Products, Lower Urinary Tract Symptoms and Bladder Dysfunctions in Patients with type 2 Diabetes Mellitus. Low Urin Tract Symptoms 2017; 9: 5-20.
[98]
Sánchez E, Baena-Fustegueras JA, de la Fuente MC, et al. Advanced glycation end-products in morbid obesity and after bariatric surgery: When glycemic memory starts to fail. Endocrinol Diabetes Nutr 2017; 64: -10
[99]
Lopez-Moreno J, Quintana-Navarro GM, Camargo A, et al. Dietary fat quantity and quality modifies advanced glycation end products metabolism in patients with metabolic syndrome. Mol Nutr Food Res 2017; 61: 01601029.
[100]
Hagen JM, Sutterland AL, Koeter MW, Lutter R, Cohen D, de Haan L. Advanced Glycation End Products in Recent-Onset Psychosis Indicate Early Onset of Cardiovascular Risk. J Clin Psychiatry 2017; 78: 395-1401.
[101]
Prasad C, Imrhan V, Marotta F, Juma S, Vijayagopal P. Lifestyle and Advanced Glycation End Products (AGEs) Burden: Its Relevance to Healthy Aging. Aging Dis 2014; 5: 12-217.
[102]
Grillo MA, Colombatto S. Advanced glycation end-products (AGEs): involvement in aging and in neurodegenerative diseases. Amino Acids 2008; 35: 9-36.
[103]
Merhi Z. Advanced glycation end products and their relevance in female reproduction. Hum Reprod 2014; 29: 35-145.
[104]
Tatone C, Eichenlaub-Ritter U, Amicarelli F. Dicarbonyl stress and glyoxalases in ovarian function. Biochem Soc Trans 2014; 42: 33-438.
[105]
Szafarowska M, Jerzak M. Ovarian aging and infertility. Ginekol Pol 2013; 84: 98-304.
[106]
Tatone C, Amicarelli F, Carbone MC, et al. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update 2008; 14: 31-142.
[107]
Tatone C, Carbone MC, Campanella G, et al. Female reproductive dysfunction during ageing: role of methylglyoxal in the formation of advanced glycation endproducts in ovaries of reproductively-aged mice. J Biol Regul Homeost Agents 2010; 24: 3-72.
[108]
Boudoures AL, Saben J, Drury A, et al. Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy. Dev Biol 2017; 426: 26-138.
[109]
Van Blerkom J, Davis P, Mathwig V, Alexander S. Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum Reprod 2002; 17: 93-406.
[110]
Au HK, Yeh TS, Kao SH, Tzeng CR, Hsieh RH. Abnormal mitochondrial structure in human unfertilized oocytes and arrested embryos. Ann N Y Acad Sci 2005; 1042: 77-185.
[111]
Pawlak P, Chabowska A, Malyszka N, Lechniak D. Mitochondria and mitochondrial DNA in porcine oocytes and cumulus cells--A search for developmental competence marker. Mitochondrion 2016; 27: 8-55.
[112]
Wang T, Zhang M, Jiang Z, Seli E. Mitochondrial dysfunction and ovarian aging. Am J Reprod Immunol 2017; 77: 2651.
[113]
Meldrum DR, Casper RF, Diez-Juan A, Simon C, Domar AD, Frydman R. Aging and the environment affect gamete and embryo potential: can we intervene? Fertil Steril 2016; 105: 548-59.
[114]
Simsek-Duran F, Li F, Ford W, Swanson RJ, Jones HW, Jr Castora FJ. Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS One 2013; 8: e64955.
[115]
Fragouli E, Wells D. Mitochondrial DNA Assessment to Determine Oocyte and Embryo Viability. Semin Reprod Med 2015; 33: 01-409.
[116]
Jansen RP, Burton GJ. Mitochondrial dysfunction in reproduction. Mitochondrion 2004; 4: 77-600.
[117]
Shoubridge EA, Wai T. (2007) Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol 2007; 77: 7-111.
