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Cyclic nucleotide in oocyte In vitro maturation in Assisted Reproductive Technology

Monash University, Australia

Received: 7 Dec 2020; Revised: 18 Dec 2020; Accepted: 23 Dec 2020; Available online: 31 Dec 2020; Published: 31 Dec 2020.
Open Access Copyright (c) 2020 Journal of Biomedicine and Translational Research

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In vitro maturation (IVM) is a promising assisted reproductive technology (ART) for human infertility treatment. However, when cumulus oocyte complexes (COCs) are removed from their follicular environment when manipulated in vitro, it can lead to a decrease of intra-oocyte cyclic adenosine 3’, 5’-monophosphare (cAMP) causing spontaneous nuclear maturation and an asynchrony with the oocytes’ cytoplasmic maturation, resulting in poor embryo developmental outcomes. Nuclear and cytoplasmic synchrony is important during oocyte maturation within antral follicles.

It is maintained partially by the actions of c-type natriuretic peptide (CNP) binding with natriuretic peptide receptor 2 (NPR2), supporting high cAMP levels thus holding the oocyte in meiotic arrest. Addition of CNP to pre-IVM media has the capacity of maintaining cAMP levels and thus improve synchrony. Moreover, in women with advanced maternal age, successful IVM of aging oocytes faces significant challenges due to the morphological and cellular changes.  Inhibiting initiation of nuclear maturation by cAMP modulator, CNP during pre-IVM period and thus improve oocyte developmental competence regardless of oocyte age.

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Keywords: Oocyte; maturation; infertility; cyclic nucleotide

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  1. Romero S, Sanchez F, Lolicato F, Ranst HV and Smitz J. Immature oocytes from unprimed mice become a valuable source from embryo production when using C-type natriuretic peptide as essential component of culture medium. Biology of Reproduction 2016; 95: 1-10
  2. Wei Q, Zhou C, Yuan M, Miao Y, Zhao X and Ma B. Effect of C-type natriuretic peptide on maturation and developmental competence of immature mouse oocytes in vitro. Reproduction, Fertility and Development 2016; 29:319-324
  3. Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, De Vos M, Smitz J, Thompson JG and Gilchrist RB. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Human Reproduction 2013; 28: 1536-1545
  4. Edwards RG. Meiosis in ovarian oocytes of adult mammals. Nature 1962; 196:446
  5. Chian RC, Uzelac PS and Nargund G. In vitro maturation of human immature oocytes for fertility preservation. Fertility Sterility 2013; 99: 1173-1181
  6. Ellenbogen A, Shavit T and Shalom-Paz E. IVM results are comparable and may have advantages over standard IVF Facts. Views & Visions in Obstetrics, Gynaecology and Reproductive Health 2014; 6: 77-80
  7. Xu J, Bernuci MP, Lawson MS, Yeoman RR, Fisher TE, Zelinski MB and Stouffer RL. Survival, growth, and maturation of secondary follicles from prepubertal, young, and older adult rhesus monkeys during encapsulated three-dimensional culture: effects of gonadotropins and insulin. Reproduction 2010; 140:685-697
  8. Child TJ, Philips SJ, Abdul-Jalil AK, Gulekli B and Tan SL. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovarie.s Obstetrics & Gynaecology 2002; 100: 665-670
  9. Pincus G and Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro: 1. the activation of ovarian eggs. The Journal of Experimental Medicine 1935; 62: 665-675
  10. Edwards RG. Maturation in vitro of human ovarian oocytes. The Lancet 1965; 2: 926-929
  11. Zhang M, Su YQ, Sugiura K, Xia G and Epping JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010; 330: 366-369
