Apoptosis in the ovary: Molecular mechanisms

Human Reproduction Update

Volumn 11, Issue 2, 2005, Pages 161-177

  Hussein, Mahmoud R ^a  

^a Assiut University   (Egypt)

Author keywords

Apoptosis; Death; Ovary

Indexed keywords

ACTIVIN; ALPHA6 INTEGRIN; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BETA INTEGRIN; CASPASE; ENDOTHELIN; FAS ANTIGEN; FAS LIGAND; GONADOTROPIN; GRANZYME B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBIN; INTEGRIN; INTERFERON; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN P53; PROTEINASE ACTIVATED RECEPTOR 4; SURVIVIN; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; APAF1 PROTEIN, HUMAN; INHIBIN A; PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; CELL DEATH; CELL LOSS; CELL SELECTION; FEMALE; HUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; REVIEW; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRION; OVARY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT;

ACTIVINS; ANIMALS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CASPASES; ENDOTHELINS; FEMALE; FOLLICULAR ATRESIA; HUMANS; INHIBINS; INTEGRINS; INTERFERONS; MITOCHONDRIA; OVARIAN FOLLICLE; OVARY; PREGNANCY; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 21244480038     PISSN: 13554786     EISSN: None     Source Type: Journal    
DOI: 10.1093/humupd/dmi001     Document Type: Review

References (143)

1. Abir R, Orvieto R, Dicker D, Zukerman Z, Barnett M and Fisch B (2002) Preliminary studies on apoptosis in human fetal ovaries. Fertil Steril 78, 259-264.
2. Amsterdam A, Keren-Tal I and Aharoni D (1996) Cross-talk between cAMP and p53-generated signals in induction of differentiation and apoptosis in steroidogenic granulosa cells. Steroids 61,252-256.
3. Amsterdam A, Dantes A, Hosokawa K, Schere-Levy CP, Kotsuji F and Aharoni D (1998) Steroid regulation during apoptosis of ovarian follicular cells. Steroids 63,314-318.
4. Amsterdam A, Keren-Tal I, Aharoni D, Dantes A, Land-Bracha A, Rimon E, Sasson R and Hirsh L (2003a) Steroidogenesis and apoptosis in the mammalian ovary. Steroids 68,861-867.
5. Amsterdam A, Sasson R, Keren-Tal L, Aharoni D, Dantes A, Rimon E, Land A, Cohen T, Dor Y and Hirsh L (2003b) Alternative pathways of ovarian apoptosis: death for life. Biochem Pharmacol 66,1355-1362.
6. Arch RH and Thompson CB (1998) 4-1BB and Ox4O are members of a tumor necrosis factor (TNF)-nerve growth factor receptor subfamily that bind TNF receptor-associated factors and activate nuclear factor kappaB. Mol Cell Biol 18,558-565.
7. Ashkenazi A and Dixit VM (1999) Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11,255-260.
8. Asselin E, Wang Y and Tsang BK (2001) X-linked inhibitor of apoptosis protein activates the phosphatidylinositol 3-kinase/Akt pathway in rat granulosa cells during follicular development. Endocrinology 142, 2451-2457.
9. Bakker TR, Reed D, Renno T and Jongeneel CV (1999) Efficient adenoviral transfer of NF-kappaB inhibitor sensitizes melanoma to tumor necrosis factor-mediated apoptosis. Int J Cancer 80,320-323.
10. Billiar RB, Zachos NC, Burch MG, Albrecht ED and Pepe GJ (2003) Up-regulation of alpha-inhibin expression in the fetal ovary of estrogen-suppressed baboons is associated with impaired fetal ovarian folliculogenesis. Biol Reprod 68,1989-1996.
11. Bladergroen BA, Strik MC, Bovenschen N, van Berkum O, Scheffer GL, Meijer CJ, Hack CE and Kummer JA (2001) The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J Immunol 166,3218-3225.
12. Bobe J and Goetz FW (2001) Molecular cloning and expression of a TNF receptor and two TNF ligands in the fish ovary. Comp Biochem Physiol B Biochem Mol Biol 129,475-481.
13. Boghaert ER, Sells SF, Walid AJ, Malone P, Williams NM, Weinstein MH, Strange R and Rangnekar VM (1997) Immunohistochemical analysis of the proapoptotic protein Par-4 in normal rat tissues. Cell Growth Differ 8,881-890.