[118]
Ortega MS, Wohlgemuth S, Tribulo P, et al. A single nucleotide polymorphism in COQ9 affects mitochondrial and ovarian function and fertility in Holstein cows. Biol Reprod 2017; 96: 52-663.
[119]
Pacella-Ince L, Zander-Fox DL, Lane M. Mitochondrial SIRT5 is present in follicular cells and is altered by reduced ovarian reserve and advanced maternal age. Reprod Fertil Dev 2014. 26: 072-1083
[120]
Zhen X, Wu B, Wang J, Lu C, Gao H, Qiao J. Increased Incidence of Mitochondrial Cytochrome C Oxidase 1 Gene Mutations in Patients with Primary Ovarian Insufficiency. PLoS One 2015; 10: e0132610.
[121]
Duncan AJ, Knight JA, Costello H, Conway GS, Rahman S. POLG mutations and age at menopause. Hum Reprod 2012; 27: 243-2244.
[122]
Tan X, Li Y. Copy number and deletion of 4 977 bp of granular cell mitochondria DNA in patients with diminished ovarian reserve. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2010; 35: 79-884.
[123]
Chao HT, Lee SY, Lee HM, Liao TL, Wei YH, Kao SH. Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann N Y Acad Sci 2005; 1042: 48-156.
[124]
Conca Dioguardi C, Uslu B, Haynes M, et al. Granulosa cell and oocyte mitochondrial abnormalities in a mouse model of fragile X primary ovarian insufficiency. Mol Hum Reprod 2016; 22: 84-396.
[125]
Lu C, Lin L, Tan H, et al. Fragile X premutation RNA is sufficient to cause primary ovarian insufficiency in mice. Hum Mol Genet 2012; 21: 039-5047.
[126]
Hoffman GE, Le WW, Entezam A, et al. Ovarian abnormalities in a mouse model of fragile X primary ovarian insufficiency. J Histochem Cytochem 2012; 60: 39-456.
[127]
Lu B, Poirier C, Gaspar T, et al. A mutation in the inner mitochondrial membrane peptidase 2-like gene (Immp2l) affects mitochondrial function and impairs fertility in mice. Biol Reprod 2008; 78: 01-610.
[128]
Muhammad F, Yivgi-Ohana N, Shveiky D, Orly J, Alexander S, Laufer N. Levels of steroidogenic acute regulatory protein and mitochondrial membrane potential in granulosa cells of older poor-responder women. Fertil Steril 2009; 91: 20-205.
[129]
Laven JS, Visser JA, Uitterlinden AG, Vermeij WP, Hoeijmakers JH. Menopause: Genome stability as new paradigm. Maturitas 2016; 92: 5-23.
[130]
Desai S, Rajkovic A. Genetics of Reproductive Aging from Gonadal Dysgenesis through Menopause. Semin Reprod Med 2017; 35: 47-159.
[131]
Oktay K, Turan V, Titus S, Stobezki R, Liu L. BRCA Mutations, DNA Repair Deficiency, and Ovarian Aging. Biol Reprod 2015; 93: 7.
[132]
Titus S, Li F, Stobezki R, et al. Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci Transl Med 2013; 5: 72ra21.
[133]
Zhou J, Stein P, Leu NA, et al. Accelerated reproductive aging in females lacking a novel centromere protein SYCP2L. Hum Mol Genet 2015; 24: 505-6514.
[134]
Gleicher N, Yu Y, Himaya E, et al. Early decline in functional ovarian reserve in young women with low (CGGn < 26) FMR1 gene alleles. Transl Res 2015; 166: 02-507.
[135]
Wang TT, Ke ZH, Song Y, et al. Identification of a mutation in GDF9 as a novel cause of diminished ovarian reserve in young women. Hum Reprod 2013; 28: 473-2481.
[136]
Lim J, Nakamura BN, Mohar I, Kavanagh TJ, Luderer U. Glutamate Cysteine Ligase Modifier Subunit (Gclm) Null Mice Have Increased Ovarian Oxidative Stress and Accelerated Age-Related Ovarian Failure. Endocrinology 2015; 156: 329-3343.