  12. Lord T, Nixon B, Jones KT and Aitken J. Melatonin prevents post-ovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro. Reproduction 2013; 88: 67-76
  13. Koyama K, Kang SS, Huang W, Yanagawa Y, Takahashi Y and Nagano M. Aging-related changes In Vitro-matured bovine oocytes: oxidative stress, mitochondrial activity and ATP content after nuclear maturation. Journal of Reproduction and Development 2014; 60:136-142
  14. Walls ML, Hunter T, Ryan JP, Keelan JA, Nathan E and Hart RJ In vitro maturation as an alternative to standard in vitro fertilisaiton for patients diagnosed with polycystic ovaries: a comparative analysis of fresh, frozen and cumulative cycle outcomes. Human Reproduction 2015; 30:88-96
  15. Maman E, Meirow D, Brengauz M, Raanani H, Dor J and Hourvitz. A Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation. Fertility and Sterility 2011; 95: 64-67
  16. Liu K and Case A. Advanced Reproductive Age and Fertility. Journal of Obstetrics and Gynaecology 2011; 33:1165-1175
  17. Hourvitz A, Maman E, Brengauz M, Machtinger R and Dor J. In vitro maturation for patients with repeated in vitro fertilization failure due to ‘oocyte maturation abnormalities. Fertility and Sterility 2010; 92: 496-501
  18. Cha KY, Koo JJ, Ko JJ, Choi DH, Han SY and Yoon TK. Pregnancy after in vitro fertilization of human follicular oocytes collected from non-stimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertility and Sterility 1991; 55:109-13
  19. Franks S, McCarthy MI and Hardy K Development of polycystic ovary syndrome: involvement of genetic and environmental factors International. Journal of Andrology 2006; 29: 278-285
  20. Goodarzi MO, Dumesic DA, Chazenbalk G and Azziz R. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis Nature Reviews Endocronology 2011; 7: 219-231
  21. Siristatidis CS, Vrachnis N, Creatsa M, Maheshwari A and Bhattacharya S. In vitro maturation in subfertile women with polycystic ovarian syndrome undergoing assisted reproduction (review). Cochrane Database of Systematic Reviews 2013; 10: 1-24
  22. Trounson A, Wood C and Kausche A. In vitro maturation and the fertilization and developmental competence of oocytes recovered from untreated polycystic ovarian patients Fertility and Sterility 1994; 62: 353-362
  23. Hassold T, Jacobs PA, Leppert M and Sheldon M Cytogenetic and molecular studies of trisomy. Journal of Medical Genetics 1987; 24: 725-732
  24. Staessen C, Platteau P, Assche EV, Michiels A, Tournaye H, Camus M, Devroey P, Liebaers I and Steirteghem AV. Comparison of blastocyst transfer with or without preimplantation genetic diagnosis for aneuploidy screening in couples with advanced maternal age: a prospective randomized controlled trial. Human Reproduction 2004; 19: 2849-2858
  25. Munne S, Alikani M, Tomkin G, Grifo J and Cohen J. Embryo morphology, developmental rates and maternal age are correlated with chromosome abnormalities Fertility and Sterility 1995; 64: 382-391
  26. Dailey T, Dale B, Cohen J and Munne S. Association between non-disjunction and maternal age in meiosis-II human oocytes detected by FISH analysis. The American Journal of Human Genetics 1996; 59:176-184
  27. Marquez C, Sanalinas M, Bahce M, Alikani M and Munne S. Chromosome abnormalities in 1255 cleavage-stage human embryos Reproductive BioMedicine Online 2000; 1: 17-26
  28. Katz-Jaffe MG, Trounson AO & Cram DS. Chromosome 21 mosaic human preimplantation embryos predominantly arise from diploid conceptions Fertility and Sterility 2005; 84: 634-643
  29. Baart EB, Martini E, Eijkemans MJ, Van Opstal D, Beckers NG, Verhoeff. Milder ovarian stimulation for in-vitro fertilization reduces aneuploidy in the human preimplantation embryo: a randomized controlled trial. Human Reproduction 2007; 22: 980–988