14. Boone DL and Tsang BK (1998) Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol Reprod 58, 1533-1539.
15. Boyd JM, Gallo GJ, Elangovan B, Houghton AB, Malstrom S, Avery BJ, Ebb RG, Subramanian T, Chittenden T and Lutz RJ (1995) Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11,1921-1928.
16. Bridgham JT and Johnson AL (2001) Expression and regulation of Fas antigen and tumor necrosis factor receptor type I in hen granulosa cells. Biol Reprod 65,733-739.
17. Bridgham JT and Johnson AL (2002) Avian TVB (DR5-like) death receptor expression in hen ovarian follicles. Biochem Biophys Res Commun 291, 226-232.
18. Bristol SK and Woodruff TK (2004) Follicle-restricted compartmentalization of transforming growth factor beta superfarmly ligands in the feline ovary. Biol Reprod 70,846-859.
19. Chan WY, Cheung KK, Schorge JO, Huang LW, Welch WR, Bell DA, Berkowitz RS and Mok SC (2000) Bcl-2 and p53 protein expression, apoptosis, and p53 mutation in human epithelial ovarian cancers. Am J Pathol 156,409-417.
20. Chawla-Sarkar M, Leaman DW and Borden EC (2001) Preferential induction of apoptosis by interferon (IFN)-beta compared with IFN-alpha2: correlation with TRAIL/Apo2L induction in melanoma cell lines. Clin Cancer Res 7,1821-1831.
21. Christopher B (2000) Immunolocalization of transforming growth factor-betal during follicular development and atresia in the mouse ovary. Endocr J 47,475-480.
22. De Felici M (2000) Regulation of primordial germ cell development in the mouse. Int J Dev Biol 44,575-580.
23. De Pol A, Marzona L, Vaccina F, Negro R, Sena P and Forabosco A (1998) Apoptosis in different stages of human oogenesis. Anticancer Res 18, 3457-3461.
24. Degli-Esposti MA, Dougall WC, Smolak PL Waugh JY, Smith CA and Goodwin RG (1997a) The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity 7,813-820.
25. Degli-Esposti MA, Smolak PJ, Walczak H, Waugh J, Huang CP, DuBose RF, Goodwin RG and Smith CA (1997b) Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J Exp Med 186,1165-1170.
26. Deveraux QL and Reed JC (1999) IAP family proteins - suppressors of apoptosis. Genes Dev 13,239-252.
27. Deveraux QL, Stennicke HR, Salvesen GS and Reed JC (1999) Endogenous inhibitors of caspases. J Clin Immunol 19,388-398.
28. Devine PJ, Payne CM, McCuskey MK and Hoyer PB (2000) Ultrastructural evaluation of oocytes during atresia in rat ovarian follicles. Biol Reprod 63,1245-1252.
29. Driancourt MA, Fair T and Reynaud K (1998) [Oocyte apoptosis: when, how, why?]. Contracept Fertil Sex 26,522-527.
30. Driancourt MA, Reynaud K, Cortvrindt R and Smitz J (2000) Roles of KIT and KIT LIGAND in ovarian function. Rev Reprod 5,143-152.
31. Elvin JA, Yan C, Wang P, Nishimori K and Matzuk MM (1999) Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 13,1018-1034.
32. Erickson GF and Shimasaki S (2003) The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 1,9.
33. Erickson GF, Fuqua L and Shimasaki S (2004) Analysis of spatial and temporal expression patterns of bone morphogenetic protein family members in the rat uterus over the estrous cycle. J Endocrinol 182,203-217.
34. Felici MD, Carlo AD, Pesce M, Iona S, Farrace MG and Piacentini M (1999) Bcl-2 and Bax regulation of apoptosis in germ cells during prenatal oogenesis in the mouse embryo. Cell Death Differ 6,908-915.
35. Fenwick MA and Hurst PR (2002) Immunchistochemical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. Reproduction 124,659-665.
36. Flaws JA, Kugu K, Trbovich AM, DeSanti A, Tilly KI, Hirshfield AN and Tilly JL (1995) Interleukin-1 beta-converting enzyme-related proteases (IRPs) and mammalian cell death: dissociation of IRP-induced oligonucleosomal endonuclease activity from morphological apoptosis in granulosa cells of the ovarian follicle. Endocrinology 136,5042-5053.
