Cellular and molecular aspects of ovarian follicle ageing

Human Reproduction Update

Volumn 14, Issue 2, 2008, Pages 131-142

  Tatone, Carla ^a   Amicarelli, Fernanda ^a   Carbone, Maria Cristina ^a   Monteleone, Patrizia ^b   Caserta, Donatella ^c   Marci, Roberto ^d   Artini, Paolo Giovanni ^b   Piomboni, Paola ^e   Focarelli, Riccardo ^e  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF L'AQUILA   (Italy)

^e UNIVERSITY OF SIENA   (Italy)

Author keywords

Antioxidants; Female infertility; Follicle development; Ovarian function; Oxidative stress

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ANTIOXIDANT; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; FREE RADICAL; GLUTATHIONE DISULFIDE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE;

AGING; CELL AGING; FEMALE INFERTILITY; FERTILIZATION IN VITRO; GAMETE; GRANULOSA CELL; HUMAN; METABOLISM; MICROENVIRONMENT; OVARY FOLLICLE CELL; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; OXIDATIVE STRESS; PRIORITY JOURNAL; REPRODUCTIVE HEALTH; REVIEW; TREATMENT OUTCOME; VASCULARIZATION;

AGING; CELL AGING; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INFERTILITY, FEMALE; OVARIAN FOLLICLE; OXIDATIVE STRESS;

EID: 40049086074     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmm048     Document Type: Review

References (157)

1. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3:28.
2. Amicarelli F, Ragnelli AM, Aimola P, Bonfigli A, Colafarina S, Di Ilio C, Miranda M. Age-dependent ultrastructural alterations and biochemical response of rat skeletal muscle after hypoxic or hyperoxic treatments. Biochim Biophys Acta 1999;1453:105-114.
3. Amicarelli F, Ragnelli AM, Aimola P, Cattani F, Bonfigli A, Zarivi O, Miranda M, Di Ilio C. Developmental expression and distribution of amphibian glutathione transferases. Biochim Biophys Acta 2001; 1526:77-85.
4. Artini PG, Fasciani A, Monti M, Luisi S, D'Ambrogio G, Genazzani AR. Changes in vascular endothelial growth factor levels and the risk of ovarian hyperstimulation syndrome in women enrolled in an in vitro fertilization program. Fertil Steril 1998;70:560-564.
5. Artini PG, Monti M, Cristello F, Matteucci C, Bruno S, Valentino V, Genazzani AR. Vascular endothelial growth factor in females of reproductive age. Gynecol Endocrinol 2003;17:477-492.
6. Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK: The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization, Int J Fertil 2000;45 314-320.
7. Bachvarova R. Gene expression during oogenesis and oocyte development in mammals. Dev Biol 1985;1:453-524.
8. Baird DT, Collins J, Egozcue J, Evers LH, Gianaroli L, Leridon H, Sunde A, Templeton A, Van Steirteghem A, Cohen J et al. Fertility and ageing. Hum Reprod Update 2005;11:261-276.
9. Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 1996;11:2217-2222.
10. Baynes JW. The role of AGEs in aging: Causation or correlation. Exp Gerontol 2001;36:1527-1537.
11. Bell EL, Emerling BM, Chandel NS. Mitochondrial regulation of oxygen sensing. Mitochondrion 2005;5:322-332.
12. Bengmark S. Impact of nutrition on aging and disease. Curr Opin Clin Nutr Metab Care 2006;9:2-7,
13. Bhal PS, Pugh ND, Chui DK, Gregory L, Walker SM, Shaw RW. The use of transvaginal power Doppler ultrasonography to evaluate the relationship between perifollicular vascularity and outcome in in-vitro fertilization treatment cycles. Hum Reprod 1999;14:939-945.
14. Bhal PS, Pugh ND, Gregory L, O'Brien S, Shaw RW. Perifollicular vascularity as a potential variable affecting outcome in stimulated intrauterine insemination treatment cycles: A study using transvaginal power Doppler. Hum Reprod 2001;16:1682-1689.
15. Bohlender JM, Franke S, Stein G, Wolf G. Advanced glycation end products and the kidney. Am J Physiol Renal Physiol 2005;289 F645-F659.