  30. Hassold T and Chiu D. Maternal age-specific rates of numerical chromosome abnormalities with special reference to trisomy. Human Genetics 1985; 70:11-17
  31. Hassold T, Hall H and Hunt P The origin of human aneuploidy: where we have been, where we are going. Human Molecular Genetics 2007; 2: R203-R208
  32. Cross PC and Brinster RL. In vitro development of mouse oocytes. Biology of Reproduction 1970; 3: 298-307
  33. Le Du A, Kadoch IJ, Bourcigaux N, Doumerc S, Bourrier MC, Chevalier N, Fanchin R, Chian RC, Tachdjian G, Frydman R and Frydman N (2005) In vitro oocyte maturation for the treatment of infertility associated with polycystic ovarian syndrome: the French experience Human reproduction 20 420-424
  34. Sanchez F, Romero S, Vos MD, Verheyen G and Smitz J. Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Human Reproduction 2015; 30: 1396-1409
  35. Romeu A, Muasher SJ, Acosta AA, Veeck LL, Diaz J, Jones GS, Jones HW Jr and Rosenwaks Z. Results of in vitro fertilization attempts in women 40 years of age and older: the Norfolk experience. Fertility and Sterility 1987; 47: 130-136
  36. Lim AS and Tsakok MF. Age-related decline in fertility: a link to degenerative oocytes? Fertility and Sterility 1997; 68: 265-271
  37. Henderson SA and Edwards RG. Chiasma frequency and maternal age in mammals. Nature 1968; 218: 22-28
  38. Tarin JJ, Brines J and Cano A. Long-term effects of delayed parenthood Human Reproduction 1998; 13:2371-2376
  39. Sher G, Keskintepe L, Keskintepe M, Ginsburg M, Maassarani G, Yakut T, Baltaci V, Kotze D & Unsal E. Oocyte karyotyping by comparative genomic hybridization (correction of hybridization) provides a highly reliable method for selecting “competent” embryos, markedly improving in vitro fertilization outcome: a multiphase study. Fertility and Sterility 2007;87:1033-1040
  40. Vivarelli E, Conti M, De Felici M and Siracusa G. Meiotic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differences 1983;12: 271-276
  41. Törnell J, Billig H and Hillensjo T. Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 3',5'-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta Physiologica Scandinavica 1990; 139: 511-517
  42. Li HJ, McDowall ML, Wang X, Sugimura S, Thompson JG and Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Human Reproduction 2016; 31: 810-821
  43. Tsuji T, Kiyosu C, Akiyama K and Kunieda T. CNP/NPR2 signaling maintains oocyte meiotic arrest in early antral follicles and is suppressed by EGFR-mediated signaling in preovulatory follicles. Molecular Reproduction and Development 2012; 79: 795-802
  44. Zeng HT, Richani D, Sutton-McDowall ML, Ren Z, Smitz J, Stokes Y, Gilchrist RB and Thompson JG. Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocyte. Biology of Reproduction 2014; 91: 1-11
  45. Bernal-Ulloa SM, Heinzmann J, Herrmann D, Hadeler KG, Aldag P, Winkler S, Pache D, Baulain U, Lucas-Hahn A and Niemann H. Cyclic AMP affects oocyte maturation and embryo development in prepubertal and adult cattle. Plos ONE 2016; 11: e0150264
  46. Zhang J, Wei Q, Cai J, Zhao X and Ma B. Effect of C-type natriuretic peptide on maturation and developmental competence of goat oocytes matured in vitro. PLoS ONE 2015; 10: e0132318
  47. Appeltant R, Beek J, Vandenberghe L, Maes D and Soom AV. Increasing the cAMP concentration during in vitro maturation of pig oocytes improves cumulus maturation and subsequent fertilization in vitro. Theriogenology 2015; 83: 344-352
  48. Kim, E, Geon A. Kim,G, Taweechaipaisankul, A, Ridlo, MR, Lee, SH, Kihae Ra,K, Ahn, C and, Chun, B., Phytanic acid-derived peroxisomal lipid metabolism in porcine oocytes. Theriogenology 2020; 157: 276-285
