Advertisement

Science China Life Sciences

, Volume 55, Issue 8, pp 659–669 | Cite as

Current understanding of ovarian aging

  • Qian Li
  • XiaoDan Geng
  • Wei Zheng
  • Jie Tang
  • Bo Xu
  • QingHua ShiEmail author
Open Access
Review Special Topic

Abstract

The reproductive system of human female exhibits a much faster rate of aging than other body systems. Ovarian aging is thought to be dominated by a gradual decreasing numbers of follicles, coinciding with diminished quality of oocytes. Menopause is the final step in the process of ovarian aging. This review focuses on the mechanisms underlying the ovarian aging involving a poor complement of follicles at birth and a high rate of attrition each month, as well as the alternated endocrine factors. We also discuss the possible causative factors that contribute to ovarian aging, e.g., genetic factors, accumulation of irreparable damage of microenvironment, pathological effect and other factors. The appropriate and reliable methods to assess ovarian aging, such as quantification of follicles, endocrine measurement and genetic testing have also been discussed. Increased knowledge of the ovarian aging mechanisms may improve the prevention of premature ovarian failure.

Keywords

ovarian aging menopause genetic factors microenvironment pathology assessment 

References

  1. 1.
    Templeton A, Morris J K, Parslow W. Factors that affect outcome of in vitro fertilisation treatment. Lancet, 1996, 348: 1402–1406PubMedGoogle Scholar
  2. 2.
    Baird D T, Collins J, Egozcue J, et al. Fertility and ageing. Hum Reprod Update, 2005, 11: 261–276PubMedGoogle Scholar
  3. 3.
    Broekmans F J, Knauff E A, te Velde E R, et al. Female reproductive ageing: Current knowledge and future trends. Trends Endocrinol Metab, 2007, 18: 58–65PubMedGoogle Scholar
  4. 4.
    Djahanbakhch O, Ezzati M, Zosmer A. Reproductive ageing in women. J Pathol, 2007, 211: 219–231PubMedGoogle Scholar
  5. 5.
    Hansen K R, Knowlton N S, Thyer A C, et al. A new model of reproductive aging: The decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod, 2008, 23: 699–708PubMedGoogle Scholar
  6. 6.
    McGee E A, Hsueh A J. Initial and cyclic recruitment of ovarian follicles. Endocr Rev, 2000, 21: 200–214PubMedGoogle Scholar
  7. 7.
    Hirshfield A N. Development of follicles in the mammalian ovary. Int Rev Cytol, 1991, 124: 43–101PubMedGoogle Scholar
  8. 8.
    Markstrom E, Svensson E, Shao R, et al. Survival factors regulating ovarian apoptosis — dependence on follicle differentiation. Reproduction, 2002, 123: 23–30PubMedGoogle Scholar
  9. 9.
    te Velde E R, Pearson P L. The variability of female reproductive ageing. Hum Reprod Update, 2002, 8: 141–154Google Scholar
  10. 10.
    Block E. A quantitative morphological investigation of the follicular system in newborn female infants. Acta anatomica, 1953, 17: 201–206PubMedGoogle Scholar
  11. 11.
    Alviggi C, Humaidan P, Howles C M, et al. Biological versus chronological ovarian age: Implications for assisted reproductive technology. Reprod Biol Endocrinol, 2009, 7: 101PubMedPubMedCentralGoogle Scholar
  12. 12.
    te Velde E R, Scheffer G J, Dorland M, et al. Developmental and endocrine aspects of normal ovarian aging. Mol Cell Endocrinol, 1998, 145: 67–73Google Scholar
  13. 13.
    Faddy M J, Gosden R G, Gougeon A, et al. Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause. Hum Reprod, 1992, 7: 1342–1346PubMedGoogle Scholar
  14. 14.
    Klein N A, Soules M R. Endocrine changes of the perimenopause. Clin Obstet Gynecol, 1998, 41: 912–920PubMedGoogle Scholar
  15. 15.
    Navot D, Bergh P A, Williams M A, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet, 1991, 337: 1375–1377PubMedGoogle Scholar
  16. 16.
    Faddy M J, Gosden R G. A mathematical model of follicle dynamics in the human ovary. Hum Reprod, 1995, 10: 770–775PubMedGoogle Scholar
  17. 17.
    Faddy M J. Follicle dynamics during ovarian ageing. Mol Cell Endocrinol, 2000, 163: 43–48PubMedGoogle Scholar