16. Brann DW, Mahesh VB. The aging reproductive neuroendocrine axis. Steroids 2005;70:273-283.
17. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Mayo KE, Shea LD, Woodruff TK. Fate of the initial follicle pool: Empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev Biol 2006;298: 149-154.
18. Broekmans FJ, Knauff EA, te Velde ER, Macklon NS, Fauser BC. Female reproductive ageing: Current knowledge and future trends. Trends Endocrinol Metab 2007;18:58-65.
19. Brook JD, Gosden RG, Chandley AC. Maternal ageing and aneuploid embryos - evidence from the mouse that biological and not chronological age is the important influence. Hum Genet 1984;66:41-45.
20. Burger HG, Dudley EC, Hopper JL, Groome N, Guthrie JR, Green A, Dennerstein L. Prospectively measured levels of serum follicle-stimulating hormone, estradiol, and the dimeric inhibins during the menopausal transition in a population-based cohort of women. J Clin Endocrinol Metab 1999;84:4025-4030.
21. Byskov AG. Differentiation of mammalian embryonic gonad. Physiol Rev 1986;66:71-117.
22. Carbone MC, Tatone C, Delle Monache S, Marci R, Caserta D, Colonna R, Amicarelli F. Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Mol Hum Reprod 2003; 9:639-643.
23. Chandel NS, Budinger GR. The cellular basis for diverse responses to oxygen. Free Radic Biol Med 2007;42:165-174.
24. Chaudhury K, Das S, Chattopadhyay R, Ghosh S, Goswami S, Ghosh S, Chakravarty B. Reactive oxygen species and fertilization (author reply). Hum Reprod 2007;22:901-902.
25. Cohen AA. Female post-reproductive lifespan: A general mammalian trait. Biol Rev Camb Philos Soc 2004;79:733-750.
26. Collins AR. Assays for oxidative stress and antioxidant status: applications to research into-the biological effectiveness of polyphenols. Am J Clin Nutr 2005;81(Suppl):261S-267S.
27. Costello MF, Shrestha SM, Sjoblom P, McNally G, Bennett MJ, Steigrad SJ, Hughes GJ: Power doppler ultrasound assessment of the relationship between age and ovarian perifollicular blood flow in women undergoing in vitro fertilization treatment. J Assist Reprod Genet 2006;23 359-365.
28. Craig J, Orisaka M, Wang H, Orisaka S, Thompson W, Zhu C, Kotsuji F, Tsang BK. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: The delicate balance between life and death. Front Biosci. 2007;12:3628-3639.
29. Cukurcam S, Betzendahl I, Michel G, Vogt E, Hegele-Hartung C, Lindenthal B, Eichenlaub-Ritter U. Influence of follicular fluid meiosis-activating sterol on aneuploidy rate and precocious chromatid segregation in aged mouse oocytes. Hum Reprod 2007;22:815-828.
30. Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A. Biomarkers of oxidative damage in human disease. Clin Chem 2006;52 601-623.
31. Dalton TP, Shertzer HG, Puga A. Regulation of gene expression by reactive oxygen. Aannu Rev Pharmacol Toxicol 1999;39:67-101.
32. Das S, Chattopadhyay R, Ghosh S, Ghosh S, Goswami SK, Chakravarty BN, Chaudhury K. Reactive oxygen species level in follicular fluid-embryo quality marker in IVF? Hum Reprod 2006;21;2403-2407.
33. Davies MJ, Fu S, Vang H, Dean RT. Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Rad Biol Med 1999;27:1151-1163.
34. de Bruin JP, Dorland M, Spek ER, Posthuma G, van Haaften M, Looman CW, te Velde ER. Ultrastructure of the resting ovarian follicle pool in healthy young women. Biol Reprod 2002;66:1151-1160.
35. de Bruin JP, Dorland M, Spek ER, Posthuma G, van Haaften M, Looman CW, te Velde ER: Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol Reprod 2004;70:419-424.
36. De Lamirande E, Gagnon C. Redox control of protein sulfhydryl levels during human sperm capacitation. Free Rad Biol Med 2003;35 1271-1285.
