Regulation of ovarian follicle atresia

Annual Review of Physiology

Volumn 59, Issue , 1997, Pages 349-363

  Kaipia, Antti ^a   Hsueh, Aaron J W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

apoptosis; follicle; gonadotropins; granulosa cell; ovary

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; DNA FRAGMENT; EPIDERMAL GROWTH FACTOR; ESTROGEN; FAS ANTIGEN; GONADOTROPIN; INTERLEUKIN 1BETA; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR ALPHA;

APOPTOSIS; ATRESIA; CELL DEATH; ETIOLOGY; GERM CELL; GRANULOSA CELL; HORMONAL REGULATION; OVARY; OVARY FOLLICLE; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; REVIEW;

EID: 0030934805     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.59.1.349     Document Type: Review

References (90)

1. Adashi EY, Resnick CE, D'Ercole AJ, Svoboda ME, Van Wyk JJ. 1985. Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocr. Rev. 6:400-20
2. Adashi EY, Resnick CE, Hernandez ER, Hurwitz A, Rosenfeld RG. 1990. Follicle-stimulating hormone inhibits the constitutive release of insulin-like growth factor binding proteins by cultured rat ovarian granulosa cells. Endocrinology 126:1305-7
3. Alnemri, ES, Robertson NM, Fernandes TF, Croce CM, Litwack G. 1992. Overexpressed full-length human bcl-2 extends the survival of baculovirus-infected Sf9 insect cells. Proc. Natl. Acad. Sci. USA 89:7295-99
4. Ankarcrona M, Dypbukt JM, Brune B, Nicotera P. 1994. Interleukin-1β-induced nitric oxide production activates apoptosis in pancreatic RINm5F cells. Exp. Cell. Res. 213:172-77
5. Baker TG. 1963. A quantitative and cytological study of germ cells in the human ovaries. Proc. R. Soc. London, Ser. B 158:417-33
6. Beaumont HM, Mandl AM. 1962. A quantitative and cytological study of oogonia and oocytes in the foetal and neonatal rat. Proc. R. Soc. London Ser. B 155:557-79
7. Benedetti, A, Jezequel AM, Orlandi F. 1988. A quantitative evaluation of apoptotic bodies in rat liver. Liver 8:172-77
8. G-monomethyl-L-arginine. FEBS Lett. 299:102-6
9. Billig H, Furuta I, Hsueh AJW. 1994. Gonadotropin releasing hormone (GnRH) directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of DNA fragmentation in granulosa cells. Endocrinology 134:245-52
10. Billig H, Furuta I, Hsueh AJW. 1993. Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133:2204-12
11. Billig H, Furuta I, Rivier C, Tapanainen J, Parvinen M, et al. 1995. Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136:5-12
12. Boldin MP, Varfolomeev EE, Pancer Z, Met IL, Camonis JH, et al. 1995. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 270:7795-98
13. Boone DL, Yan W, Tsang BK. 1995. Identification of a deoxyribonuclease I-like endonuclease in rat granulosa and luteal cell nuclei. Biol. Reprod. 53:1057-65
14. Braw RH, BarAmi S, Tsafriri A. 1981. Effect of hypophysectomy on atresia of rat preovulatory follicles. Biol. Reprod. 25:989-96
15. Braw RH, Tsafriri A. 1980. Effects of PMSG on follicular atresia in the rat ovary. J. Reprod. Fertil. 59:267-72
16. Cain L, Chatterjee S, Colling TJ. 1995. In vitro folliculogenesis of rat preantral follicles. Endocrinology 136:3369-77
17. Carson RS, Findlay JK, Clarke IJ, Burger HG. 1981. Estradiol, testosterone, and androstenedione in ovine follicular fluid during growth and atresia of ovarian follicles. Biol. Reprod. 24:105-13
18. Chinnaiyan AM, O'Rourke K, Tewari M, Dixit VM. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81:505-12
19. Chun SY, Billig H, Tilly JL, Furuta I, Tsafriri A, et al. 1994. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous IGF-I. Endocrinology 135:1845-53
20. Chun SY, Eisenhauer KM, Kubo M, Hsueh AJW. 1995. Interleukin-1β suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 136:3120-27
21. Chun SY, Eisenhauer K, Minami S, Billig H, Perlas E, Hsueh AJW. 1996. Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinology 137: 1447-56
22. Clarke PGH. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181: 195-213
23. Davoren JB, Kasson BG, Li CH, Hsueh AJW. 1986. Specific insulin-like growth factor I and II binding sites on rat granulosa cells: relation to IGF action. Endocrinology 119:2155-62
24. Dolci S, Pesce MD, De Felici M. 1993. Combined action of stem cell factor, leukemia inhibitory factor, and cAMP on in vitro proliferation of mouse primordial germ cells. Mol. Reprod. Dev. 35:134-39
25. Driscoll M. 1992. Molecular genetics of cell death in the nematode Caenorhabditis elegans. J. Neurobiol. 23:1327-51
26. Eisenhauer K, Chun SY, Billig H, Hsueh AJW. 1995. Growth hormone suppression of apoptosis in preovulatory follicles and partial neutralization by insulin-like growth factor binding protein (IGFBP). Biol. Reprod. 53:13-20
