Follicle Selection in Mammalian Ovaries: Regulatory Mechanisms of Granulosa Cell Apoptosis during Follicular Atresia

The Ovary: Second Edition

Volumn , Issue , 2004, Pages 369-385

  Manabe, Noboru ^a   Inoue, Naoke ^a   Sugimoto, Miki ^a   Miyamoto, Hajime ^a   Miyano, Takashi ^b   Sakamaki, Kazuhiro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84942791616     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012444562-8/50022-7     Document Type: Chapter

References (158)

1. Baker T.G. A quantitative and cytological study of germ cells in the human ovaries. Proc. Roy. Soc. Lond. 1963, 158:417-433.
2. Braw R.H., Byskov A.G., Peters H., Faber M. Follicular atresia in the human infant ovary. J. Reprod. Fertil. 1976, 46:55-59.
3. Cárdenas H., Pope W.F. Control of ovulation rate in swine. J. Anim. Sci. 2002, 80:36-46.
4. Byskov A.G.S. Atresia. Ovarian Follicular Development and Function 1979, 41-57. Raven Press, New York. A.R. Midgley, W.A. Sadler (Eds.).
5. Hirshfield A.N. Development of follicles in the mammalian ovary. Int. Rev. Cytol. 1991, 124:43-101.
6. Herwitz A., Adashi E.Y. Ovarian follicular atresia as an apoptotic process. The Ovary 1993, 473-485. Raven Press, New York. 1st ed. E.Y. Adashi, P.C.K. Leung (Eds.).
7. Tilly J.L. Cell death and species propagation: Molecular and genetic aspects of apoptosis in the vertebrate female gonad. When Cells Die 1998, 431-452. Wiley-Liss, Inc., New York. R.A. Lockshin, Z. Zakeri, J.L. Tilly (Eds.).
8. Hirshfield A.N. Rescue of atretic follicles in vitro and in vivo. Biol. Reprod. 1989, 40:181-190.
9. Imai Y., Manabe N., Uchio K., Kinoshita A., Kimura Y., Nakayama M., Nishihara S., Wada S., Sugimoto M., Miyamoto H. Interactions of apoptosis and extra-cellular matrices in granulosa cells of atretic follicles in porcine ovaries. J. Mamm. Ova. Res. 1999, 16:59-66.
10. Bagavandoss P., Midgley A.R., Wicha M. Developmental changes in the ovarian follicular basal lamina detected by immunofluorescence and electron microscopy. J. Histochem. Cytochem. 1983, 31:633-640.
11. Hay M.F., Cran D.G., Moor R.M. Structural changes occurring during atresia in sheep ovarian follicles. Cell Tissue Res. 1976, 169:515-529.
12. Sugimoto M., Manabe N., Kimura Y., Myomoto A., Imai Y., Ohno H., Miyamoto H. Ultrastructural changes in granulosa cells in porcine antral follicles under-going atresia indicate apoptotic cell death. J. Reprod. Dev. 1998, 44:7-14.
13. Greenwald G.S. Temporal and topographic changes in DNA synthesis after induced follicular atresia. Biol. Reprod. 1989, 40:175-181.
14. Tilly L.J., Kowalski K.I., Schomberg D.W., Hsueh A.J.W. Apoptosis in atretic ovarian follicles is associated with selective decrease in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 1992, 131:1670-1676.
15. Erickson G.F., Magoffin D.A., Dyer C.A., Hofeditz C. The ovarian androgen producing cells: A review of structure/function relationship. Endocr. Rev. 1985, 6:371-399.
16. Tsafriri A., Braw R.H. Experimental approach to atresia in mammals. Oxf. Rev. Reprod. Biol. 1984, 6:226-265.
17. ++-dependent endonuclease activity in rat granulosa and luteal cells. Endocrinology 1989, 125:2218-2220.
18. Tilly J.L., Kowalski K.I., Johnson A.L., Hsueh A.J.W. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 1991, 129:2799-2801.
19. 2+-dependent or cation-independent endonuclease is involved in granulosa cell apoptosis of pig atretic follicles. J. Reprod. Dev. 1996, 42:247-253.
20. Black J.L., Erickson B.H. Oogenesis and ovarian development in the prenatal pig. Anat. Rec. 1968, 161:45-55.
21. Picton H., Briggs D., Gosden R. The molecular basis of oocyte growth and development. Mol. Cell. Endocrinol. 1998, 145:27-37.
22. Zamboni L. Fine morphology of the follicle wall and follicle cell-oocyte association. Biol. Reprod. 1974, 10:125-149.
23. Grant S.A., Hunter M.G., Foxcroft G.R. Morphological and biochemical characteristics during ovarian follicular development in the pig. J. Reprod. Fertil. 1989, 86:171-183.
24. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gunsmuller A., LeMeur M., Sassoni-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: Targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. USA 1998, 95:13612-13617.
25. Hunter R.H.F. Ovarian follicular responsiveness and oocyte quality after gonadotrophic stimulation in mature pigs. Ann. Biol. Biochem. Biophys. 1979, 5:1511-1520.
26. Guthrie H.D., Pursel V.G., Wall R.J. Porcine follicle stimulating hormone treatment of gilts during an altrenogest-synchronized follicular phase: Effects on follicle growth, hormone secretion, ovulation and fertilization. J. Anim. Sci. 1997, 75:3246-3254.
27. Paterson A.M. The controlled induction of puberty. Control of Pig Reproduction 1982, 139-159. Butterworth Scientific, London. D.J. Cole, G.R. Foxcroft (Eds.).
28. Brown R.W., Hungerford J.W., Greenwood P.E., Bloor R.J., Evans D.F., Tsonis C.G., Forage G. Immunization against recombinant bovine inhibin alpha subunit causes increased ovulation rate in gilts. J. Reprod. Fertil. 1990, 90:199-205.
29. King B.F., Britt J.H., Esbenshade K.L., Flowers W.L., Sesti L.A.C., Martin T.L., Ireland J.J. Ovulatory and endocrine responses after active immunization of gilts against a synthetic fragment of bovine inhibin. J. Anim. Sci. 1993, 71:975-982.
30. Foxcroft G.R., Hunter M.G. Basic physiology of follicular maturation in the pig. J. Reprod. Fertil. 1985, 33:1-19.
31. Fortune J.E. Ovarian follicular growth and development in mammals. Biol. Reprod. 1994, 50:225-232.
32. Guthrie H.D., Grimes R.W., Cooper B.S., Hammond J.M. Follicular atresia in pigs: Measurement and physiology. J. Anim. Sci. 1995, 73:2834-2844.
33. Morbeck D.E., Esbenshade K.L., Flowers W.L., Britt J.H. Kinetics of follicle growth in the prepuberal gilt. Biol. Reprod. 1992, 47:485-491.
34. Clark J.R., Brazier S.G., Wiginton L.M., Stevenson G.R., Tribble L.F. Time of ovarian follicle selection during the porcine estrous cycle. Theriogenology 1982, 18:697-709.
35. Dailey R.A., Clark J.R., Staigmiller R.B., First N.L., Chapman A.B., Casida L.E. Growth of new follicles following electrocautery in four genetic groups of swine. J. Anim. Sci. 1976, 43:175-183.
36. Miller A.T., Picton H.M., Craigon J., Hunter M.G. Follicle dynamics and aromatase activity in high-ovulating Meisha sows and in Large-White hybrid contemporaries. Biol. Reprod. 1998, 58:1372-1378.
37. Kaipia A., Hsueh A.J.W. Regulation of ovarian follicle atresia. Ann. Rev. Physiol. 1997, 59:349-363.
38. Hsu S.Y., Hsueh A.J.W. Tissue-specific Bcl2-protein partners in apoptosis: An ovarian paradigm. Physiol. Rev. 2000, 80:593-614.
39. Tilly J.L. Ovarian follicular atresia: A model to study the mechanisms of physiological cell death. Endocrinol. J. 1993, 1:67-72.
40. Manabe N., Kimura Y., Myoumoto A., Matsushita H., Tajima C., Sugimoto M., Miyamoto H. Role of granulosa cell apoptosis in ovarian follicle atresia. Apoptosis: Its Roles and Mechanism 1998, 97-111. Academic Societies Japan, Tokyo. T. Yamada, Y. Hashimoyto (Eds.).
41. Yonehara S., Ishii A., Yonehara M.A. Cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 1989, 169:1747-1756.
42. Ellis R.E., Yuan J.Y., Horvitz H.R. Mechanisms and functions of cell death. Annu. Rev. Cell. Biol. 1991, 663-698.
43. Steller H. Mechanisms and genes of cellular suicide. Science 1995, 267:1445-1449.
44. Nagata S. Apoptosis by death factor. Cell 1997, 88:355-365.
45. Golstein P. Cell death: TRAIL and its receptors. Curr. Biol. 1997, 7:750-753.
46. Schulze-Osthoff K., Ferrari D., Los M., Wesselborg S., Peter M.E. Apoptosis signaling by death receptors. Eur. J. Biochem. 1998, 254:439-459.