[137]
Lim J, Ortiz L, Nakamura BN, et al. Effects of deletion of the transcription factor Nrf2 and benzo [a]pyrene treatment on ovarian follicles and ovarian surface epithelial cells in mice. Reprod Toxicol 2015; 58: 4-32.
[138]
Benayoun BA, Georges AB, L’Hôte D, et al. Transcription factor FOXL2 protects granulosa cells from stress and delays cell cycle: role of its regulation by the SIRT1 deacetylase. Hum Mol Genet 2011; 20: 673-1686.
[139]
Hanna CW, Bretherick KL, Gair JL, Fluker MR, Stephenson MD, Robinson WP. Telomere length and reproductive aging. Hum Reprod 2009; 24: 206-1211.
[140]
Dorland M, van Kooij RJ, te Velde ER. General ageing and ovarian ageing. Maturitas 1998; 30: 13-118.
[141]
Aydos SE, Elhan AH, Tukun A. Is telomere length one of the determinants of reproductive life span? Arch Gynecol Obstet 2005; 272: 13-116.
[142]
Keefe DL, Liu L, Marquard K. Telomeres and aging-related meiotic dysfunction in women. Cell Mol Life Sci 2007; 64: 39-143.
[143]
Keefe DL, Marquard K, Liu L. The telomere theory of reproductive senescence in women. Curr Opin Obstet Gynecol 2006; 18: 80-285.
[144]
Xu X, Chen X, Zhang X, et al. Impaired telomere length and telomerase activity in peripheral blood leukocytes and granulosa cells in patients with biochemical primary ovarian insufficiency Hum Reprod 2017; 32: 01- 207
[145]
Yamada-Fukunaga T, Yamada M, Hamatani T, et al. Age-associated telomere shortening in mouse oocytes Reprod Biol Endocrinol 2013; 11: 08
[146]
Bayne S, Li H, Jones ME, et al. Estrogen deficiency reversibly induces telomere shortening in mouse granulosa cells and ovarian aging in vivo. Protein Cell 2011; 2: 33-346.
[147]
Li H, Simpson ER, Liu JP. Oestrogen, telomerase, ovarian ageing and cancer. Clin Exp Pharmacol Physiol 2010; 37: 8-82.
[148]
Kalmbach KH, Antunes DM, Kohlrausch F, Keefe DL. Telomeres and Female Reproductive Aging. Semin Reprod Med 2015; 33: 89-395.
[149]
Keefe DL, Liu L. Telomeres and reproductive aging Reprod Fertil Dev 2009; 21: 0-14
[150]
Pavlov KI, Mukhin VN, Klimenko VM, Anisimov VN. Telomere-telomerase system in aging, norm and pathology (literature review). Adv Gerontol 2017; 30: 7-26.
[151]
Chapman C, Cree L, Shelling AN. The genetics of premature ovarian failure: current perspectives. Int J Womens Health 2015; 7: 99-810.
[152]
Gleicher N, Weghofer A, Oktay K, Barad D. Do etiologies of premature ovarian aging (POA) mimic those of premature ovarian failure (POF)? Hum Reprod 2009; 24: 395-2400.
[153]
Pal L, Santoro N. Premature ovarian failure (POF): discordance between somatic and reproductive aging. Ageing Res Rev 2002; 1: 13-423.
[154]
Yaba A, Demir N. The mechanism of mTOR (mammalian target of rapamycin) in a mouse model of polycystic ovary syndrome (PCOS). J Ovarian Res 2012; 5: 8.
[155]
Paixão L, Ramos RB, Lavarda A, Morsh DM, Spritzer PM. Animal models of hyperandrogenism and ovarian morphology changes as features of polycystic ovary syndrome: a systematic review. Reprod Biol Endocrinol 2017; 15: 2.
