The genes of cell death and cellular susceptibility to apoptosis in the ovary: A hypothesis

Cell Death and Differentiation

Volumn 4, Issue 3, 1997, Pages 180-187

  Tilly, Jonathan L ^a   Tilly, Kim I ^a   Perez, Gloria I ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Apoptosis; Atresia; BaX; Bcl 2; Bcl x; Caspase; Granulosa cell; ICE; Oocyte; p53

Indexed keywords

GONADOTROPIN; GROWTH FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; FEMALE; FETUS DEVELOPMENT; FOLLITROPIN BLOOD LEVEL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TRANSFER; GERM CELL; GRANULOSA CELL; HUMAN; HUMAN CELL; MULTIGENE FAMILY; NONHUMAN; OOCYTE; OVARY CELL; OVULATION; PERINATAL PERIOD; PRIORITY JOURNAL; TUMOR CELL LINE;

ANIMALIA;

EID: 0030954023     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400238     Document Type: Article

References (90)

1. Abrahamson JLA, Lee JM and Bernstein A (1995) Regulation of p53-mediated apoptosis and cell cycle arrest by Steel factor. Mol Cell Biol 15: 6953 - 6960
2. Ainemri ES Livingston DJ, Nicholson DW, Salvesen G, Thomberry NA, Wong WW and Yuan J (1996) Human ICE/CED-3 protease nomenclature. Cell 87: 171
3. Arenas MJ, Morns RG and Wyllie AH (1990) Apoptosis. The role of the endonuclease. Am J Pathol 136: 593 - 608
4. Baker TG (1963) A quantitative and cytological study of germ cells in human ovaries. Proc Royal Soc London (B) 158: 417 - 433
5. Beaumont HM and Mandl AM (1961) A quantitative and cytological study of oogonia and oocytes in the foetal and neonatal rat Proc Royal Soc London (B) 155: 557 - 579
6. Besmer P, Manova K, Duttlinger R, Huang EJ, Packer A, Gyssler C and Bacharova RF (1993) The kit-ligand (steel factor) and its receptor c-kit/W: pleiotropic roles in gametogenesis and melariogenesis Development (Supplement) 125 - 137
7. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nuñez G and Thompson CB (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 4: 597 - 608
8. Borum K (1961) Oogenests in the mouse: a study of the meiotic prophase, Exp Cell Res 24: 495 - 507
9. Braw RH, Bar-Ami S and Tsafriri A (1981) Effect of hypophysectomy on atresia of rat preovulatory follicles Biof Reprod 25: 989 - 996
10. Byskov, AGS (1974) Cell kinetic studies of follicular atresia in the mouse ovary. J Reprod Fertil 37: 277 - 285
11. L. Nature 379: 554 - 556
12. L function upstream of the CED-3-like apoptotic proteases. J Biol Chem 271: 4573 - 4584
13. Chun S-Y, Billig H, Tilly JL, Furuta I, Tsafriri A and Hsueh AJW (1994) Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogerious insulin-like growth factor-I. Endocrinology 135: 1845 - 1853
14. Coucouvanis EC, Sherwood SW, Carswell-Crumpton C, Spack EG and Jones PP (1993) Evidence that the mechanism of prenatal germ cell death in the mouse is apoptosis. Exp Cell Res 209: 238 - 247
15. Dolci S, Williams DE, Ernst MK, Resnick JL, Brannan CI, Lock LF, Lyman SD, Boswell S and Donovan PJ (1991) Requirement for mast cell growth factor for primordial germ cell survival in culture Nature 352. 809 - 811
16. Estoppey S, Rodriquez I, Sadoul Rand Martinou J-C (1997) Bcl-2 prevents activation of CPP32 cysteine protease and cleavage of poly (ADP-ribose) polymerase and U1-70 kD proteins in staurosporine-mediated apoptosis Cell Death and Differentiation 4: 34 - 38
17. Fernandes-Alnemri T, Litwack G and Alnemri ES (1994) CPP32, a novel human protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1β-converting enzyme. J Biol Chem 269: 30761 - 30764
18. Flaws JA, De Santi A, Tilly KI, Javid RO, Kugu K, Johnson AL, Hirshfield AN and Tilly JL (1995a) 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 - 4359
19. Flaws JA, Kugu K, Trbovich AM, Tilly KI, De Santi A, Hirshfield AN and Tilly JL (1995b) Interleukm-1β-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