47. Ashkenazi A., Dixit V.M. Death receptors: Signaling and modulation. Science 1998, 281:1305-1308.
48. Ashkenazi A., Dixit V.M. Apoptosis control by death and decoy receptors. Curr. Opin. Cell. Biol. 1999, 11:255-260.
49. Cohen G.M. Caspases: The executioners of apoptosis. Biochem. J. 1997, 326:1-16.
50. Nicholson D.W., Thornberry N.A. Caspases: Killer proteases. Trend. Biochem. Sci. 1997, 22:299-306.
51. Thornberry N.A., Lazebnik Y. Caspases: Enemies within. Science 1998, 281:1312-1316.
52. Grutter M.G. Caspases: Key players in programmed cell death. Curr. Opin. Struc. Biol. 2000, 10:649-655.
53. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: A basic biological phenomenon with wide ranging implication in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
54. Tilly J.L., Hsueh A.J.W. Apoptosis as the basis of ovarian follicular atresia. Gonadal Development and Function 1992, 157-165. Raven Press, New York. S.G. Hillier (Ed.).
55. Tilly J.L. Apoptosis and ovarian function. Rev. Reprod. 1996, 1:162-172.
56. Manabe N., Imai Y., Ohno H., Takahagi Y., Sugimoto M., Miyamoto H. Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in the pig ovaries. Experientia 1996, 52:647-651.
57. Hsueh A.J.W., Kaipia A. Regulation of ovarian follicle atresia. Annu. Rev. Physiol. 1997, 59:349-363.
58. Izawa M., Nguyen P.H., Kim H.H., Yeh J. Expression of the apoptosis-related genes, caspase-1, caspase-3, DNA fragmentation factor, and apoptotic protease activating factor-1, in human granulosa cells. Fertil. Steril. 1998, 70:549-552.
59. Robles R., Tao X-J, Trbovich A.M., Maravel D.V., Nahum R., Perez G.I., Tilly K.I., Tilly J.L. Localization, regulation and possible consequences of apoptotic protease-activating factor-1 (Apaf-1) expression in granulosa cells of the mouse ovary. Endocrinology 1999, 140:2641-2644.
60. Kimura Y., Manabe N., Nishihara S., Matsushita H., Tajima C., Wada S., Miyamoto H. Up-regulation of the α2,6-sialyltransferase messenger ribonucleic acid increases glycoconjugates containing α2,6-linked sialic acid residues in granulosa cells during follicular atresia of porcine ovaries. Biol. Reprod. 1999, 60:1475-1482.
61. Tajima C., Manabe N., Inoue N., Matsui T., Hondo E., Miyamoto H. Monoclonal antibody recognizes follicular granulosa cell antigens in porcine ovaries. J. Reprod. Dev. 2002, 48:567-572.
62. Anderson P. Kinase cascades regulating entry into apoptosis. Microbiol. Mol. Biol. Rev. 1997, 61:33-46.
63. Okamura Y., Myoumoto A., Manabe N., Tanaka N., Okamura H., Fukumoto M. Protein tyrosine kinase expression in the porcine ovary. Mol. Human Reprod. 2001, 7:723-729.
64. Flemming W. Über die Bildung von Richtungsfiguren in Säugethiereiern beim Untergang Graaf'scher Follikel. Arch. Anat. EntGesch. 1885, 221-244.
65. Manabe N., Imai Y., Myoumoto A., Kimura Y., Sugimoto M., Okamura Y., Fukumoto M., Sakamaki K., Miyamoto H. Apoptosis occurs in granulosa cells but not cumulus cells in the atretic graafian follicles in multiparous pig ovaries. Acta. Histochem. Cytochem. 1997, 30:85-92.
66. Nakayama M., Manabe N., Nishihara S., Miyamoto H. Species specific differences in apoptotic cell localization in granulosa and theca interna cells during follicular atresia in porcine and bovine ovaries. J. Reprod. Dev. 2000, 46:147-156.
67. Palumbo A., Yeh J. In situ localization of apoptosis in the rat ovary during follicular atresia. Biol. Reprod. 1994, 51:888-895.
68. Hernandez E.R., Roberts C.T.J., LeRoith D., Adashi E.Y. Rat ovarian insulin-like growth factor I (IGF-I) gene expression is granulosa cell-selective: 5'-untranslated mRNA variant representation and hormonal regulation. Endocrinology 1989, 136:2770-2775.
69. Dhanasekaran N., Moudgal N.R. Studies on follicle atresia: Role of gonadotropins and gonadal steroids in regulating cathepsin-D activity of preovulatory follicles in the rat. Endocrinology 1989, 63:133-142.
70. Findlay J.K. An update on the roles of inhibin, activin and follistatin as local regulators of folliculogenesis. Biol. Reprod. 1993, 48:15-23.
71. Yoshimura Y. Insulin-like growth factors and ovarian physiology. J. Obstet. Gynecol. Res. 1998, 24:305-323.
72. Billig H., Furuta I., Hsueh A.J.W. Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: Biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells. Endocrinology 1994, 134:245-251.