  18. 18.
    Nikolaou D, Templeton A. Early ovarian ageing: A hypothesis. Detection and clinical relevance. Hum Reprod, 2003, 18: 1137–1139PubMedGoogle Scholar
  19. 19.
    de Bruin J P, Dorland M, Spek E R, et al. Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol Reprod, 2004, 70: 419–424PubMedGoogle Scholar
  20. 20.
    Treloar A E. Menstrual cyclicity and the pre-menopause. Maturitas, 1981, 3: 249–264PubMedGoogle Scholar
  21. 21.
    Battaglia D E, Goodwin P, Klein N A, et al. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod, 1996, 11: 2217–2222PubMedGoogle Scholar
  22. 22.
    Kuliev A, Cieslak J, Verlinsky Y. Frequency and distribution of chromosome abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 193–198PubMedGoogle Scholar
  23. 23.
    Hunt P A, Hassold T J. Human female meiosis: What makes a good egg go bad? Trends Genet, 2008, 24: 86–93PubMedGoogle Scholar
  24. 24.
    Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 206–212PubMedGoogle Scholar
  25. 25.
    Warburton D. Biological aging and the etiology of aneuploidy. Cytogenet Genome Res, 2005, 111: 266–272PubMedGoogle Scholar
  26. 26.
    Menken J, Trussell J, Larsen U. Age and infertility. Science, 1986, 233: 1389–1394PubMedGoogle Scholar
  27. 27.
    Howles C M, Kim C H, Elder K. Treatment strategies in assisted reproduction for women of advanced maternal age. Int Surgery, 2006, 91: S37–54Google Scholar
  28. 28.
    Gougeon A, Ecochard R, Thalabard J C. Age-related changes of the population of human ovarian follicles: Increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol Reprod, 1994, 50: 653–663PubMedGoogle Scholar
  29. 29.
    van Zonneveld P, Scheffer G J, Broekmans F J M, et al. Do cycle disturbances explain the age-related decline of female fertility? Cycle characteristics of women aged over 40 years compared with a reference population of young women. Hum Reprod, 2003, 18: 495–501PubMedGoogle Scholar
  30. 30.
    Santoro N, Isaac B, Neal-Perry G, et al. Impaired folliculogenesis and ovulation in older reproductive aged women. J Clin Endocrinol Metab, 2003, 88: 5502–5509PubMedGoogle Scholar
  31. 31.
    Treloar A E, Boynton R E, Behn B G, et al. Variation of the human menstrual cycle through reproductive life. Int J Fertil, 1967, 12: 77–126PubMedGoogle Scholar
  32. 32.
    Yamoto M, Minami S, Nakano R, et al. Immunohistochemical localization of inhibin/activin subunits in human ovarian follicles during the menstrual cycle. J Clin Endocrinol Metab, 1992, 74: 989–993PubMedGoogle Scholar
  33. 33.
    Schwall R H, Mason A J, Wilcox J N, et al. Localization of inhibin/activin subunit mrnas within the primate ovary. Mol Endocrinol, 1990, 4: 75–79PubMedGoogle Scholar
  34. 34.
    Roberts V J, Barth S, el-Roeiy A, et al. Expression of inhibin/activin subunits and follistatin messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J Clin Endocrinol Metab, 1993, 77: 1402–1410PubMedGoogle Scholar
  35. 35.
    Klein N A, Illingworth P J, Groome N P, et al. Decreased inhibin B secretion is associated with the monotropic FSH rise in older, ovulatory women: A study of serum and follicular fluid levels of dimeric inhibin a and b in spontaneous menstrual cycles. J Clin Endocr Metab, 1996, 81: 2742–2745PubMedGoogle Scholar
  36. 36.
    Klein N A, Houmard B S, Hansen K R, et al. Age-related analysis of inhibin a, inhibin B, and activin a relative to the intercycle monotropic follicle-stimulating hormone rise in normal ovulatory women. J Clin Endocrinol Metab, 2004, 89: 2977–2981PubMedGoogle Scholar
  37. 37.
    Danforth D R, Arbogast L K, Mroueh J, et al. Dimeric inhibin: A direct marker of ovarian aging. Fertil Steril, 1998, 70: 119–123PubMedGoogle Scholar
  38. 38.
    Hurwitz J M, Santoro N. Inhibins, activins, and follistatin in the aging female and male. Semin Reprod Med, 2004, 22: 209–217PubMedGoogle Scholar
  39. 39.