37. de Vet A, Laven JS, de Jong FH, Themmen AP, Fauser BC. Antimullerian hormone serum levels: A putative marker for ovarian aging. Fertil Steril 2002;77:357-362.
38. Del Rio, D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecules and biological marker of oxidative stress. Nutr Metab Cardiovas 2005;15:316,328.
39. Diamanti-Kandarakis E, Piperi C, Patsouris E, Korkolopoulou P, Panidis D, Pawelczyk L, Papavassiliou AG, Duleba AJ. Immunohistochemical localization of advanced glycation end-products (AGEs) and their receptor (RAGE) in polycystic and normal ovaries. Histochem Cell Biol 2007;127:581-589.
40. Dixit H, Rao LK, Padmalatha VV, Kanakavalli M, Deenadayal M, Gupta N, Chakrabarty B, Singh L. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet 2006;119:408-415.
41. Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol 2007;77:21-49.
42. Eaton P. protein thiol oxidation in health and disease: Techniques for measuring disulfides and related modification in complex protein mixtures. Free Radic Biol Med 2006;40:1889-1999.
43. Eichenlaub-Ritter U. Genetics of oocyte ageing. Maturitas 1998; 30:143-169.
44. Eichenlaub-Ritter U, Vogt E, Yin H, Gosden R. Spindles, mitochondria and redox potential in ageing oocytes. Reprod Biomed Online 2004;8 45-58.
45. El Mouatassim S, Guerin P, Menezo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Mol Hum Reprod 1999;5:720-725.
46. Eppig JJ, O'Brien MJ. In vitro maturation and fertilization of oocytes isolated from aged mice: A strategy to rescue valuable genetic resources. Assist Reprod Genet 1995;12:269-273.
47. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause. Hum Reprod. 1992;7:1342-1346.
48. Fanchin R, Mendez Lozano DH, Frydman N, Gougeon A, di Clemente N, Frydman R, Taieb J. Anti-Mullerian hormone concentrations in the follicular fluid of the preovulatory follicle are predictive of the implantation potential of the ensuing embryo obtained by in vitro fertilization. J Clin Endocrinol Metab. 2007;92:1796-1802.
49. Friedman CI, Danforth DR, Herbosa-Encarnacion C, Arbogast L, Alak BM, Seifer DB. Follicular fluid vascular, endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction. Fertil Steril 1997;68 607-612.
50. Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, Nakamura H, Ogita S, Sato E, Inoue M. DNA fragmentation of oocytes in aged mice. Hum Reprod 1996;11:1480-1483.
51. Gaulden ME. Maternal age effect: The enigma of Down syndrome and other trisomic conditions. Mutat Res 1992;296:69-88.
52. Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 2004; 82-83:431-446.
53. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: Sparking the development of diabetic vascular injury. Circulation 2006;114:597-605.
54. Gougeon A, Chainy GB. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 1987;81:433-442.
55. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS. Age-associated alteration of gene expression patterns in mouse oocytes. Ham Mol Genet 2004;13:2263-2278.
56. Hamet P, Tremblay J. Genes of aging. Metabolism 2005;52:5-9.
57. Harman D. Aging: A theory based on free radical and radiation chemistry. J Gerontol 1956;11:298-300.
58. HarmaI D. Free, radical theory of aging: An update: increasing the functional life span. Ann N Y Acad Sci 2006;1067:10-21.
59. Hayes JD, McLellan LL. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Rad Res 1999;31:273-300.
60. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA. SMC1beta-deficient female mice provide evidence that cohesins are missing link in age-related nondisjunction. Nat Genet 2005;37 1351-1355.
61. Homer HA. Mad2 and spindle assembly checkpoint function during meiosis I in mammalian oocytes. Histol Histopathol 2006;21:873-886.
62. Huey S, Abuhamad A, Barroso G, Hsu MI, Kolm P, Mayer J, Oehninger S. Perifollicular blood flow Doppler indices, but not follicular pO2, pCO2, or pH, predict oocyte developmental competence in in vitro fertilization. Fertil Steril 1999;72:707-712.
63. Jiang JY, Cheung CK, Wang Y, Tsang BK. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 2003;8:d222-d237.
64. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 2004;428:145-150.