20. Flemming W (1885) Über die bildung von richtungsfiguren in säugethiereiem beim untergang Graafscher follikel. Archiv fur Anatomie und Entwickelungs-geschichte (Archives fur Anatomie und Physiologie) 221 - 244
21. Forabosco A, Sforza C, De Pol A, Vizzotto L, Marzona L and Ferrario VF (1991) Morphometric study of the human neonatal ovary. Anatom Rec 231: 201 - 208
22. Fraser A and Evan G (1996) A license to kill. Cell 85: 781 - 784
23. Ginther OJ, Wiltbank MC, Fricke PM, Gibbons JR and Kot K (1996) Selection of the dominant follicle in cattle. Biol Reprod 55 1187 - 1194
24. Godin I, Deed R, Cooke J, Zsebo K, Dexter M and Wyllie CC (1991) Effects of the steel gene product on mouse primordial germ cells in culture. Nature 352: 807 - 809
25. L and Bcl-2 to prevent apoptosis can be differentially regulated. Cell Death and Differ 3: 113 - 118
26. Guthrie HD, Grimes, RW, Cooper BS and Hammond JM (1995) Follicular atresia in pigs: measurement and physiology. J Animal Sci 73: 2834 - 2844
27. Hengartner MO and Horvrtz HR (1994) Programmed cell death in Caenorhabditis elegans Curr Opm Genet Develop 4 581 - 586
28. Hirshfield AN and Midgley Jr AR (1978a) Morphometric analysis of follicular development in the rat Biol Reprod 19. 606 - 611
29. Hirshfield AN and Midgley Jr AR (1978b) The role of FSH in the selection of large ovarian follicles in the rat. Biol Reprod 19: 606 - 611
30. Hodgen GD (1982) The dominant ovarian follicle. Fertil Steril 38: 281 - 300
31. Hockenberry DM, Oltvai ZN, Yin X-M, Milliman CL and Korsmeyer SJ (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241 - 251
32. Hughes Jr FM 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
33. longgene expression. Endocrinology 137: 2059 - 2066
34. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T and Bredesen DE (1993) Bcl-2 inhibition of neural death. decreased generation of reactive oxygen species Science 262: 1274 - 1277
35. Keren-Tal I, Suh B-S, Dantes A, Lindner S, Oren M and Amsterdam A (1995) Involvement of p53 expression in cAMP-mediated apoptosis in immortalized granulosa cells Exp Cell Res 218: 283 - 295
36. Kerr JFR, Wyllie AH and Currie AR (1972) Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26: 239 - 257
37. Knudson CM, Tung KSK, Tourtellotte WG, Brown GAJ and Korsmeyer SJ (1995) Baxdeficient mice with lymphoid hyperplasia and male germ cell death. Science 270: 96 - 99
38. Knudson CM, Tung KSK, Flaws JA, Brown GAJ, Tilly JL and Korsmeyer SJ (1996) Oocyte survival but spermatocyte cell death in BAX-deficient mice. Proceedings from the International Symposium on Cell Death in Reproductive Physiology, Chicago, IL, p 33
39. Korsmeyer SJ (1995) Regulators of cell death Trends in Genetics 11: 101 - 105
40. Kumar S (1997) The Bcl-2 family of proteins and activation of the ICE-CED-3 family of proteases. a balancing act in apoptosis? Cell Death and Differ 4: 2 - 3
41. Luciano AM, Pappalardo A., Ray C and Peluso JJ (1994) Epidermal growth factor inhibits large granulosa cell apoptosis by stimulating progesterone synthesis and regulating the distribution of intracellular free calcium Biol Reprod 51: 646 - 654
42. Maravei DV, Trbovich AM, Perez GI, Tilly KI, Wong W and Tilly JL (1996) Recombinant CPP32 catalyzes proteolytic degradation of the cytoskeletal elements, α-fodrin and α-actin. Mol Biol Cell (Supplement) 7: 195a
43. Martimbeau S, Manganaro TK, Donahoe PK and Tilly JL (1996) Preliminary characterization of an in vitro model to elucidate the regulation of germ cell apoptosis in the intactfetal rat ovary J Soc Gynecol Invest (Supplement) 3: 216A
44. Martin SJ and Green DR (1995) Protease activation during apoptosis. death by a thousand cuts? Cell 82: 349 - 352