37. Fortune JE, Cushman RA, Wahl CM and Kito S (2000) The primordial to primary follicle transition. Mol Cell Endocrinol 163,53-60.
38. Franco AV, Zhang XD, Van Berkel E, Sanders JE, Zhang XY, Thomas WD, Nguyen T and Hersey P (2001) The role of NF-kappa B in TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of melanoma cells. J Immunol 166,5337-5345.
39. Fulda S, Sieverts H, Friesen C, Herr I and Debatin KM (1997) The CD95 (APO-1/Fas) system mediates drug-induced apoptosis in neuroblastoma. cells. Cancer Res 57,3823-3829.
40. Furger C, Zorn JR and Ferre F (1995) Endothelins inhibit FSH-mediated function via ETA receptors in cultured human granulosa-lutein cells. Early Pregn 1,188-195.
41. Gaytan F, Morales C, Bellido C and Sanchez-Criado JE (2002) Selective apoptosis of lineal endothelial cells in dexamethasone-treated rats leads to ischemic necrosis of luteal tissue. Biol Reprod 66,232-240.
42. Gebauer G, Peter AT, Onesime D and Dhanasekaran N (1999) Apoptosis of ovarian granulosa cells: correlation with the reduced activity of ERK-signaling module. J Cell Biochem 75,547-554.
43. Giebel J and Rune GM (1997) Relationship between expression of integrins and granulosa cell apoptosis in ovarian follicles of the marmoset (Callithrix jacchus). Tissue Cell 29,525-531.
44. Giebel J, de Souza P and Rune GM (1996) Expression of integrins in marmoset (Callithrix jacchus) ovary during folliculogenesis. Tissue Cell 28,379-385.
45. Giebel J, Hegele-Hartung C and Rune GM (1997) Proliferation and apoptosis in follicles of the marmoset monkey (Callithrix jacchus) ovary. Anat Anz 179,413-419.
46. Gougeon A (1994) [Inhibin, activin, follistatin, and transforming growth factor beta (TGF-beta) presence in the ovary and possible role in the regulation of folliculogenesis in primates]. Contracept Fertil Sex 22, 571-576.
47. Gougeon A (1996) Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 17,121-155.
48. Gougeon A and Busso D (2000) Morphologic and functional determinants of primordial and primary follicles in the monkey ovary. Mol Cell Endocrinol 163,33-42.
49. Haapajarvi T, Pitkanen K and Laiho M (1999) Human melanoma cell line UV responses show independency of p53 function. Cell Growth Differ 10,163-171.
50. Hakuno N, Koji T, Yano T, Kobayashi N, Tsutsumi O, Taketani Y and Nakane PK (1996) Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. Endocrinology 137,1938-1948.
51. Heikinheimo M, Ermolaeva M, Bielinska M, Rahman NA, Narita N, Huhtaniemi IT, Tapanainen JS and Wilson DB (1997) Expression and hormonal regulation of transcription factors GATA-4 and GATA-6 in the mouse ovary. Endocrinology 138,3505-3514.
52. Honda T, Fujiwara H, Ueda M, Maeda M and Mori T (1995) Integrin alpha 6 is a differentiation antigen of human granulosa cells. J Clin Endocrinol Metab 80,2899-2905.
53. Hosokawa K, Aharoni D, Dantes A, Shaulian E, Schere-Levy C, Atzmon R, Kotsuji F, Oren M, Vlodavsky I and Amsterdam A (1998) Modulation of Mdm2 expression and p53-induced apoptosis in immortalized human ovarian granulosa cells. Endocrinology 139,4688-4700.
54. Hsu SY, Lai RJ, Finegold M and Hsueh AJ (1996) Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 137,4837-4843.
55. Hsu SY, Kaipia A, McGee E, Lomeli M and Hsueh AJ (1997) Bok is a proapoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective anti-apoptotic Bcl-2 family members. Proc Natl Acad Sci USA 94,12401-12406.
56. Hsu SY, Lin P and Hsueh AJ (1998) BOD (Bcl-2-related ovarian death gene) is an ovarian BH3 domain-containing proapoptotic Bcl-2 protein capable of dimerization with diverse antiapoptotic Bcl-2 members. Mol Endocrinol 12,1432-1440.
57. Hsueh AJ, Eisenhauer K, Chun SY, Hsu SY and Billig H (1996) Gonadal cell apoptosis. Recent Prog Horm Res, 433-455, discussion 455-456.