[156]
Tremellen K, Zander-Fox D. Serum anti-Mullerian hormone assessment of ovarian reserve and polycystic ovary syndrome status over the reproductive lifespan. Aust N Z J Obstet Gynaecol 2015; 55: 84-389.
[157]
Rashidi BH, Gorginzadeh M, Aalipour S, Sills ES. Age related endocrine patterns observed in polycystic ovary syndrome patients vs. ovulatory controls: descriptive data from a university based infertility center. Arch Endocrinol Metab 2016; 60: 86-491.
[158]
Carmina E, Campagna AM, Mansuet P, Vitale G, Kort D, Lobo R. Serum AMH may help predict ovulatory function with aging in anovulatory women with PCOS Fertil Steril 2012; 98: 043-1046
[159]
Rezvanfar MA, Shojaei Saadi HA, Gooshe M, Abdolghaffari AH, Baeeri M, Abdollahi M. Ovarian aging-like phenotype in the hyperandrogenism-induced murine model of polycystic ovary. Oxid Med Cell Longev 2014; 2014: 48951.
[160]
Hsu MI. Changes in the PCOS phenotype with age. Steroids 2013; 78: 61-766.
[161]
Brown ZA, Louwers YV, Fong SL, et al. The phenotype of polycystic ovary syndrome ameliorates with aging. Fertil Steril 2011; 96: 259-1265.
[162]
Park JH, Choi TS. Polycystic ovary syndrome (PCOS)-like phenotypes in the d-galactose-induced aging mouse model. Biochem Biophys Res Commun 2012; 427: 01-704.
[163]
Tehrani FR, Solaymani-Dodaran M, Hedayati M, Azizi F. Is polycystic ovary syndrome an exception for reproductive aging? Hum Reprod 2010; 25: 775-1781.
[164]
Vulpoi C, Lecomte C, Guilloteau D, Lecomte P. Ageing and reproduction: is polycystic ovary syndrome an exception? Ann Endocrinol (Paris) 2007; 68: 5-50.
[165]
Molinari E, Bar H, Pyle AM, Patrizio P. Transcriptome analysis of human cumulus cells reveals hypoxia as the main determinant of follicular senescence. Mol Hum Reprod 2016; 22: 66-876.
[166]
Hosni W, Bastu E. Ovarian stem cells and aging. Climacteric 2012; 15: 25-132.
[167]
Fernandois D, Cruz G, Na EK, Lara HE, Paredes AH. Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system. J Endocrinol 2017; 232: 7-105.
[168]
Zhang J, Fang L, Shi L, et al. Protective effects and mechanisms investigation of Kuntai capsule on the ovarian function of a novel model with accelerated aging ovaries. J Ethnopharmacol 2017; 195: 73-181.
[169]
Ahangarpour A, Najimi SA, Farbood Y. Effects of Vitex agnus-castus fruit on sex hormones and antioxidant indices in a d-galactose-induced aging female mouse model. J Chin Med Assoc 2016; 79: 89-596.
[170]
Ahangarpour A, Lamoochi Z, Fathi Moghaddam H. ansouri SM. Effects of Portulaca oleracea ethanolic extract on reproductive system of aging female mice. Int J Reprod Biomed 2016; 14: 05-212.
[171]
Özcan P, Fıçıcıoğlu C, Kizilkale O, et al. Can Coenzyme Q10 supplementation protect the ovarian reserve against oxidative damage? J Assist Reprod Genet 2016; 33: 223-1230.
[172]
Ben-Meir A, Burstein E, Borrego-Alvarez A, et al. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell 2015; 14: 87-895.
[173]
Liang L, Zhang XH, Ji B, et al. Yifuning postpones ovarian aging through antioxidant mechanisms and suppression of the Rb/p53 signal transduction pathway. Mol Med Rep 2016; 14: 88-896.
[174]
Li YJ, Han Z, Ge L, et al. C-phycocyanin protects against low fertility by inhibiting reactive oxygen species in aging mice. Oncotarget 2016; 7: 7393-17409.