    Santoro N, Adel T, Skurnick J H. Decreased inhibin tone and increased activin a secretion characterize reproductive aging in women. Fertil Steril, 1999, 71: 658–662PubMedGoogle Scholar
  40. 40.
    Reame N E, Wyman T L, Phillips D J, et al. Net increase in stimulatory input resulting from a decrease in inhibin B and an increase in activin a may contribute in part to the rise in follicular phase follicle-stimulating hormone of aging cycling women. J Clin Endocrinol Metab, 1998, 83: 3302–3307PubMedGoogle Scholar
  41. 41.
    Randolph J F Jr., Sowers M, Bondarenko I V, et al. Change in estradiol and follicle-stimulating hormone across the early menopausal transition: Effects of ethnicity and age. J Clin Endocrinol Metab, 2004, 89: 1555–1561PubMedGoogle Scholar
  42. 42.
    Santoro N. The menopausal transition. Am J Med, 2005, 118: 8–13PubMedGoogle Scholar
  43. 43.
    Burger H G, Hale G E, Robertson D M, et al. A review of hormonal changes during the menopausal transition: Focus on findings from the melbourne women’s midlife health project. Hum Reprod Update, 2007, 13: 559–565PubMedGoogle Scholar
  44. 44.
    Beemsterboer S N, Homburg R, Gorter N A, et al. The paradox of declining fertility but increasing twinning rates with advancing maternal age. Hum Reprod, 2006, 21: 1531–1532PubMedGoogle Scholar
  45. 45.
    Gleicher N, Weghofer A, Barad D H. Defining ovarian reserve to better understand ovarian aging. Reprod Biol Endocrinol, 2011, 9: 23PubMedPubMedCentralGoogle Scholar
  46. 46.
    Ferrell R J, Sowers M. Longitudinal, epidemiologic studies of female reproductive aging. Ann N Y Acad Sci, 2010, 1204: 188–197PubMedGoogle Scholar
  47. 47.
    Younis J S. Ovarian aging: Latest thoughts on assessment and management. Curr Opin Obstet Gynecol, 2011, 23: 427–434PubMedGoogle Scholar
  48. 48.
    Murabito J M, Yang Q, Fox C, et al. Heritability of age at natural menopause in the framingham heart study. J Clin Endocrinol Metab, 2005, 90: 3427–3430PubMedGoogle Scholar
  49. 49.
    Torgerson D J, Thomas R E, Reid D M. Mothers and daughters menopausal ages: Is there a link? Eur J Obstet Gynecol Reprod Biol, 1997, 74: 63–66PubMedGoogle Scholar
  50. 50.
    van Asselt K M, Kok H S, Pearson P L, et al. Heritability of menopausal age in mothers and daughters. Fertil Steril, 2004, 82: 1348–1351PubMedGoogle Scholar
  51. 51.
    Wicks J, Treloar S A, Martin N G. Using identity-by-de scent information in affected sib pairs to increase the efficiency of genetic association studies. Twin Res, 2004, 7: 211–216PubMedGoogle Scholar
  52. 52.
    Jagarlamudi K, Reddy P, Adhikari D, et al. Genetically modified mouse models for premature ovarian failure (POF). Mol Cell Endocrinol, 2010, 315: 1–10PubMedGoogle Scholar
  53. 53.
    Altshuler D, Brooks L D, Chakravarti A, et al. A haplotype map of the human genome. Nature, 2005, 437: 1299–1320Google Scholar
  54. 54.
    Lakhal B, Laissue P, Braham R, et al. Bmp15 and premature ovarian failure: Causal mutations, variants, polymorphisms? Clin Endocrinol, 2010, 72: 425–426Google Scholar
  55. 55.
    Willer C J, Scott L J, Bonnycastle L L, et al. Tag snp selection for finnish individuals based on the ceph utah hapmap database. Genet Epidemiol, 2006, 30: 180–190PubMedGoogle Scholar
  56. 56.
    Hamatani T, Falco G, Carter M G, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet, 2004, 13: 2263–2278PubMedGoogle Scholar
  57. 57.
    Welt C K, Smith P C, Taylor A E. Evidence of early ovarian aging in fragile X premutation carriers. J Clin Endocr Metab, 2004, 89: 4569–4574PubMedGoogle Scholar
  58. 58.
    Hsu S Y, Hsueh A J W. Tissue-specific Bcl-2 protein partners in apoptosis: An ovarian paradigm. Physiol Rev, 2000, 80: 593–614PubMedGoogle Scholar
  59. 59.
    Petros A M, Olejniczak E T, Fesik S W. Structural biology of the Bcl-2 family of proteins. Bba-Mol Cell Res, 2004, 1644: 83–94Google Scholar
  60. 60.