45. Mattison DR (1980) Morphology of oocyte and follicle destruction by polycyclic aromatic hydrocarbons in mice. Toxicol Appl Pharmacol 53. 249 - 259
46. Mintz B and Russell ES (1957) Gene-induced embryological modifications of primordial germ cells in the mouse J Exp Zool 134: 207 - 230
47. Miyashita T and Reed JC (1995) Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80: 293 - 299
48. Miyashita T, Harigai M, Hanada M and Reed JC (1994a) Identification of a p53-dependent negative response element in the bcl-2 gene Cancer Res 54: 3131 - 3135
49. Miyashita T, Krajewski S, Krajewski M, Wang HG, Lin HK, Liebermann DA, Hoffman B and Reed JC (1994b) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo Oncogene 9: 1799 - 1805
50. Metro B, van der Kooy D, Rossant J, Reith A and Bernstein A (1995) Contiguous patterns of c-kit and steel expression: analysis of mutations at the Wand S/loci. Development 110 1057 - 1069
51. Oltvai ZN and Korsmeyer SJ (1994) Checkpoints of dueling dimers foil death wishes Cell 79: 189 - 192
52. Oltvai ZN, Milliman CL and Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74: 609 - 619
53. O'Shea JD, Hay MF and Cran DG (1978) Ultrastuctural changes in the theca interna during follicular atresia in sheep. J Reprod Fertil 54 183 - 187
54. Patel T, Gores GJ and Kaufmann SH (1996) The role of proteases during apoptosis. FASEB J 10: 587 - 597
55. Perry DK, Smyth MJ, Wang H-G, Reed JC, Poirier GG, Obeid LM and Hannun YA (1997) Bcl-2 acts upstream of the PARP proteases and prevents its activation. Cell Death and Differ 4: 29 - 33
56. Pesce M and De Felici M (1994) Apoptosis in mouse primordial germ cells: astudy by transmission and scanning electron microscope. Anat Embryol 189: 435 - 440
57. Pesce M, Farrace MG, Piacentini M, Dolci S and 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 - 1094
58. Pinkerton JHM, McKay DG, Adams EC and Hertig TA (1961) Development of the human ovary a study using histochemical techniques. Obstet Gynecol 18. 152 - 181
59. Quatacker JR (1971) Formation of autophagic vacuoles during human corpus luteum involution Zeitschrift fur Zellforschung und Mikroskopische Anatomie 122: 479 - 487
60. 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
61. Reed JC (1994) Bcl-2 and the regulation of programmed cell death. J Cell Biol 124: 1 - 6
62. Rodger FE, Fraser HM, Duncan WC and Illingworth PJ (1995) Immunolocalization of Bcl-2 in the human corpus luteum. Human Reprod 10: 1566 - 1570
63. Rueda BR, Tilly KI, Botros I, Jolly PD, Hansen TR, Hoyer PB and Tilly JL (1997) Increased bax and interleukin-1β-converting enzyme (lce) messenger RNA levels coincide with apoptosis in the bovine corpus luteum during structural regression. Biol Reprod 56: 186 - 193
64. Sato T, Hanada M, Bodrug S, lrie S, Iwama N, Boise LH, Thompson CB, Golemis E, Fong L. Wang H-G and Reed JC (1994) Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc Natl Acad Sci USA 91: 9238 - 9242
65. Schwartzman RA and Cidlowski JA (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocrine Rev 14: 133 - 151
66. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB and Korsmeyer SJ (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax Proc Natl Acad Sci USA 92 7834 - 7838
67. Springer LN, McAsey ME, Flaws JA, Tilly JL, Sipes IG and Hoyer PB (1996a) Involvement of apoptosis in 4-vinylcyclohexene diepoxide-induced ovotoxicity in rats Toxicol Appl Pharmacol 139: 394 - 401
68. Springer LN, Tilly JL, Sipes IG and Hoyer PB (1996b) Enhanced expression of baxin small preantral follicles during 4-vinylcyclohexene diepoxide-induced ovotoxicity in the rat. Toxicol Appl Pharmacol 139: 402 - 410
69. Steinman HM (1995) The Bcl-2 oncoprotein functions as a pro-oxidant J Biol Chem 270 3487 - 3490