58. Hu CL, Cowan RG, Harman RM, Porter DA and Quirk SM (2001) Apoptosis of bovine granulosa cells after serum withdrawal is mediated by Fas antigen (CD95) and Fas ligand. Biol Reprod 64,518-526.
59. Hughes FM, Jr and Gorospe WC (1991) Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129, 2415-2422.
60. Hussein MR, Haemel AK and Wood GS (2003a) Apoptosis and melanoma: molecular mechanisms. J Pathol 199,275-288.
61. Hussein MR, Haemel AK and Wood GS (2003b) p53-related pathways and the molecular pathogenesis of melanoma. Eur J Cancer Prev 12, 93-100.
62. Inoue N, Manabe N, Matsui T, Maeda A, Nakagawa S, Wada S and Miyamoto H (2003) Roles of tumor necrosis factor-related apoptosis-inducing ligand signaling pathway in granulosa cell apoptosis during atresia in pig ovaries. J Reprod Dev 49,313-321.
63. Ivanov VN, Kehrl JH and Ronai Z (2000) Role of TRAF2/GCK in melanoma sensitivity to UV-induced apoptosis. Oncogene 19,933-942.
64. Iwai M, Hasegawa M, Taii S, Sagawa N, Nakao K, Imura H, Nakanishi S and Mori T (1991) Endothelins inhibit luteinization of cultured porcine granulosa cells. Endocrinology 129,1909-1914.
65. Jiang MR, Li YC, Yang Y and Wu JR (2003) c-Myc degradation induced by DNA damage results in apoptosis of CHO cells. Oncogene 22, 3252-3259.
66. Johnson AL and Bridgham JT (2002) Caspase-mediated apoptosis in the vertebrate ovary. Reproduction 124,19-27.
67. Johnson NC, Dan HC, Cheng JQ and Kruk PA (2004) BRCAl 185delAG mutation inhibits Akt-dependent, IAP-mediated caspase 3 inactivation in human ovarian surface epithelial cells. Exp Cell Res 298,9-16.
68. Kaipia A, Hsu SY and Hsueh AJ (1997) Expression and function of a proapoptotic Bcl-2 family member Bcl-XL/Bcl-2-associated death promoter (BAD) in rat ovary. Endocrinology 138,5497-5504.
69. Kerr JF, Wyllie AH and Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26,239-257.
70. Kim JM, Yoon YD and Tsang BK (1999) Involvement of the Fas/Fas ligand system in p53-mediated granulosa cell apoptosis during follicular development and atresia. Endocrinology 140,2307-2317.
71. Kiso M, Manabe N, Komatsu K, Shimabe M and Miyamoto H (2003) Abnormal structural luteolysis in ovaries of the senescence accelerated mouse (SAM) expression of Fas ligand/Fas-mediated apoptosis signaling molecules in luteal cells. J Reprod Dev 49,457-463.
72. Komatsu K, Manabe N, Kiso M, Shimabe M and Miyamoto H (2003) Soluble Fas (FasB) regulates luteal cell apoptosis during luteolysis in murine ovaries. Mol Reprod Dev 65,345-352.
73. Kugu K, Ratts VS, Piquette GN, Tilly KI, Tao XJ, Martimbeau S, Aberdeen GW, Krajewski S, Reed JC, Pepe GJ, Albrecht ED and Tilly JL (1998) Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 5,67-76.
74. Kuranaga E, Kanuka H, Bannai M, Suzuki M, Nishihara M and Takahashi M (1999) Fas/Fas ligand system in prolactin-induced apoptosis in rat corpus luteum: possible role of luteal immune cells. Biochem Biophys Res Commun 260,167-173.
75. Laitinen MP, Anttonen M, Ketola I, Wilson DB, Ritvos O, Butzow R and Heikinheimo M (2000) Transcription factors GATA-4 and GATA-6 and a GATA family cofactor, FOG-2, are expressed in human ovary and sex cord-derived ovarian tumors. J Clin Endocrinol Metab 85, 3476-3483.
76. Leo CP, Hsu SY, Chun SY, Bae HW and Hsueh AJ (1999) Characterization of the antiapoptotic Bcl-2 family member myeloid cell leukemia-1 (Mel-1) and the stimulation of its message by gonadotropins in the rat ovary. Endocrinology 140,5469-5477.