[175]
Liu J, Liu M, Ye X, et al. Delay in oocyte aging in mice by the antioxidant N-acetyl-L-cysteine (NAC). Hum Reprod 2012; 27: 411-1420.
[176]
Liu M, Yin Y, Ye X, et al. Resveratrol protects against age-associated infertility in mice Hum Reprod 2013; 28: 07-717
[177]
Lee HC, Wei YH. Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging. Exp Biol Med (Maywood) 2007; 232: 92-606.
[178]
Ma YS, Wu SB, Lee WY, Cheng JS, Wei YH. Response to the increase of oxidative stress and mutation of mitochondrial DNA in aging. Biochim Biophys Acta 2009. 1790: 021-1029.
[179]
Wei YH, Wu SB, Ma YS, Lee HC. Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J 2009; 32: 13-132.
[180]
Radman M. Protein damage, radiation sensitivity and aging. DNA Repair (Amst) 2016; 44: 86-192.
[181]
Ellgaard L, Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003; 4: 81-191.
[182]
Lemus L, Goder V. Regulation of endoplasmic reticulum-associated protein degradation (ERAD) by ubiquitin. Cells 2014; 3: 24-847.
[183]
Yorimitsu T, Klionsky DJ. Eating the endoplasmic reticulum: quality control by autophagy. Trends Cell Biol 2007; 17: 79-285.
[184]
Gibellini L, De Biasi S, Nasi M, Iannone A, Cossarizza A, Pinti M. Mitochondrial Proteases as Emerging Pharmacological Targets. Curr Pharm Des 2016; 22: 679-2688.
[185]
Feleciano DR, Kirstein J. Collapse of redox homeostasis during aging and stress. Mol Cell Oncol 2015; 3: e1091060.
[186]
Kirstein J, Morito D, Kakihana T, et al. Proteotoxic stress and ageing triggers the loss of redox homeostasis across cellular compartments. EMBO J 2015; 34: 334-2349.
[187]
Feleciano DR, Arnsburg K, Kirstein J. Interplay between redox and protein homeostasis. Worm 2016; 5: e1170273.
[188]
Labbadia J, Morimoto RI. Proteostasis and longevity: when does aging really begin? F1000Prime Rep 2014; 6.
[189]
Prasad KN, Wu M, Bondy SC. Telomere shortening during aging: Attenuation by antioxidants and anti-inflammatory agents. Mech Ageing Dev 2017; 164: 1-66.
[190]
Arsenis NC, You T, Ogawa EF, Tinsley GM, Zuo L. Physical activity and telomere length: Impact of aging and potential mechanisms of action. Oncotarget 2017; 8: 5008-45019.
[191]
Von Zglinicki T. Role of oxidative stress in telomere length regulation and replicative senescence. Ann N Y Acad Sci 2000; 908: 9-110.
[192]
Zhou J, Mao B, Zhou Q, et al. Endoplasmic reticulum stress activates telomerase. Aging Cell 2014; 13: 97-200.
[193]
Hosoi T, Inoue Y, Nakatsu K, et al. TERT attenuated ER stress-induced cell death. Biochem Biophys Res Commun 2014; 447: 378-82.
[194]
Pluquet O, Pourtier A, Abbadie C. The unfolded protein response and cellular senescence. A review in the theme: cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. Am J Physiol Cell Physiol 2015; 308: C415-25.
[195]
Crooke A, Huete-Toral F, Colligris B, Pintor J. The role and therapeutic potential of melatonin in age-related ocular diseases. J Pineal Res 2017; 63: 2430.
[196]
Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Mitochondrial bioenergetics decay in aging: beneficial effect of melatonin. Cell Mol Life Sci 2017; 74: 897-3911.
[197]
Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Protective role of melatonin in mitochondrial dysfunction and related disorders. Arch Toxicol 2015; 89: 23-939.
[198]
Reiter RJ, Rosales-Corral S, Tan DX, Jou MJ, Galano A, Xu B. Melatonin as a mitochondria-targeted antioxidant: one of evolution’s best ideas. Cell Mol Life Sci 2017; 4: 863-3881.