65. Jozwik M, Wolczynski S, Jozwik M, Szamatowicz M. Oxidative stress markers in preovulatory follicular fluid in humans. Mol Hum Reprod 1999;5:409-413.
66. Kamel NS, Gammack J, Cepeda O, Flaherty JH. Antioxidants and hormones as antiaging therapies: High hopes, disappointing results. Cleve Clin J Med 2006;73:1049-1056.
67. Keefe DL, Niven-Fairchild T, Powell S, Buradagunta S. Mitochondrial deoxyribonucleic acid deletions in oocytes and reproductive aging in women. Fertil Steril 1995;64:577-583.
68. Keefe DL, Liu L, Marquard K. Telomeres and aging-related meiotic dysfunction in women. Cell Mol Life Sci 2007;64:139-143.
69. Kevenaar ME, Meerasahib MF, Kramer P, van de Lang-Born BM, de Jong FH, Groome NP, Themmen AP, Visser JA. Serum anti-mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology 2006;147:3228-3234.
70. Klein NA, Battaglia DE, Woodruff TK, Padmanabhan V, Giudice LC, Bremner WJ, Soules MR. Ovarian follicular concentrations of activin, follistatin, inhibin, insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-2 (IGFBP-2), IGFBP-3, and vascular endothelial growth factor in spontaneous menstrual cycles of normal women of advanced reproductive age. J Clin Endocrinol Metab 2000;85 4520-4525.
71. Kok HS, van Asselt KM, Schouw van der YT, Tweel van der I, Peeters PH, Wilson PW, Pearson PL, Grobbee DE. Heart disease risk determines menopausal age rather than the reverse. J Am Coll Cardiol 2006; 47:1976-1983.
72. Kregel KC, Zhang HJ. An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Integr Comp Physiol 2007;292:R18-R36.
73. Kuliev A, Cieslak J, Verlinsky Y. Frequency and distribution of chromosome abnormalities in human oocytes. Cytogenet Genome Res 2005;111: 193-198.
74. Laissue P, Christin-Maitre S, Touraine P, Kuttenn F, Ritvos O, Aittomaki K, Bourcigaux N, Jacquesson L, Bouchard P, Frydman R et al. Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur J Endocrinol 2006;154:739-744.
75. Lam PM, Haines C. Vascular endothelial growth factor plays more than an angiogenic role in the female reproductive system. Fertil Steril 2005;84:1775-1778.
76. Ledent C, Demeestere I, Blum D, Petermans J, Hamalainen T, Smits G, Vassart G. Premature ovarian aging in mice deficient for Gpr3. Proc Natl Acad Sci USA 2005;102:8922-8926.
77. Li Y, Zhu H, Kuppusamy P, Roubaud V, Zweier JL, Trush MA. Validation of lucigenin (Bis-N-methylacridium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J Biol Chem 1998;273:2015-2023.
78. Linton S, Davies MJ, Dean RT. Protein oxidation and ageing. Exp Gerontol 2001;36:1503-1518.
79. Liu L, Keefe DL. Ageing-associated aberration in meiosis of oocytes from senescence-accelerated mice. Hum Reprod 2002;17:2678-2685.
80. Liu Y, Wu C, Lyu Q, Yang D, Albertini DF, Keefe DL, Liu L. Germline stem cells and neo-oogenesis in the adult human ovary. Dev Biol 2007; 306:112-120.
81. Malmanche N, Maia A, Sunkel CE. The spindle assembly checkpoint: preventing chromosome mis-segregation during- mitosis and meiosis. FEBS Lett 2006;580:2888-2895.
82. McTavish KJ, Jimenez M, Walters KA, Spaliviero J, Groome NP Themmen AP, Visser JA, Handelsman DJ, Allan CM. Rising follicle-stimulating hormone levels with age accelerate female reproductive failure. Endocrinology 2007;148:4432-4439.
83. Miquel J, Economos AC, Fleming J, Johnson JE, Jr. Mitochondrial role in cell aging. Exp Gerontol 1980;15:575-591.
84. Moffatt O, Drury S, Tomlison M, Afnan M, Denny S. The apoptotic profile of human cumuflus cells changes with patient age and after exposure to sperm but not in relation to oocyte maturity. Fertil Steril 2002;77: 1006-1011.