27. Ellis RE, Yuan J, Horvitz HR. 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7:663-98
28. Flaws JA, DeSanti A, Tilly KI, Roya JO, Kugu K, et al. 1995. Vasoactive intestinal peptide-mediated suppression of apoptosis in the ovary: potential mechanisms of action and evidence of a conserved antiatretogenic role through evolution. Endocrinology 136:4351-59
29. Gorospe WC, Hughes FMJ, Spangelo BL. 1992 Interleukin-6: effects on and production by rat granulosa cells in vitro. Endocrinology 130:1750-52
30. Gougeon A. 1993. Dynamics of human follicular growth: a morphlogical perspective. In The Ovary, ed. EY Adashi, PCK Leung, pp. 21-31. New York: Raven
31. Gu Y, Sarnecki C, Aldape RA, Livingston DJ, Su MS. 1995. Cleavage of poly(ADP-ribose) polymerase by interleukin-1β converting enzyme and its homologs TX and Nedd2. J. Biol. Chem. 270:18715-18
32. Hakuno N, Koji T, Yano T, Kobayashi N, Tsutsumi O, et al. 1996. Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. Endocrinology 137:1938-48
33. Hay MF, Cran DG, Moor RM. 1976. Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res. 169:515-29
34. Hengartner MO, Ellis RE, Horvitz HR. 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356:494-99
35. Hengartner MO, Horvitz HR. 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76:665-76
36. Hirshfield AN. 1991. Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124:43-101
37. Hirshfield AN, Midgley ARJ. 1978. The role of FSH in the selection of large ovarian follicles in the rat. Biol. Reprod. 19:606-11
38. Hsu SY, Lai RJM, Chun SY, Hsueh AJW. 1996. Targeted overexpression of Bcl-2 in ovaries of transgenic mice decreases follicel apoptosis, increases litter size, and enhances tumorigenesis. Endocrinolog 137:4837-43
39. Hsu H, Xiong J, Goeddel DV. 1995. The TNF receptor I-associated protein TRADD signals cell death and NF-κB activation. Cell 81:495-504
40. Hsueh AJW, Billig H, Tsafriri A. 1994. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr. Rev. 15:1-18
41. Hsueh AJ, Jones PB. 1981. Extrapituitary actions of gonadotropin-releasing hormone. Endocr. Rev. 2:437-61
42. Hughes FMJ, Gorospe WC. 1991. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129:2415-22
43. Hutchinson LA, Findlay JK, Herington AC. 1988. Growth hormone and insulin-like growth factor-I accelerate PMSG-induced differentiation of granulosa cells. Mol. Cell. Endocrinol. 55:61-69
44. Jia XC, Kessel B, Yen SS, Tucker EM, Hsueh AJ. 1986. Serum bioactive follicle-stimulating hormone during the human menstrual cycle and in hyper- and hypogonadotropic states: application of a sensitive granulosa cell aromatase bioassay. J. Clin. Endocrinol. Metab. 62:1243-49
45. Jolly PD, Tisdall DJ, Heath DA, Lun S, McNatty KP. 1994. Apoptosis in bovine granulosa cells in relation to steroid synthesis, cAMP response to FSH and follicular atresia. Biol. Reprod. 51:934-44
46. Jones PB, Conn PM, Marian J, Hsueh AJ. 1980. Binding of gonadotropin releasing hormone agonist to rat ovarian granulosa cells. Life Sci. 27:2125-32
47. Kaipia A, Chun SY, Eisenhauer K, Hsueh AWJ. 1996. Tumor necrosis factor-α and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles. Endocrinology 137:4864-70
48. Kudlow JE, Kobrin MS, Purchio AF, Twardzik DR, Hernandez ER, et al. 1987. Ovarian transforming growth factor-α gene expression: immunohistochemical localization to the theca-interstitial cells. Endocrinology 121:1577-79
49. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirier GG, Earnshaw WC. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346-47
50. Leung PCK, Steele GL. 1992. Intracellular signaling in the gonads. Endocr. Rev. 13:476-98
51. Louvet JP, Harman SM, Ross GT. 1975. Effects of human interstitial cell stimulating hormone and human follicle-stimulating hormone on ovarian weights in estrogen-primed hypophysectomized immature male rats. Endocrinology 96:1179-86
52. Louvet JP, Harman SM, Schrieber JR, Ross GT. 1975. Evidence of a role of adrogens in follicular maturation. Endocrinology 97:366-72
53. Miura M, Zhu H, Rotello R, Hartwieg EA, Yuan J. 1993. Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75:653-60
54. Nagata S, Golstein P. 1995. The Fas death factor. Science 267:1449-56
55. Nayudu PL, Osborn M. 1992. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. J. Reprod. Fertil. 95:349-62
56. Neufeld G, Ferrara N, Schweigerer L, Mitchell R, Gospodarowicz D. 1987. Bovine granulosa cells produce basic fibroblast growth factor. Endocrinology 121:597-603