  49. Wynn P, Picton HM, Krapez JA, Rutherford AJ, Balen AH and Gosden RG. Pretreatment with follicle stimulating hormone promotes the numbers of human oocytes reaching metaphase II by in-vitro maturation. Human Reproduction 1998; 13: 3132-3138
  50. Mikkelsen AL, Smith SD, Lindenberg S. In-vitro maturation of human oocytes from regularly menstruating women may be successful without follicle stimulating hormone priming. Human Reproduction 1999; 14: 1847-1851
  51. Creux H, Monnier P, Son W, Tulandi T and Buckett W. Immature oocyte retrieval and in vitro oocyte maturation at different phases of the menstrual cycle in women with cancer who require urgent gonadotoxic treatment. Fertility Sterility 2017; 107: 198-204
  52. Zhao JZ, Zhou W, Zhang W, Ge HS, Huang XF and Lin JJ. In vitro maturation and fertilization of oocytes from unstimulated ovaries in infertile women with polycystic ovary syndrome. Fertility and Sterility 2009; 91: 2568-2571
  53. Ge HS, Huang XF, Zhang W, Zhao JZ, Lin JJ and Zhou W. Exposure to human chorionic gonadotrophin during in vitro maturation does not improve the maturation rate and developmental potential of immature oocytes from patients with polycystic ovary syndrome Fertility and Sterility 2008; 89: 98-103
  54. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122: 829-838
  55. Fortune JE and Eppig JJ. Effects of gonadotropins on steroid secretion by infantile and juvenile mouse ovaries in vitro. Endocrinology 1979; 10:5 760-768
  56. Cortvrindt R, Smitz J and VanSteirteghem A. Assessment of the need for follicle stimulating hormone in early preantral mouse follicle culture in vitro. Human Reproduction 1997; 12: 759-768
  57. Brower PT and Schultz RM. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Developmental Biology 1982; 90: 144-153
  58. Schultz RM, Montgomery RR and Belanoff JR. Regulation of mouse oocyte eiotic maturation: implication of a decrease in oocyte cAMP and protein dephophoryltion in commitment to resume meiosis. Developmental Biology 1983; 97: 264-273
  59. Salustri A, Ulisse S, Yanagishita M, and Hascall VC. Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-b. The Journal of Biological Chemistry 1990; 265: 19517-19523
  60. Gilchrist RB, Lane M and Thompson JG. Oocyte secreted factors: regulators of cumulus cell function and oocyte quality. Human Reproduction 2008; 14: 159-177
  61. Hashimoto N and Kishimoto T. Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Developmental Biology 1988; 126: 242-252
  62. Fulka JJ, First NL and Moor RM. Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Molecular Human Reproduction 1998; 4: 41-49
  63. Thibault C, Szollosi D and Gerard M. Mammalian oocyte maturation. Reproduction Nutrition Development 1987; 27: 865-896
  64. Eppig JJ, Schultz RM, O’Brien M and Chesnel F. Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Developmental Biology 1994; 164: 1-9
  65. Motlik J and Fulka J. Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. Journal of Experimental Zoology 1976; 198: 155-162
  66. Rodman TC and Bachvarova R. RNA synthesis in preovulatory mouse oocytes. Journal of Cell Biology 1976; 70: 251
  67. Erickson BH. Development and senescence of the postnatal bovine ovary. Journal of Animal Science 1966; 25: 800-805
  68. Kruip TAM, Cran DG, Van Beneden TH, Dieleman SJ. Structural changes in bovine oocytes during final maturation in vivo. Gamete Research 1983; 8 :29-47
  69. Hyttel P, Callensen H, Greve T. Ultrastructure features of pre-ovulatory oocyte maturation in superovulated cattle. Journal of Reproduction and Fertility 1986; 76: 645-656
  70. Sirard MA and First NL. In vitro inhibition of oocyte nuclear maturation in the bovine. Biology of Reproduction 1988: 39; 229-234
  71. Combelles CM, Cekleniak NA, Racowsky C and Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Human Reproduction 2002; 17: 1006-1016