    He C Y, Kraft P, Chen C, et al. Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat Genet, 2009, 41: 724–728PubMedPubMedCentralGoogle Scholar
  61. 61.
    Stolk L, Zhai G, van Meurs J B J, et al. Loci at chromosomes 13, 19 and 20 influence age at natural menopause. Nat Genet, 2009, 41: 645–647PubMedPubMedCentralGoogle Scholar
  62. 62.
    Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res, 2005, 111: 206–212PubMedGoogle Scholar
  63. 63.
    Pellestor F, Andreo B, Anahory T, et al. The occurrence of aneuploidy in human: Lessons from the cytogenetic studies of human oocytes. European J Med Genet, 2006, 49: 103–116Google Scholar
  64. 64.
    Colbere-Garapin F, Duncan G, Pavio N, et al. An approach to understanding the mechanisms of poliovirus persistence in infected cells of neural or non-neural origin. Clin Diagn Virol, 1998, 9: 107–113PubMedGoogle Scholar
  65. 65.
    Battaglia D E, Goodwin P, Klein N A, et al. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod, 1996, 11: 2217–2222PubMedGoogle Scholar
  66. 66.
    Ghosh S, Bhaumik P, Ghosh P, et al. Chromosome 21 non-disjunction and down syndrome birth in an indian cohort: Analysis of incidence and aetiology from family linkage data. Genet Res, 2010, 92: 189–197Google Scholar
  67. 67.
    Hassold T, Abruzzo M, Adkins K, et al. Human aneuploidy: Incidence, origin, and etiology. Environ Mol Mutag, 1996, 28: 167–175Google Scholar
  68. 68.
    Macdonald M, Hassold T, Harvey J, et al. The origin of 47,XXY and 47,XXX aneuploidy-heterogeneous mechanisms and role of aberrant recombination. Hum Mol Genet, 1994, 3: 1365–1371PubMedGoogle Scholar
  69. 69.
    Angell R R. Predivision in human oocytes at meiosis-I — a mechanism for trisomy formation in man. Hum Genet, 1991, 86: 383–387PubMedGoogle Scholar
  70. 70.
    Petersen M B. Origin and mechanisms of nondisjunction in human autosomal trisomies. Cytogenet Cell Genet, 1999, 85: 21–21Google Scholar
  71. 71.
    Watanabe Y, Nurse P. Cohesin rec8 is required for reductional chromosome segregation at meiosis. Nature, 1999, 400: 461–464PubMedGoogle Scholar
  72. 72.
    Trifunovic A, Wredenberg A, Falkenberg M, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 2004, 429: 417–423PubMedGoogle Scholar
  73. 73.
    Seifer D B, DeJesus V, Hubbard K. Mitochondrial deletions in luteinized granulosa cells as a function of age in women undergoing in vitro fertilization. Fertil Steril, 2002, 78: 1046–1048PubMedGoogle Scholar
  74. 74.
    Tatone C, Carbone M C, Falone S, et al. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod, 2006, 12: 655–660PubMedGoogle Scholar
  75. 75.
    Perez G I, Jurisicova A, Matikainen T, et al. A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J, 2005, 19: 860–862PubMedGoogle Scholar
  76. 76.
    Perez G I, Tilly J L. Cumulus cells are required for the increased apoptotic potential in oocytes of aged mice. Hum Reprod, 1997, 12: 2781–2783PubMedGoogle Scholar
  77. 77.
    Gaulden M E. Maternal age effect: The enigma of down syndrome and other trisomic conditions. Mutat Res, 1992, 296: 69–88PubMedGoogle Scholar
  78. 78.
    Gordo A C, Rodrigues P, Kurokawa M, et al. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod, 2002, 66: 1828–1837PubMedGoogle Scholar
  79. 79.
    Eichenlaub-Ritter U, Vogt E, Yin H, et al. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online, 2004, 8: 45–58PubMedGoogle Scholar
  80. 80.
    Klein J, Sauer M V. Assessing fertility in women of advanced reproductive age. Am J Obstet Gynecol, 2001, 185: 758–770PubMedGoogle Scholar
  81. 81.
    Blasco M A, Gasser S M, Lingner J. Telomeres and telomerase. Genes Dev, 1999, 13: 2353–2359PubMedGoogle Scholar
  82. 82.
    Greider C W. Telomeres, telomerase and senescence. Bioessays, 1990, 12: 363–369PubMedGoogle Scholar
  83. 83.
    Harley C B, Futcher A B, Greider C W. Telomeres shorten during aging of human fibroblasts. Nature, 1990, 345: 458–460PubMedGoogle Scholar
  84. 84.