77. Leung PC, Cheng CK and Zhu XM (2003) Multi-factorial role of GnRH-I and GnRH-II in the human ovary. Mol Cell Endocrinol 202,145-153.
78. Li A, Yang H, Wang F, Wei C and Kang J (1999) [The expression of IGF-I, TGF beta and Fas-L in granulosa cells of ovarian follicle with relation to the onset of atresia in rats]. Hua Xi Yi Ke Da Xue Xue Bao 30,158-161.
79. Li J, Kim JM, Liston P, Li M, Miyazaki T, Mackenzie AE, Korneluk RG and Tsang BK (1998) Expression of inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia. Endocrinology 139,1321-1328.
80. Li YZ, Li CJ, Pinto AV and Pardee AB (1999) Release of mitochondrial cytochrome C in both apoptosis and necrosis induced by beta-lapachone in human carcinoma cells. Mol Med 5,232-239.
81. Luo J, Xiao J, Tao Z and Li X (1997) Detection of c-myc gene expression in nasopharyngeal carcinoma by nonradioactive in situ hybridization and immunohistochemistry. Chin Med J (Engl) 110,229-232.
82. Malinin NL, Boldin MP, Kovalenko AV and Wallach D (1997) MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1 Nature 385,540-544.
83. Marone M, Scambia G, Mozzetti S, Ferrandina G, Iacovella S, De Pasqua A, Benedetti-Panici P and Mancuso S (1998) bcl-2, bax, bcl-XL, and bcl-XS expression in normal and neoplastic ovarian tissues. Clin Cancer Res 4,517-524.
84. Matsumoto K, Nakayama T, Sakai H, Tanemura K, Osuga H, Sato E and Ikeda JE (1999) Neuronal apoptosis inhibitory protein (NAIP) may enhance the survival of granulosa cells thus indirectly affecting oocyte survival. Mol Reprod Dev 54,103-111.
85. McCracken JA, Custer EE and Lamsa JC (1999) Luteolysis: a neuroendocrine-mediated event. Physiol Rev 79,263-323.
86. McGee EA and Hsueh AJ (2000) Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21,200-214.
87. Miceli F, Minici F, Garcia Pardo M, Navarra P, Proto C, Mancuso S, Lanzone A and Apa R (2001) Endothelins enhance prostaglandin (PGE(2) and PGF(2alpha)) biosynthesis and release by human luteal cells: evidence of a new paracrine/autocrine regulation of luteal function. J Clin Endocrinol Metab 86,811-817.
88. Miyazono K (2000) [Transforming growth factor-beta signaling and cancer]. Hum Cell 13,97-101.
89. Monniaux D (2002) [Oocyte apoptosis and evolution of ovarian reserve]. Gynecol Obstet Fertil 30,822-826.
90. Morita Y and Tilly JL (1999) Oocyte apoptosis: like sand through an hour-glass. Dev Biol 213,1-17.
91. Murphy CR, Sabel JL, Sandler AD and Dagle JM (2002) Survivin mRNA is down-regulated during early Xenopus laevis embryogenesis. Dev Dyn 225,597-601.
92. Nakayama H, Kajikawa S, Shinozuka J, Su WP and Doi K (1999) Possible involvement of DNA methylation in 5-azacytidine-induced neuronal cell apoptosis. Histol Histopathol 14,143-150.
93. Nandedkar TD and Dharma SJ (2001) Expression of bcl(xs) and c-myc in atretic follicles of mouse ovary. Reprod Biomed Online 3,221-225.
94. Nguyen T, Thomas W, Zhang XD, Gray C and Hersey P (2000) Immunologically-mediated tumour cell apoptosis: the role of TRAIL in T cell and cytokine-mediated responses to melanoma. Forum (Genova) 10, 243-252.
95. Nilsson EE and Skinner MK (2003) Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 69,1265-1272.
96. Orlicky DJ, Fisher L, Dunscomb N and Miller GJ (1992) Immunohistochemical localization of PGF2 alpha receptor in the rat ovary. Prostaglandins Leukot Essent Fatty Acids 46,223-229.
97. Otani H, Yamoto M, Fujinaga H and Nakano R (1996) Presence and localization of endothelin receptor in the rat ovary and its regulation by pituitary gonadotropins. Eur J Endocrinol 135,449-454.