  72. Wang JZ, Sui HS, Miao DQ, Liu N, Zhou P, Ge L and Tan JH. Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 2009; 137: 181-189
  73. Brevini-Gandolfi T and Gandolfi F. The maternal legacy to the embryo: Cytoplasmic components and their effects on early development . Theriogenology 2001; 55: 1255-1276
  74. Sirard MA, Richard F, Blondin P and Robert C. Contribution of the oocyte to embryo quality. Theriogenology 2006; 65: 126-136
  75. Fujiwara T, Nakada K, Shirakawa H and Miyazaki S. Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Developmental Biology 1993; 156: 69-79
  76. Liu J, Lu Q, Qian Y, Mao Y and Ding W. Pregnancies and births achieved from in vitro matured oocytes retrieved from poor responders undergoing stimulating in vitro fertilization cycles. Fertility and Sterility 2003; 80: 447-449
  77. Bai ZD, Liu K and Wang XY. Developmental potential of aged oocyte rescued by nuclear transfer following parthenogenetic activation and in vitro fertilization. Molecular Reproduction and Development 2006; 73: 1448-1453
  78. Eppig JJ. Regulation of mammalian oocyte maturation. In The Ovary 1993pp 185-208 Eds EY Adashi and PCK Leung. Raven Press, New York
  79. Kanatsu-Shinohara M, Schultz RM and Kopf GS. Acquisition of meiotic competence in mouse oocytes: absolute amounts of p34cdc2, cyclin B1, cdc25C, and wee1 in meiotically incompetent and competent oocytes. Biology of Reproduction 2000; 63: 1610-1616
  80. Tsafriri A and Dekel N. Molecular mechanisms in ovulation. In Molecular Biology Female Reproductive System 1994; pp 207-258 Eds JK Findlay. Academic Press, San Diego
  81. Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA,Wang H, KE H, Nikolaev VO and Jaffe LA. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009; 136: 1869-1878
  82. Peng XR, Hsueh AJ, LaPolt PS, Bjersing L and Ny T. Localization of luteinizing hormone receptor messenger ribonucleic acid ex- pression in ovarian cell types during follicle development and ovulation. Endocrinology 1991; 129: 3200-3207
  83. Eppig JJ, Wigglesworth K, Pendola F and Hirao Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biology of Reproduction 1997; 56: 976-984
  84. Lonergan P, Monaghan P, Rizos D, Boland MP and Gordon I. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Molecular Reproduction and Development 1994; 37: 48-53
  85. Xiao S, Duncan FE, Bai L, Nguyen CT, Shea LD and Woodruff TK. Size-specific follicle selection improves mouse oocyte reproductive outcomes. Reproduction 2015; 150: 183-192
  86. Gautier J, Norbury C, Lohka M, Nurse P and Maller J. Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control gene cdc2+. Cell 1988; 54: 433-439
  87. Labbé JC, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Lelias JM, Picard A and Dorée M. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. The EMBO Journal 1989; 8: 3053-3058
  88. Hirao Y, Tsuji Y, Miyano T, Okano A, Miyake M, Kato S and Moor RM. Association between p34cdc1 levels and meiotic arrest in pig oocytes during early growth. Zygote 1995; 3: 325-332
  89. Christmann L, Jung T and Moor RM. MPF components and meiotic competence in growth pig oocytes.. Molecular Reproduction and Development 1994; 38: 85-90
  90. Heikinheimo O and Gibbons WE. The molecular mechanisms of oocyte maturation and early embryonic development are unveiling new insights into reproductive medicine. Molecular Human Reproduction 1998;4: 745-756
  91. Vanderhyden BC and Tonary AM (1995) Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by a factor(s) secreted by the oocyte Biology of Reproduction 53 1243-1250
  92. Chen ZQ, Ming TX and Nielsen HI. Maturation arrest of human oocytes at germinal vesicle stage. Journal of Human Reproductive Sciences 2010; 3: 153-157