    Vonzglinicki T, Saretzki G, Docke W, et al. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts-a model for senescence. Exp Cell Res, 1995, 220: 186–193Google Scholar
  85. 85.
    Collins K. Structure and function of telomerase. Curr Opin Cell Biol, 1996, 8: 374–380PubMedGoogle Scholar
  86. 86.
    Harrington L A, Greider C W. Telomerase primer specificity and chromosome healing. Nature, 1991, 353: 451–454PubMedGoogle Scholar
  87. 87.
    Yu G L, Blackburn E H. Developmentally programmed healing of chromosomes by telomerase in tetrahymena. Cell, 1991, 67: 823–832PubMedGoogle Scholar
  88. 88.
    Keefe D L, Marquard K, Liu L. The telomere theory of reproductive senescence in women. Curr Opin Obstet Gyn, 2006, 18: 280–285Google Scholar
  89. 89.
    Kinugawa C, Murakami T, Okamura K, et al. Telomerase activity in normal ovaries and premature ovarian failure. Tohoku J Exp Med, 2000, 190: 231–238PubMedGoogle Scholar
  90. 90.
    Hanna C W, Bretherick K L, Gair J L, et al. Telomere length and reproductive aging. Hum Reprod, 2009, 24: 1206–1211PubMedPubMedCentralGoogle Scholar
  91. 91.
    Butts S, Riethman H, Ratcliffe S, et al. Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab, 2009, 94: 4835–4843PubMedPubMedCentralGoogle Scholar
  92. 92.
    Moore G E. Biochemical and cellular mechanisms of aging and degenerative disease: Excessive, poor-quality caloric intake may deplete essential nutrients and interfere with cellular processes to produce degenerative damage. Med Hypotheses, 2008, 70: 768–775PubMedGoogle Scholar
  93. 93.
    Yin D, Chen K. The essential mechanisms of aging: Irreparable damage accumulation of biochemical side-reactions. Exp Gerontol, 2005, 40: 455–465PubMedGoogle Scholar
  94. 94.
    Sohal R S. Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med, 2002, 33: 37–44PubMedGoogle Scholar
  95. 95.
    Agarwal A, Aponte-Mellado A, Premkumar B J, et al. The effects of oxidative stress on female reproduction: A review. Reprod Biol Endocrinol, 2012, 10: 49PubMedPubMedCentralGoogle Scholar
  96. 96.
    Sahin E, Depinho R A. Axis of ageing: Telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol, 2012, 13: 397–404PubMedPubMedCentralGoogle Scholar
  97. 97.
    Miquel J, Economos A C, Fleming J, et al. Mitochondrial role in cell aging. Exp Gerontol, 1980, 15: 575–591PubMedGoogle Scholar
  98. 98.
    Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: Implications for cell death. Ann Rev Pharmacol Toxicol, 2007, 47: 143–183Google Scholar
  99. 99.
    Vercesi A E, Kowaltowski A J, Oliveira H C, et al. Mitochondrial Ca2+ transport, permeability transition and oxidative stress in cell death: Implications in cardiotoxicity, neurodegeneration and dyslipidemias. Front Biosci, 2006, 11: 2554–2564PubMedGoogle Scholar
  100. 100.
    Tatone C, Amicarelli F, Carbone M C, et al. Cellular and molecular aspects of ovarian follicle ageing. Hum Reprod Update, 2008, 14: 131–142PubMedGoogle Scholar
  101. 101.
    Wiener-Megnazi Z, Vardi L, Lissak A, et al. Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil Steril, 2004, 82: 1171–1176PubMedGoogle Scholar
  102. 102.
    Tarin J J. Aetiology of age-associated aneuploidy: A mechanism based on the ‘free radical theory of ageing’. Hum Reprod, 1995, 10: 1563–1565PubMedGoogle Scholar
  103. 103.
    Tarin J J. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod, 1996, 2: 717–724PubMedGoogle Scholar
  104. 104.
    Tamura H, Takasaki A, Miwa I, et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res, 2008, 44: 280–287PubMedGoogle Scholar
  105. 105.
    Liu L, Keefe D L. Cytoplasm mediates both development and oxidation-induced apoptotic cell death in mouse zygotes. Biol Reprod, 2000, 62: 1828–1834PubMedGoogle Scholar
  106. 106.
    Liu L, Trimarchi J R, Keefe D L. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod, 2000, 62: 1745–1753PubMedGoogle Scholar
  107. 107.