57. Obeid LM, Linardic CM, Karolak LA, Hannun YA. 1993. Programmed cell death induced by ceramide. Science 259:1769-71
58. Ohno S, Smith JB. 1964. Role of fetal follicular cells in meiosis of mammalian oocyte. Cytogenetics 3:324-33
59. Pedersen T, Peters H. 1968. Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17:555-57
60. Peters H, Byskov AG, Grinsted J. 1978. Follicular growth in fetal and prepubertal ovaries of human and other primates. In Gynecological Endocrinology, ed. GT Ross, Lipsett MB, pp. 469-85. London: Saunders
61. Peluso JJ, Pappalardo A. 1994. Progesterone and cell adhesion interact to regulate granulosa cell apoptosis. Biochem. Cell Biol. 72:547-51
62. Pesce M, Farrace MG, Piacentini M, Dolci S, De Felici M. 1993. Stem cell factor and leukemia inhibitory factor promote primordial germ cell survival by suppressing programmed cell death (apoptosis). Development 118:1089-94
63. Quirk SM, Cowan RG, Joshi SG, Henrikson KP. 1995. Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol. Reprod. 52:279-87
64. Raff MC. 1992. Social controls on cell survival and cell death. Nature 356:397-400
65. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, et al. 1993. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262:695-700
66. Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL. 1995. Ablation of bcl-2 gene expression decreases the number of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136:3665-68
67. Resnick JL, Bixler LS, Cheng L, Donovan PJ. 1992. Long-term proliferation of mouse primordial cells in culture. Nature 359:550-51
68. Santana P, Lianes L, Hernandez I, Gallardo G, Quintana J, et al. 1995. Ceramide mediates tumor necrosis factor effects on P450-aromatase activity in cultured granulosa cells. Endocrinology 136:2345-48
69. Sato T, Hanada M, Bodrug S, Irie S, Iwama N, et al. 1994. Interactions among members of the bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 91:9238-42
70. Schmidt HHHW, Walter U. 1994. NO at work. Cell 78:919-25
71. Schwartz NB. 1974. The role of FSH and LH and of their antibodies on follicular growth and on ovulation. Biol. Reprod. 10:236-76
72. Stanger BZ, Leder P, Lee TH, Kim E, Seed B. 1995. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 81:513-23
73. Tapanainen JS, Tilly JL, Vihko KK, Hsueh AJW. 1993. Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors. Mol. Endocrinol. 7:643-50
74. Tartaglia LA, Rothe M, Hu YF, Goeddel DV. 1993. Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor. Cell 73:213-16
75. Terranova PF. 1981. Steroidogenesis in experimentally induced atretic follicles of the hamster: a shift from estradiol to progesterone synthesis. Endocrinology 108:1885-90
76. Thompson CB. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-62
77. Tilly JL, Billig H, Kowalski KI, Hsueh AJW. 1992. Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat granulosa cells and follicles by a tyrosine kinase-dependent mechanism. Mol. Endocrinol. 6:1942-50
78. Tilly JL, Kowalski KI, Johnson AL, Hsueh AJW. 1991. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129:2799-801
79. Tilly JL, Kowalski KI, Schomberg DW, Hsueh AJW. 1992. Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger RNA transcripts for gonadotropin receptors and cytochrome p450 aromatase. Endocrinology 131:1670-76
80. Vaux DL, Weissman IL, Kim SK. 1992. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258:1955-57
81. Westergaard LG, Andersen CY. 1989. Epidermal growth factor (EGF) in human preovulatory follicles. Hum. Reprod. 4:257-60
82. Williams PC. 1940. Effect of stilbestrol on ovaries of hypophysectomized rats. Nature 145:388-89
83. Wyllie AH. 1987. Apoptosis: cell death in tissue regulation. J. Pathol. 153:313-16
84. Wyllie AH, Kerr JFR, Currie AR. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306
85. Wyllie AH, Kerr JFR, Macaskill IAM, Currie AR. 1973. Adrenocortical cell deletion: the role of ACTH. J. Pathol. 111:85-94
86. Yin X, Oltvai ZN, Korsmeyer SJ. 1994. BH1 and BH2 domains of bcl-2 are required for inhibition of apoptosis and heterodimerization with BAX. Nature 369:321-23
87. Yuan J, Horvitz HR. 1992. The Caenorhabditis elegans cell death gene ced4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 116:309-20
88. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75:641-52
89. Zeleznik AJ, Hillier SG, Ross GT. 1979. Follicle stimulating hormone-induced follicular development: an examination of the role of androgens. Biol. Reprod. 21:673-81
90. 2+-dependent endonuclease activity in rat granulosa and luteal cells. Endocrinology 125:2218-20