98. Paredes A, Romero C, Dissen GA, DeChiara TM, Reichardt L, Cornea A, Ojeda SR and Xu B (2004) TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. Dev Biol 267, 430-449.
99. Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ and Tilly JL (1999) Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet 21,200-203.
100. Perez GI, Maravei DV, Trbovich AM, Cidlowski JA, Tilly JL and Hughes FM, Jr (2000) Identification of potassium-dependent and -independent components of the apoptotic machinery in mouse ovarian germ cells and granulosa cells. Biol Reprod 63,1358-1369.
101. Peter AT and Dhanasekaran N (2003) Apoptosis of granulosa cells: a review on the role of MAPK-signalling modules. Reprod Domest Anim 38,209-213.
102. Piek E and Roberts AB (2001) Suppressor and oncogenic roles of transforming growth factor-beta and its signaling pathways in tumorigenesis. Adv Cancer Res 83,1-54.
103. Pombo CM, Kehrl JH, Sanchez I, Katz P, Avruch J, Zon LI, Woodgett JR, Force T and Kyriakis JM (1995) Activation of the SAPK pathway by the human STE20 bomologue germinal centre kinase. Nature 377,750-754.
104. Porter SB (1997) Current status of clinical trials with anti-TNF. Chest 112,339S-341S.
105. Raisova M, Bektas M, Wieder T, Daniel P, Eberle J, Orfanos CE and Geilen CC (2000) Resistance to CD95/Fas-induced and ceramide-mediated apoptosis of human melanoma cells is caused by a defective mitochondrial cytochrome c release. FEBS Lett 473,27-32.
106. Rajkovic A, Pangas SA, Ballow D, Suzumori N and Matzuk MM (2004) NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305,1157-1159.
107. Ratts VS, Flaws JA, Kolp R, Sorenson CM and Tilly JL (1995) Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 136,3665-3668.
108. Robles R, Tao XJ, Trbovich AM, Maravel DV, Nahum R, Perez GI, Tilly KI and Tilly JL (1999) Localization, regulation and possible consequences of apoptotic protease-activating factor-1 (Apaf-1) expression in granulosa cells of the mouse ovary. Endocrinology 140,2641-2644.
109. Robles R, Morita Y, Mann KK, Perez GI, Yang S, Matikainen T, Sherr DH and Tilly JL (2000) The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology 141,450-453.
110. Sato T, Irie S, Krajewski S and Reed JC (1994) Cloning and sequencing of a cDNA encoding the rat Bcl-2 protein. Gene 140,291-292.
111. Sauerwald TM, Betenbaugh MJ and Oyler GA (2002) Inhibiting apoptosis in mammalian cell culture using the caspase inhibitor XIAP and deletion mutants. Biotechnol Bioeng 77,704-716.
112. Schams D, Berisha B, Neuvians T, Amselgruber W and Kraetzl WD (2003) Real-time changes of the local vasoactive peptide systems (angiotensin, endothelin) in the bovine corpus luteum after induced luteal regression. Mol Reprod Dev 65,57-66.
113. Song Q, Kuang Y, Dixit VM and Vincenz C (1999) Boo, a novel negative regulator of cell death, interacts with Apaf-1. Embo J 18,167-178.
114. Sugino N, Suzuki T, Kashida S, Karube A, Takiguchi S and Kato H (2000) Expression of Bcl-2 and Bax in the human corpus luteum during the menstrual cycle and in early pregnancy: regulation by human chorionic gonadotropin. J Clin Endocrinol Metab 85,4379-4386.
115. Suh CS, Sonntag B and Erickson GF (2002) The ovarian life cycle: a contemporary view. Rev Endocr Metab Disord 3,5-12.
116. Suzumori N, Yan C, Matzuk MM and Rajkovic A (2002) Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes. Mech Dev 111,137-141.
117. Symonds D, Tomic D, Borgeest C, McGee E and Flaws JA (2003) Smad 3 regulates proliferation of the mouse ovarian surface epithelium. Anat Rec 273A,681-686.
118. Thompson WE, Powell JM, Whittaker JA, Sridaran R and Thomas KH (1999) Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Anat Rec 256,40-48.
119. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE and Thomas K (2001) Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 142, 4076-4085.
120. Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im GS, Prather RS, Isom SC, Rucker E 3rd and Tsang BK (2004) Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biol Reprod 71,282-290.