85. Ng EH, Chan CC, Yeung WS, Ho PC. Effect of age on ovarian stromal flow measured by three-dimensional ultrasound with power Doppler in Chinese-women with proven fertility. Hum Reprod 2004;19 2132-2137.
86. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 2007;47 143-183.
87. Ottolenghi C, Uda M, Hamatani T, Crisponi L, Garcia JE, Ko M, Pilia G, Sforza C, Schlessinger D, Forabosco A. Aging of oocyte, ovary, and human reproduction. Ann N Y Acad Sci. 2004;1034:117-131.
88. Oya T, Hattori N, Mizuno Y, Miyata S, Maeda S, Osawa T, Uchida K. Methylglyoxal modification of protein. Chemical and immunochemical characterization of methylglyoxal-arginine adducts. Biol Chem 1999;274:18492-18502.
89. Oyawoye O, Abdel Gadir A, Garner A, Constantinovici N, Perrett C, Hardiman P. Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: Relationship to outcome. Human Reprod 2003;11:2270-2274.
90. Pangas SA. Growth factors in ovarian development. Semin Reprod Med 2007;25:225-234.
91. Pasqualotto EB, Agarwal A, Sharma RK, Izzo VM, Pinotti JA, Joshi NJ, Rose BI. Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 2004;81 973-976.
92. Pasqualotto FF, Pasqualotto EB. Reactive oxygen species and fertilization. Hum Reprod 2007;22:901.
93. Pellestor F, Anahory T, Hamamah S. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet Genome Res 2005;111:206-212.
94. Pellicer A, Mari M, Santos MJ, Simon C, Remohi J, Tarin JJ. Effects of aging on human ovary: Secretion of immnunoreactive alpha-inhibin and progesterone, Fertil Steril 1994;61:663-668.
95. Pepling ME. From primordial germ cell to primordial follicle: Mammalian female germ cell development. Genesis. 2006;44:622-632.
96. Perez GI, Jurisicova A, Matikainen T, Moriyama T, Kim MR, Takai Y, Pru JK, Kolesnick RN, Tilly JL. A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J 2005;19:60-862.
97. Perez GI, Tilly JL. Cumulus cells are required for the increased apoptotic potential in oocytes of aged mice. Hum Reprod 1997;12 2781-2783.
98. Prior RL, Cao G. In vivo total antioxidant capacity: Comparison of different analytical methods. Free Radic Biol Med 1999;27 1173-1181.
99. Pripp U, Eriksson-Berg M, Orth-Gomer K, Schenck-Gustafsson K, Landgren BM. Does body mass index, smoking, lipoprotein levels, surgically induced menopause, hormone replacement therary, years since menopause, or age affect hemostasis in postmenopausal women? Gend Med 2005; 2:88-95.
100. Rabilloud T, Chevallet M, Luche S, Leize-Wagner E. Oxidative stress response: A proteomic view. Expert Rev Proteomics 2005;2 949-956.
101. Ramasamy R, Yan SF, Schmidt AM. Methylglyoxal comes of AGE. Cell 2006;124:258-260.
102. Redmer AD, Reynolds LP. Angiogenesis in the ovary. Rev Reprod 1996;1:182-192.
103. Richardson SJ, Nelson JF. Follicalar depletion during the menopausal transition. Ann N Y Acad Sci 1990;592:13-20.
104. Sauer MV, Paulson RJ, Lobo RA. A preliminary report on oocyte donation extending reproductive potential to women over 40. N Engl J Med 1990;323-1157-1160.
105. Schmidt AM, Yan SD, Yan SF, Stern DM. The biology of the receptor for advanced glycation end products and its ligands. Biochim Biophys Acta 2000;1498:99-111.
106. Schmidt D, Ovitt CE, Anlag K, Fehsenfeld S, Gredsted L, Treier AC, Treier M. The murine winged-helix transcription factor Fox12 is required for granulosa cell differentiation and ovary maintenance. Development 2004;131:933-942.