    Lass A, Skull J, McVeigh E, et al. Measurement of ovarian volume by transvaginal sonography before ovulation induction with human menopausal gonadotrophin for in-vitro fertilization can predict poor response. Hum Reprod, 1997, 12: 294–297PubMedGoogle Scholar
  108. 108.
    Van Blerkom J. The influence of intrinsic and extrinsic factors on the developmental potential and chromosomal normality of the human oocyte. J Soc Gynecol Investig, 1996, 3: 3–11PubMedGoogle Scholar
  109. 109.
    Tarin J J, Perez-Albala S, Cano A. Oral antioxidants counteract the negative effects of female aging on oocyte quantity and quality in the mouse. Mol Reprod Dev, 2002, 61: 385–397PubMedGoogle Scholar
  110. 110.
    Zhang X, Wu X Q, Lu S, et al. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res, 2006, 16: 841–850PubMedGoogle Scholar
  111. 111.
    Carbone M C, Tatone C, Delle Monache S, et al. Antioxidant enzymatic defences in human follicular fluid: Characterization and age-dependent changes. Mol Hum Reprod, 2003, 9: 639–643PubMedGoogle Scholar
  112. 112.
    Gonzalez-Parraga P, Hernandez J A, Arguelles J C. Role of antioxidant enzymatic defences against oxidative stress H2O2 and the acquisition of oxidative tolerance in candida albicans. Yeast, 2003, 20: 1161–1169PubMedGoogle Scholar
  113. 113.
    Yim M B, Yim H S, Lee C, et al. Protein glycation: Creation of catalytic sites for free radical generation. Ann N Y Acad Sci, 2001, 928: 48–53PubMedGoogle Scholar
  114. 114.
    Schmidt A M, Yan S D, Yan S F, et al. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta, 2000, 1498: 99–111PubMedGoogle Scholar
  115. 115.
    Mullarkey C J, Edelstein D, Brownlee M. Free radical generation by early glycation products: A mechanism for accelerated atherogenesis in diabetes. Biochem Biophys Res Commun, 1990, 173: 932–939PubMedGoogle Scholar
  116. 116.
    Sakurai T, Tsuchiya S. Superoxide production from nonenzymatically glycated protein. FEBS Lett, 1988, 236: 406–410PubMedGoogle Scholar
  117. 117.
    Wen Y, Skidmore J C, Porter-Turner M M, et al. Relationship of glycation, antioxidant status and oxidative stress to vascular endothelial damage in diabetes. Diabetes Obes Metab, 2002, 4: 305–308PubMedGoogle Scholar
  118. 118.
    Soldatos G, Cooper M E. Advanced glycation end products and vascular structure and function. Curr Hypertens Rep, 2006, 8: 472–478PubMedGoogle Scholar
  119. 119.
    Frye E B, Degenhardt T P, Thorpe S R, et al. Role of the maillard reaction in aging of tissue proteins. Advanced glycation end product-dependent increase in imidazolium cross-links in human lens proteins. J Biol Chem, 1998, 273: 18714–18719PubMedGoogle Scholar
  120. 120.
    Kim J, Kim O S, Kim C S, et al. Accumulation of argpyrimidine, a methylglyoxal-derived advanced glycation end product, increases apoptosis of lens epithelial cells both in vitro and in vivo. Exp Mol Med, 2012, 44: 167–175PubMedPubMedCentralGoogle Scholar
  121. 121.
    Mizutani K, Ikeda K, Tsuda K, et al. Inhibitor for advanced glycation end products formation attenuates hypertension and oxidative damage in genetic hypertensive rats. J Hypertens, 2002, 20: 1607–1614PubMedGoogle Scholar
  122. 122.
    Dixit H, Rao L K, Padmalatha V V, et al. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet, 2006, 119: 408–415PubMedGoogle Scholar
  123. 123.
    Laissue P, Christin-Maitre S, Touraine P, et al. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol, 2006, 154: 739–744PubMedGoogle Scholar
  124. 124.
    Schmidt D, Ovitt C E, Anlag K, et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development, 2004, 131: 933–942PubMedGoogle Scholar
  125. 125.
    Van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: Association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum Reprod, 1997, 12: 1047–1055PubMedGoogle Scholar
  126. 126.
    Modlich U, Kaup F J, Augustin H G. Cyclic angiogenesis and blood vessel regression in the ovary: Blood vessel regression during luteolysis involves endothelial cell detachment and vessel occlusion. Lab Invest, 1996, 74: 771–780PubMedGoogle Scholar