121. Tilly JL (1996) The molecular basis of ovarian cell death during germ cell attrition, follicular atresia, and luteolysis. Front Biosci 1,d1-11.
122. Tilly JL (1997) Apoptosis and the ovary: a fashionable trend or food for thought? Fertil Steril 67,226-228.
123. Tilly JL (2001) Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2,838-848.
124. Tilly JL, Kowalski KI, Johnson AL and Hsueh AJ (1991) Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129,2799-2801.
125. Tilly JL, Kowalski KI, Schomberg DW and Hsueh AJ (1992) Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 131,1670-1676.
126. Tilly JL, Tilly KI, Kenton ML and Johnson AL (1995) Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. Endocrinology 136,232-241.
127. Tomic D, Brodie SG, Deng C, Hickey RJ, Babus JK, Malkas LH and Flaws JA (2002) Smad 3 may regulate follicular growth in the mouse ovary. Biol Reprod 66,917-923.
128. Van Nassauw L, Tao L and Harrisson F (1999) Distribution of apoptosis-related proteins in the quail ovary during folliculogenesis: BCL-2, BAX and CPP32. Acta Histochem 101,103-112.
129. Vaskivuo TE and Tapanainen JS (2003) Apoptosis in the human ovary. Reprod Biomed Online 6,24-35.
130. Vaskivuo TE, Anttonen M, Herva R, Billig H, Dorland M, te Velde ER, Stenback F, Heikinheimo M and Tapanainen JS (2001) Survival of human ovarian follicles from fetal to adult life: apoptosis, apoptosis-related proteins, and transcription factor GATA-4. J Clin Endocrinol Metab 86,3421-3429.
131. Viger RS, Mertineit C, Trasler JM and Nemer M (1998) Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Mullerian inhibiting substance promoter. Development 125,2665-2675.
132. Wada M, Armae S, Sasaki H, Ishii T, Sano N, Nio M, Hayashi Y and Ohi R (2003) The functional roles of porcine CD80 molecule and its ability to stimulate and regulate human anti-pig cellular response. Transplantation 75,1887-1894.
133. Wandji SA, Wood TL, Crawford J, Levison SW and Hammond JM (1998) Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology 139, 5205-5214.
134. Wang Y, Asselin E and Tsang BK (2002) Involvement of transforming growth factor alpha in the regulation of rat ovarian X-linked inhibitor of apoptosis protein expression and follicular growth by follicle-stimulating hormone. Biol Reprod 66,1672-1680.
135. Wang Z, Tamura K, Yoshie M, Tamura H, Imakawa K and Kogo H (2003) Prostaglandin F2alpha-induced functional regression of the corpus luteum and apoptosis in rodents. J Pharmacol Sci 92,19-27.
136. Wieser R (2001) The transforming growth factor-beta signaling pathway in tumorigenesis. Curr Opin Oncol 13,70-77.
137. Wyllie AH (1993) Apoptosis (the 1992 Frank Rose Memorial Lecture). Br J Cancer 67,205-208.
138. Xiao CW, Ash K and Tsang BK (2001) Nuclear factor-kappaB-mediated X-linked inhibitor of apoptosis protein expression prevents rat granulosa cells from tumor necrosis factor alpha-induced apoptosis. Endocrinology 142,557-563.
139. Yoon HJ and Carbon J (1999) Participation of Bir1p, a member of the inhibitor of apoptosis family, in yeast chromosome segregation events. Proc Natl Acad Sci USA 96,13208-13213.
140. Young CY, Murtha PE and Zhang J (1994) Tumor-promoting phorbol ester-induced cell death and gene expression in a human prostate adenocarcinoma cell line. Oncol Res 6,203-210.
141. Young FM, Illingworth PJ and Fraser HM (1998) Ubiquitin and apoptosis in the corpus luteum of the marmoset monkey (Callithrix jacchus). J Reprod Fertil 114,163-168.
142. Young TW, Mei FC, Yang G, Thompson-Lanza JA, Liu J and Cheng X (2004) Activation of antioxidant pathways in ras-mediated oncogenic transformation of human surface ovarian epithelial cells revealed by functional proteomics and mass spectrometry. Cancer Res 64,4577-4584.
143. Zwain IH and Amato P (2001) cAMP-induced apoptosis in granulosa cells is associated with up-regulation of P53 and bax and down-regulation of clusterin. Endocr Res 27,233-249.