107. Seffer DB, Gardiner AC, Ferreira KA, Peluso JJ. Apoptosis as a function of ovarian reserve in women undergoing in vitro fertilization. Fertil Steril 1996a,66:593-598.
108. Seifer DB, Gardiner AC, Lambert-Messerlian G, Schneyer AL. Differential secretion of dimeric inhibin in cultured luteinized granulosa cells as a function of ovarian reserve. J Clin Endocrinol Metab 1996b;81 736-739.
109. Seifer DB, DeJesus V, Hubbard K. Mitochondrial deletions in luteinized granulosa cells as a function of age in women undergoing in vitro fertilization. Fertil Steril 2002;78:1046-1048.
110. Shoubridge EA, Wai T. Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol 2007;77:87-111.
111. Sohal RS. Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med 2002;33:37-44.
112. Soldatos G, Cooper ME. Advanced glycation end products and vascular structure and function. Curr Hypertens Rep 2006;8:472-478.
113. Steuerwald N, Cohen J, Herreta RJ, Sandalinas M, Brenner CA. Association between spindle assembly checkpoint expression and maternal age in human oocytes. Mol Hum Reprod 2001;7:49-55.
114. Steuerwald NM, Bermudez MG, Wells D, Munne S, Cohert J. Maternal age related differential global expression profiles observed in human oocytes. Reprod Biomed Online 2007;14:700-708.
115. Takeuchi T, Neri QV, Katagiri Y, Rosenwaks Z, Palermo GD. Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol Reprod 2005;72:584-592.
116. Tarin JJ. Aetiology of age-associated aneuploidy: A mechanism based on the 'free radical theory of ageing'. Hum Reprod 1995;10 1563-1565.
117. Tarin JJ. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod 1996;2:717-224.
118. Tarin JJ, Perez-Albala S, Cano A. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod 2001;65:141-150.
119. Tarin JJ, 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 2002a;61:385-397.
120. Tarin JJ, Perez-Albala S, Pertusa JF, Cano A. Oral administration of pharmacological doses of vitamins C and E reduces reproductive fitness and impairs the ovarian and uterine functions of female mice. Theriogenology 2002b;57:1539-1550.
121. Tarin JJ, Gomez-Piquer V, Pertusa JF, Hermenegildo C, Cano A. Association of female aging with decreased parthenogenetic activation, raised MPF, and MAPKs activities and-reduced levels of glutathione S-transferases activity and thiols in mouse oocytes. Mol Reprod Dev 2004;69:402-410.
122. Tatone C, Carbone MC, Falone S, Aimola P, Giardinelli A, Caserta D, Marci R, Pandolfi A, Ragnelli AM, Amicarelli F. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod 2006a;12:655-660.
123. Tatone C, Carbone MC, Gallo R, Delle Monache S, Di Cola M, Alesse E, Amicarelli F. Age-associated changes in mouse oocytes during postovulatory in vitro culture: Possible role for meiotic kinases and survival factor BCL2. Biol Reprod 2006b;74:395-402.
124. Tatone C, Carbone MC, Di Cola M, Marci R, Amicarelli F. Possible role of carbonyl stress in ovarian aging. Hum Reprod 2007;22:i75.
125. Tempfer CB, Riener EK, Keck C, Grimm C, Heinze G, Huber JC, Gitsch G, Hefler LA. Polymorphisms associated with thrombophilia and vascular homeostasis and the timing of menarche and menopause in 728 white women. Menopause 2005;12:325-330.
126. te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update 2002;8:141-154.
127. Thomas DR. Vitamins in health and aging. Clin Geriatr Med 2004; 20: 259-274.
128. Thouas GA, Trounson AO, Jones GM. Effect of female age on mouse oocyte developmental competence following mitochondrial injury. Biol Reprod 2005;73:366-373.
129. Tilly JL, Kowalski KI, Johnson AL, Hsueh AJ. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 1991;129:2799-2801.
130. Tilty JL. Commuting the death sentence: How oocytes strive to survive. Nat Rev Mol Cell Biol 2001;2:838-848.
131. van Asselt KM, Kok HS, Peeters PH, Roest M, Pearson PL, te Velde ER, Grobbee DE, van der Schouw YT. Factor V Leiden mutation accelerates the onset of natural menopause. Menopause 2003;10:477-481.