[199]
Wongprayoon P, Govitrapong P. Melatonin as a mitochondrial protector in neurodegenerative diseases. Cell Mol Life Sci 2017; 4: 999-4014.
[200]
Mendivil-Perez M, Soto-Mercado V, Guerra-Librero A, et al. Melatonin enhances neural stem cell differentiation and engraftment by increasing mitochondrial function. J Pineal Res 2017; 63: 2415.
[201]
Wątroba M, Dudek I, Skoda M, Stangret A, Rzodkiewicz P, Szukiewicz D. Sirtuins, epigenetics and longevity. Ageing Res Rev 2017; 40: 1-19.
[202]
Satoh A, Stein L, Imai S. The role of mammalian sirtuins in the regulation of metabolism, aging, and longevity. Handb Exp Pharmacol 2011; 206: 25-162.
[203]
Mayo JC, Sainz RM, González Menéndez P, Cepas V, Tan DX, Reiter RJ. Melatonin and sirtuins: A “not-so unexpected” relationship. J Pineal Res 2017; 62: 2391.
[204]
Hardeland R. Melatonin and the pathologies of weakened or dysregulated circadian oscillators. J Pineal Res 2017; 2: 2377.
[205]
Rastmanesh R. Potential of melatonin to treat or prevent age-related macular degeneration through stimulation of telomerase activity. Med Hypotheses 2011; 76: 9-85.
[206]
Akbulut KG, Gonul B, Akbulut H. The role of melatonin on gastric mucosal cell proliferation and telomerase activity in ageing J Pineal Res 2009; 47: 08-312
[207]
Chan KA, Bernal AB, Vickers MH, Gohir W, Petrik JJ, Sloboda DM. Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol Reprod 2015; 92: 10.
[208]
Choi HS, Kang JW, Lee SM. Melatonin attenuates carbon tetrachloride-induced liver fibrosis via inhibition of necroptosis. Transl Res 2015; 66: 92-303.
[209]
Ali T, Badshah H, Kim TH, Kim MO. Melatonin attenuates D-galactose-induced memory impairment, neuroinflammation and neurodegeneration via RAGE/NF-K B/JNK signaling pathway in aging mouse model. J Pineal Res 2015; 8: 1-85.
[210]
Tamura H, Nakamura Y, Korkmaz A, et al. Melatonin and the ovary: physiological and pathophysiological implications. Fertil Steril 2009; 2: 28-343.
[211]
Majidinia M, Reiter RJ, Shakouri SK, et al. The multiple functions of melatonin in regenerative medicine. Ageing Res Rev 2018; 5: 3-52.
[212]
Rodella LF, Favero G, Rossini C, et al. Aging and vascular dysfunction: beneficial melatonin effects. Age (Dordr) 2013; 5: 03-115
[213]
Jenwitheesuk A, Nopparat C, Mukda S, Wongchitrat P, Govitrapong P. Melatonin regulates aging and neurodegeneration through energy metabolism, epigenetics, autophagy and circadian rhythm pathways. Int J Mol Sci 2014; 5: 6848-16884.
[214]
Lee FY, Sun CK, Sung PH, et al. Daily melatonin protects the endothelial lineage and functional integrity against the aging process, oxidative stress, and toxic environment and restores blood flow in critical limb ischemia area in mice. J Pineal Res 2018; e12489.
[215]
Idowu AJ, Kumar SL, Yidong B, Russel R. Melatonin modulates neuronal mitochondria function during normal ageing in mice. Niger J Physiol Sci 2017; 2: 45-152.
[216]
Jenwitheesuk A, Park S, Wongchitrat P, et al. Comparing the Effects of Melatonin with Caloric Restriction in the Hippocampus of Aging Mice: Involvement of Sirtuin1 and the FOXOs Pathway. Neurochem Res 2018; 3: 44-152.