  127. 127.
    Redmer D A, Reynolds L P. Angiogenesis in the ovary. Rev Reprod, 1996, 1: 182–192PubMedGoogle Scholar
  128. 128.
    Huey S, Abuhamad A, Barroso G, et al. Perifollicular blood flow doppler indices, but not follicular po2, pco2, or ph, predict oocyte developmental competence in in vitro fertilization. Fertil Steril, 1999, 72: 707–712PubMedGoogle Scholar
  129. 129.
    Bhal P S, Pugh N D, Gregory L, et al. Perifollicular vascularity as a potential variable affecting outcome in stimulated intrauterine insemination treatment cycles: A study using transvaginal power doppler. Hum Reprod, 2001, 16: 1682–1689PubMedGoogle Scholar
  130. 130.
    Borini A, Maccolini A, Tallarini A, et al. Perifollicular vascularity and its relationship with oocyte maturity and IVF outcome. Ann N Y Acad Sci, 2001, 943: 64–67PubMedGoogle Scholar
  131. 131.
    Amicarelli F, Ragnelli A M, Aimola P, et al. Age-dependent ultrastructural alterations and biochemical response of rat skeletal muscle after hypoxic or hyperoxic treatments. Biochim Biophys Acta, 1999, 1453: 105–114PubMedGoogle Scholar
  132. 132.
    Vessey M P, Villard-Mackintosh L, Painter R. Epidemiology of endometriosis in women attending family planning clinics. BMJ, 1993, 306: 182–184PubMedPubMedCentralGoogle Scholar
  133. 133.
    Allaire C. Endometriosis and infertility: A review. J Reprod Med, 2006, 51: 164–168PubMedGoogle Scholar
  134. 134.
    Jacobson T Z, Duffy J M, Barlow D, et al. Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev, 2010, CD001398Google Scholar
  135. 135.
    Islam M N, Islam M M. Biological and behavioural determinants of fertility in bangladesh: 1975–1989. Asia Pac Popul J, 1993, 8: 3–18PubMedGoogle Scholar
  136. 136.
    McKinlay S M, Brambilla D J, Posner J G. The normal menopause transition. Maturitas, 2008, 61: 4–16PubMedGoogle Scholar
  137. 137.
    Jensen T K, Henriksen T B, Hjollund N H, et al. Adult and prenatal exposures to tobacco smoke as risk indicators of fertility among 430 danish couples. Am J Epidemiol, 1998, 148: 992–997PubMedGoogle Scholar
  138. 138.
    Sharara F I, Scott R T Jr., Seifer D B. The detection of diminished ovarian reserve in infertile women. Am J Obstet Gynecol, 1998, 179: 804–812PubMedGoogle Scholar
  139. 139.
    Goldin A, Beckman J A, Schmidt A M, et al. Advanced glycation end products: Sparking the development of diabetic vascular injury. Circulation, 2006, 114: 597–605PubMedGoogle Scholar
  140. 140.
    Richardson S J, Nelson J F. Follicular depletion during the menopausal transition. Ann N Y Acad Sci, 1990, 592: 13–20; discussion 44–51PubMedGoogle Scholar
  141. 141.
    Lass A, Silye R, Abrams D C, et al. Follicular density in ovarian biopsy of infertile women: A novel method to assess ovarian reserve. Hum Reprod, 1997, 12: 1028–1031PubMedGoogle Scholar
  142. 142.
    Lambalk C B, de Koning C H, Flett A, et al. Assessment of ovarian reserve. Ovarian biopsy is not a valid method for the prediction of ovarian reserve. Hum Reprod, 2004, 19: 1055–1059Google Scholar
  143. 143.
    Hendriks D J, Kwee J, Mol B W J, et al. Ultrasonography as a tool for the prediction of outcome in ivf patients: A comparative meta-analysis of ovarian volume and antral follicle count. Fertil Steril, 2007, 87: 764–775PubMedGoogle Scholar
  144. 144.
    van Rooij I A J, Tonkelaar I, Broekmans F J M, et al. Anti-mullerian hormone is a promising predictor for the occurrence of the menopausal transition. Menopause, 2004, 11: 601PubMedGoogle Scholar
  145. 145.
    Broekmans F J, de Ziegler D, Howles C M, et al. The antral follicle count: Practical recommendations for better standardization. Fertil Steril, 2010, 94: 1044–1051PubMedGoogle Scholar
  146. 146.
    Younis J S, Haddad S, Matilsky M, et al. Undetectable basal ovarian stromal blood flow in infertile women is related to low ovarian reserve. Gynecol Endocrinol, 2007, 23: 284–289PubMedGoogle Scholar