  93. Tsutsumi M, Fujiwara R, Nishizawa H, Ito M, Kogo H, Inagaki H, Ohye T, Kato T, Fujii T and Kurahashi H. Age-related decrease of meiotic cohesins in human oocytes. PLoS ONE 2014; 9: e96710
  94. Horner K, Livera G, Hinckley M, Trinh K, Storm D and Conti M. Rodent oocytes express in active adenylyl cyclase required for meiotic arrest. Developmental Biology 2003; 258: 385-396
  95. Hinckley M, Vaccari S, Horner K, Chen R and Conti M. The G-protein- coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Developmental Biology 2005; 287: 249-261
  96. Racowsky C. Effect of forskolin on maintenance of meiotic arrest and stimulation of cumulus expansion, progesterone and cyclic AMP production by pig oocyte-cumulus complexes. Journal of Reproduction and Fertility 1985; 74: 9-21
  97. Vaccari S, Horner K, Mehlmann LM and Conti M. Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Developmental Biology 2008; 316: 124-134
  98. Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS and Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biology of Reproduction 2009; 81: 595-604
  99. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul PD and Jaffe LA. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 2008; 135: 3229-3238
  100. Conti M and Franciosi F. Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Human Reproduction Update 2018; 24: 245-266
  101. Takahashi T, Igarashi H, Kawagoe J, Amita M, Hara S and Kurachi H. Poor embryo development in mouse oocytes aged in vitro is associated with impaired calcium homeostasis. Biology of Reproduction 2009; 80: 493-502
  102. Loane M, Morris JK, Addor M, Arriola L, Budd J, Doray B, Garne E, Gatt M, Haeusler M, Khoshnood B, Melve K, Latos-Bielenska A, McDonnell B, Mullaney C, O’Mahony M, Wahrendorf AQ, Rankin J, Rissmann A, Rounding C, Salvador J, Tucker D, Wellesley D, Yevtushok L and Dolk H. Twenty-year trends in the prevalence of down syndrome and other trisomies in Europe: impact of maternal age and preantal screening. European Journal of Human Genetics 2013; 21: 27-33
  103. Yoon PW, Freeman SB, Sherman SL, Taft LF, Gu F, Pettay D, Flanders WD, Khoury M and Hassold TJ, Advanced maternal age and the risk of Down syndrome characterized by the meiotic stage of chromosomal error: a population-based study The American Journal of Human Genetics 1996; 58:628-633
  104. Tiwari BS, Belenghi B and Levine A. Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death1 American Society of Plant Biologists 2002;128;1271-1281
  105. Tripathi A, Khatun S, Pandey AN, Mishra SK, Chaube R, Shrivastav TG and Chaube SK. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radical Research 2009; 43: 287-294
  106. Agung B, Otoi T, Wongsrikeao P, Yaniguchi M, Shimizu R, Watari H and Nagai. T. Effect of maturation culture period of oocytes on the sex ratio of in vitro fertilized bovine embryos. Journal of Reproduction and Development 2006; 52: 123-127
  107. Kikuchi K, Naito K, Noguchi J, Shimada A, Kaneko H, Yamashita M, Aoki F, Tojo H and Yoyoda Y. Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biology of Reproduction 2000; 63: 715-722
  108. Webb M, Howlett SK, Maro B. Parthenogenesis and cytoskeletal organization in ageing mouse eggs. Journal of Embryology and Experimental Morphology 1986; 9:5 131-145
  109. Orisaka M, Orisaka S, Jiang JY, Craig J, Wang Y, Kotsuji F and Tsang BK. Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. Molecular Endocrinology 2006; 20: 2456-2468
  110. Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im GS, Prather RS, Isom SC, Rucker E and Tsang BK. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biology of Reproduction 2004; 71: 282-290

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