70. Tilly JL (1994) Use of the terminal transferase DNA labeling reaction for the biochemical and in situ analysis of apoptosis. In Cell biology a laboratory handbook. in Cells JE, ed. (San Diego: Academic Press) pp. 330 - 337
71. Tilly JL (1996) Apoptosis and ovarian function. Rev Reprod 1. 162 - 172
72. Tilly JL and Ratts VS (1996) Biological and clinical importance of ovarian cell death. Contemp Obstet Gynecol 41: 59 - 86
73. Tilly JL and Tilly KI (1995) Inhibitors of oxidative stress mimic the ability of folliclestimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 136: 242 - 252
74. Tilly JL, Kowalski KI, Johnson AL and Hsueh AJW (1991) Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129: 2799 - 2801
75. Tilly JL, Billig H, Kowalski KI and Hsueh AJW (1992) Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine kinase-dependent mechanism Mol Endocrinol 6: 1942 - 1950
76. long messenger ribonucleic acid levels, Endocnnology 136: 232 - 241
77. Tilly JL, Flaws JA, DeSanti A, Kugu K, Rubin JS and Hirshfield AN (1995b) Role of intrafollicular growth factors in maturation and atresia of rat ovarian follicles. Biol Reprod (Supplement 1) 52. 159
78. Tilly KI, Banerjee S, Banerjee PP and Tilly JL (1995c) Expression of the p53 and Wilms' tumor suppressor genes in the rat ovary: gonadotropin repression in vivo and immunohistochemical localization of nuclear p53 protein to apoptotic granulosa cells of atretic follicles Endocrinology 136. 1394 - 1402
79. Tilly JL, Kugu K, Ratts VS, Piquette GN, Tilly KI, Aberdeen GW, Pepe J and Albrecht ED (1996a) Apoptosis and cell death gene expression in the human and baboon ovary J Soc Gynecol Invest (Supplement) 3: 70A
80. Tilly JL, Tao XJ and Ratts VS (1996b) Immunolocalization of the BAX deatbsusceptibility factor in the regressing human corpus luteum. Proceedings from the 52nd Annual Meeting of the American Society for Reproductive Medicine, Boston, MA, p S136
81. Trbovich AM, Hughes Jr FM, Perez GI, Tilly KI, Cidlowski JA and Tilly JL (1996a) Requirement for ICE-related protease (IRP) activity in oligonucleosomal endonuclease activation dunng apoptosis resides in the cytoplasmic compartment of rat ovarian granulosa cells Proceedings from the International Symposium on Cell Death in Reproductive Physiology, Chicago, IL, p 36
82. Trbovich AM, Hughes Jr FM, Perez GI, Kugu K, Flaws JA, De Santi AM, Hirshfield AN and Tilly JL (1996b) High molecular weight DNA cleavage occurs in apoptotic granulosa cells (GC) of atretic follicles and is induced via a pathway independent of interleukin-1β-converting enzyme (ICE) activity J Soc Gynecol Invest (Supplement) 3: 173A
83. Wang L, Miura M, Bergeron L, Zhu H and Yuan J (1994) lch-1, an ICE/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78. 739 - 750
84. Williams JR, Little JB and Shipley WU (1974) Association of mammalian cell death with specific endonucleolytic degradation of DMA. Nature 252: 754 - 756
85. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284. 555 - 556
86. Yin X-M, Oltvai ZN and Korsmeyer SJ (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369: 321 - 323
87. Zeleznik AJ (1981) Premature elevation of systemic estradiol reduces serum level of follicle-stimulating hormone and lengthens the follicular phase of the menstrual cycle in rhesus monkeys. Endocrinology 109. 352 - 355
88. Zeleznik AJ, Schuler HM and Reichert Jr LE (1981) Gonadotropin binding sites in the rhesus monkey ovary role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 109: 356 - 362
89. Zeleznik AJ, Hutchinson JS and Schuler HM (1985) Interference with the gonadotropin-suppressing actions of estradiol in macaques overrides the selection of a single preovulatory follicle Endocrinology 117: 991 - 999
90. ++-dependent endonuclease activity in rat granulosa and luteal cells. Endocrinology 125: 2218 - 2220