[217]
Crooke A, Huete-Toral F, Colligris B, Pintor J. The role and therapeutic potential of melatonin in age-related ocular diseases. J Pineal Res 2017; 3: 2430.
[218]
Wang T, Gao YY, Chen L, et al. Melatonin prevents postovulatory oocyte aging and promotes subsequent embryonic development in the pig. Aging (Albany NY) 2017; •••: 552-1564.
[219]
Guo XH, Li YH, Zhao YS, Zhai YZ, Zhang LC. Anti-aging effects of melatonin on the myocardial mitochondria of rats and associated mechanisms Mol Med Rep 2017; 5: 03-410
[220]
Tamura H, Kawamoto M, Sato S, et al. Long-term melatonin treatment delays ovarian aging. J Pineal Res 2017; 2: 2381.
[221]
Chan KA, Bernal AB, Vickers MH, Gohir W, Petrik JJ, Sloboda DM. Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol Reprod 2015; 2: 10.
[222]
Kleszczynski K, Fischer TW. Melatonin and human skin aging. Dermatoendocrinol 2012; 4: 245-52.
[223]
Tamura H, Takasaki A, Taketani T, et al. Melatonin and female reproduction J Obstet Gynaecol Res 2014; 40: -11
[224]
Dragojevic Dikic S, Jovanovic AM, Dikic S, Jovanovic T, Jurisic A, Dobrosavljevic A. Melatonin: a “Higgs boson” in human reproduction. Gynecol Endocrinol 2015; 31: 2-101.
[225]
Gursoy AY, Kiseli M, Caglar GS. Melatonin in aging women. Climacteric 2015; 18: 790-6.
[226]
Song C, Peng W, Yin S, et al. Melatonin improves age-induced fertility decline and attenuates ovarian mitochondrial oxidative stress in mice. Sci Rep 2016; 6: 5165.
[227]
Fernández BE, Díaz E, Fernández C, Núñez P, Díaz B. Ovarian aging: melatonin regulation of the cytometric and endocrine evolutive pattern Curr Aging Sci 2013; 6: -7
[228]
Meredith S, Jackson K, Dudenhoeffer G, Graham L, Epple J. Long-term supplementation with melatonin delays reproductive senescence in rats, without an effect on number of primordial follicles. Exp Gerontol 2000; 35: 43-352.
[229]
Tamura H, Nakamura Y, Korkmaz A, et al. Melatonin and the ovary: physiological and pathophysiological implications. Fertil Steril 2009; 92: 328-43.
[230]
Takasaki A, Nakamura Y, Tamura H, Shimamura K, Morioka H. Melatonin as a new drug for improving oocyte quality. Reprod Med Biol 2004; 39-144.
[231]
Wu X, Cao N, Fenech M, Wang X. Role of Sirtuins in Maintenance of Genomic Stability: Relevance to Cancer and Healthy Aging. DNA Cell Biol 2016; 35: 42-575.
[232]
Coto-Montes A, Boga JA, Rosales-Corral S, Fuentes-Broto L, Tan DX, Reiter RJ. Role of melatonin in the regulation of autophagy and mitophagy: a review. Mol Cell Endocrinol 2012; 361: 2-23.
[233]
Ali T, Badshah H, Kim TH, Kim MO. Melatonin attenuates D-galactose-induced memory impairment, neuroinflammation and neurodegeneration via RAGE/NF-K B/JNK signaling pathway in aging mouse model. J Pineal Res 2015; 58: 1-85.
[234]
Paradies G, Paradies V, Ruggiero FM, Petrosillo G. Protective role of melatonin in mitochondrial dysfunction and related disorders. Arch Toxicol 2015; 89: 23-939.
[235]
Fernández A, Ordóñez R, Reiter RJ, González-Gallego J, Mauriz JL. Melatonin and endoplasmic reticulum stress: relation to autophagy and apoptosis. J Pineal Res 2015; 59: 92-307.


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VOLUME: 20
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Year: 2019
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DOI: 10.2174/1389450119666180828144843
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