  147. 147.
    Robertson D M. Anti-müllerian hormone as a marker of ovarian reserve: An update. Women’s Health, 2008, 4: 137–141PubMedGoogle Scholar
  148. 148.
    Sowers M F R, Eyvazzadeh A D, McConnell D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab, 2008, 93: 3478–3483PubMedPubMedCentralGoogle Scholar
  149. 149.
    Sharov A A, Falco G, Piao Y, et al. Effects of aging and calorie restriction on the global gene expression profiles of mouse testis and ovary. BMC Biol, 2008, 6: 24PubMedPubMedCentralGoogle Scholar
  150. 150.
    Welt C K, Smith Z A, Pauler D K, et al. Differential regulation of inhibin a and inhibin B by luteinizing hormone, follicle-stimulating hormone, and stage of follicle development. J Clin Endocr Metab, 2001, 86: 2531–2537PubMedGoogle Scholar
  151. 151.
    Catteau-Jonard S, Pigny P, Reyss A C, et al. Changes in serum anti-müllerian hormone level during low-dose recombinant follicular-stimulating hormone therapy for anovulation in polycystic ovary syndrome. J Clin Endocr Metab, 2007, 92: 4138–4143PubMedGoogle Scholar
  152. 152.
    Fanchin R, Schonauer L M, Righini C, et al. Serum anti-mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod, 2003, 18: 323–327PubMedGoogle Scholar
  153. 153.
    Ficicioglu C, Kutlu T, Baglam E, et al. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril, 2006, 85: 592–596PubMedGoogle Scholar
  154. 154.
    Visser J A, de Jong F H, Laven J S E, et al. Anti-müllerian hormone: A new marker for ovarian function. Reproduction, 2006, 131: 1–9PubMedGoogle Scholar
  155. 155.
    de Vet A, Laven J S E, de Jong F H, et al. Antimüllerian hormone serum levels: A putative marker for ovarian aging. Fertil Steril, 2002, 77: 357–362PubMedGoogle Scholar
  156. 156.
    Hagstad A, Johansson S, Wilhelmsson C, et al. Gynaecology of middle-aged women — menstrual and reproductive histories. Maturitas, 1985, 7: 99–113PubMedGoogle Scholar
  157. 157.
    van Rooij I A J, Broekmans F J M, Scheffer G J, et al. Serum antimüllerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: A longitudinal study. Fertil Steril, 2005, 83: 979–987PubMedGoogle Scholar
  158. 158.
    Fanchin R, Taieb J, Lozano D H M, et al. High reproducibility of serum anti-müllerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status. Hum Reprod, 2005, 20: 923–927PubMedGoogle Scholar
  159. 159.
    La Marca A, Sighinolfi G, Radi D, et al. Anti-müllerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update, 2010, 16: 113–130PubMedGoogle Scholar
  160. 160.
    Sowers M R, Eyvazzadeh A D, McConnell D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab, 2008, 93: 3478–3483PubMedPubMedCentralGoogle Scholar
  161. 161.
    Groome N P, Illingworth P J, O’Brien M, et al. Detection of dimeric inhibin throughout the human menstrual cycle by two-site enzyme immunoassay. Clin Endocrinol (Oxf), 1994, 40: 717–723Google Scholar
  162. 162.
    Groome N P, Illingworth P J, O’Brien M, et al. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab, 1996, 81: 1401–1405PubMedGoogle Scholar
  163. 163.
    Hall J E, Welt C K, Cramer D W. Inhibin A and inhibin B reflect ovarian function in assisted reproduction but are less useful at predicting outcome. Hum Reprod, 1999, 14: 409–415PubMedGoogle Scholar
  164. 164.
    Hartge P. Genetics of reproductive lifespan. Nat Genet, 2009, 41: 637–638PubMedGoogle Scholar
  165. 165.
    Kok H S, van Asselt K M, van der Schouw Y T, et al. Genetic studies to identify genes underlying menopausal age. Hum Reprod Update, 2005, 11: 483–493PubMedGoogle Scholar

Copyright information

© The Author(s) 2012

Authors and Affiliations

  • Qian Li
    • 1
  • XiaoDan Geng
    • 1
  • Wei Zheng
    • 1
  • Jie Tang
    • 1
  • Bo Xu
    • 1
  • QingHua Shi
    • 1
    Email author
  1. 1.Hefei National Laboratory for Physical Sciences at Microscale and School of Life SciencesUniversity of Science and Technology of ChinaHefeiChina

Personalised recommendations