132. 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;3:3-11.
133. Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogeresis: Engines of metabolism, ionic regulation and developmental competence. Reproduction 2004;128:269-280.
134. 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 1047-1055.
135. Van Blerkom J, Sinclair J, Davis P. Mitochondrial transfer between oocytes: Potential applications of mitochondrial donation and the issue of heteroplasmy, Hum Reprod 1998;13:2857-2868.
136. Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FP, Baynes JW, TeKoppele JM. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 2000;275:39027-39031.
137. Vilim V, Wilhelm J. What do we measure by a luminol-dependent chemiluminescence of phagocytes? Free Radic Biol Med 1989;6 623-629.
138. Visser JA, de Jong FH, Laven JS, Themmen AP. Anti-Mullerian hormone: A new marker for ovarian function. Reproduction 2006;131:1-9.
139. Voss P, Siems W. Clinical oxidation parameters of aging. Free Rad Res 2006;40:1339-1349.
140. Wang GL, Jiang BH, Semenza GL. Effect of altered redox states on expression and DNA-binding activity of hypoxia-inducible factor 1. Biochem Biophys Res Commun 1995;212:550-556.
141. Wang TH, Chang CL, Wu HM, Chiu YM, Chen CK, Wang HS. Insulin-like growth factor-II (IGF-II), IGF-binding protein-3 (IGFBP-3), and IGFBP-4 in follicular fluid are associated with oocyte maturation and embryo development. Fertil Steril 2006;86:1392-1401.
142. Wardman P. Fluorescent and luminesccnt probes for measurement of oxidative and nitrosative speciess in cells and tissues: Progress, pitfalls, and proscpects. Free Rad Biol Med 2007 (in press).
143. Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003;13:1596-1608.
144. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 2001;280 E685-E694.
145. Wei YH, Lee HC. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med (Maywood) 2002;227:671-682.
146. Wen Y, Skidmore JC, Porter-Turner MM, Rea CA, Khokher MA, Singh BM. Relationship of glycation; antioxidant status and oxidative stress to vascular endothelial damage in diabetes. Diabetes Obes Metab 2002;4:305-308.
147. Westergaard CG, Byskov AG, Anderaen CY. Morphometric characteristics of the primordial to primary follicle transition in the human ovary in relation to age. Hum Reprod 2007;22:2225-2231.
148. Wiener-Megnazi Z, Vardi L, Lissak A, Shniser S, Reznick AZ, Ishai D, Lahav-Baratz S, Shilo H, Koifman M, Dirnfeld M. Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilizaton. Fertil Steril 2004;82(Suppl 3):117-1176.
149. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 2001;16:909-917.
150. Wood JW, Fecundity and natural fertility in humans. Oxf Rey Reprod Biol. 1989;11:61-109.
151. Wright VC, Chang J, Jeng G, Macaluso M. Assisted reproductive techology surveillance - United States, 2003. MMWR Surveill Summ. 2006;55 1-22.
152. Wu YT, Tang L, Cai J Lu XE, Xu J, Zhu XM, Luo Q, Huang HF. High bone morphogenetic protein-15 level in follicular fluid is associated with high quality ooeyte and subsequent embryonic development. Hum Reprod 2007;22:1526-1531.
153. Yanaihara A, Mitsukawa K, Iwasaki S, Otsuki K, Kawamura T, Okai T. High concentrations of lactoferrin in the follicular fluid correlate with embryo quality during in vitro fertilization cycles. Fertil Steril 2007;87:279:-282.
154. Yin D, Brunk UF. Carbonyl toxification hypothesis of biological aging. In: Maciera-Coelho A (ed). Molecular Basis of Aging. New York: CRC Press, Inc, New York 1995, 421-436.
155. Yin D, Chen K. The essential mechanisms of aging: Irreparable damage accumulation of biochemical side-reactions. Exp Gerontol 2003; 40:455-465.
156. Yin MB, Yin HS, Lee C, Kang SO, Chock PB. Protein glyeation: Creation of catalytic sites for free radical generation. Ann N Y Acad Sci 2001;928:48-53.
157. Zhang X, Wd XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res 2006;160:841-850.