73. Chun S.Y., Billig H., Tilly J., Furuta I., Tsafriri A., Hsueh A.J.W. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: Mediatory role of endogenous IGF-I. Endocrinology 1994, 135:1845-1853.
74. Eisenhauer K.M., Chun S.Y., Billig H., Hsueh A.J.W. Growth hormone suppression of ovarian follicle apoptosis and partial neutralization by insulin-like growth factor binding protein (IGFBP). Biol. Reprod. 1995, 53:13-20.
75. Chun S.Y., Eisenhauer K.M., Kubo M., Hsueh A.J.W. Interleukin-1β suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 1995, 136:3120-3127.
76. Chun S.Y., Eisenhauer K.M., Minami S., Billig H., Perlas E., Hsueh A.J.W. Hormonal regulation of apoptosis in early antral follicles: Follicle-stimulating hormone as a major survival factor. Endocrinology 1996, 137:1447-1456.
77. McGee E., Spears N., Minami S., Hsu S.Y., Chun S.Y., Billig H., Hsueh A.J.W. Preantral ovarian follicles in serum-free culture: Suppression of apoptosis after activation of the cGMP pathway and stimulation of growth and differentiation by FSH. Endocrinology 1997, 138:2417-2424.
78. Ingram D.L. The effect of oestrogen on the atresia of ovarian follicles. J. Endocrinol. 1959, 19:123-125.
79. Maxson W.S., Haney A.F., Schomberg D.W. Steroidogenesis in porcine atretic follicles: Loss of aromatase activity in isolated granulosa and theca. Biol. Reprod. 1985, 33:495-501.
80. Babaloa G.O., Shapiro H. Correlation of follicular steroid hormone profiles with ovarian cyclicity in sows. J. Reprod. Fertil. 1988, 84:79-87.
81. Billig H., Furuta I., Hsueh A.J.W. Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 1993, 133:2204-2212.
82. Coley A.J., Howard H.J., Slanger W.D., Ford J.J. Steroidogenesis in the preovulatory porcine follicle. Biol. Reprod. 1994, 51:655-661.
83. Guthrie H.D., Cooper B.S., Welch G.R., Zakaria A.D., Johnson L.A. Atresia in follicles grown after ovulation in the pig: Measurement of increased apoptosis in granulosa cells and reduced follicular fluid estradiol-17β. Biol. Reprod. 1995, 52:920-927.
84. Hsueh A.J.W., Billig H., Tsafriri A. Ovarian follicle atresia: A hormonally controlled apoptotic pathway. Endocr. Rev. 1994, 15:1-18.
85. Billig H. Follicle apoptosis. Gynecol. Endocrinol. 1996, 10:7-8.
86. Billig H., Chun S.Y., Eisenhauer K., Hsueh A.J.W. Gonadal cell apoptosis: Hormone-regulated cell demise. Human Reprod. Update 1996, 2:103-117.
87. Hsueh A.J.W., Eisenhauer K., Chun S.Y., Hsu S.Y., Billig H. Gonadal cell apoptosis. Rec. Prog. Hormone Res. 1996, 51:433-456.
88. Gougeon A. Regulation of ovarian follicular development in primates: Facts and hypotheses. Endocr. Rev. 1996, 17:121-155.
89. Chun S.Y., Hsueh A.J.W. Paracrine mechanisms of ovarian follicle apoptosis. J. Reprod. Immunol. 1998, 39:63-75.
90. Driancourt M.A., Thuel B. Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. Reprod. Nutr. Dev. 1998, 38:345-362.
91. Juengel J.L., Garverick H.A., Johnson A.L., Youngquist R.S., Smith M.F. Apoptosis during luteal regression in cattle. Endocrinology 1993, 132:249-254.
92. Quirk S.M., Cowan R.G., Joshi S.G., Henrikson K.P. Fas antigen-mediated apoptosis in human granulosa/luteal cells. Biol. Reprod. 1995, 52:279-287.
93. Rueda B.R., Wegner J.A., Marion S.L., Wahlen D.D., Hoyer P.B. Internucleosomal DNA fragmentation in ovine luteal tissue associated with luteolysis: In vivo and in vitro analyses. Biol. Reprod. 1995, 52:305-312.
94. Shikone T., Yamamoto M., Kokawawa K., Yamashita K., Nishimori K., Nakano R. Apoptosis of human corpora lutea during cyclic luteal regression and early pregnancy. J. Clin. Endocrinol. Metab. 1996, 81:2376-2380.
95. Sakamaki K., Yoshida H., Nishimura Y., Nishikawa S.I., Manabe N., Yonehara S. Involvement of Fas antigen in ovarian follicular atresia and luteolysis. Mol. Reprod. Dev. 1997, 47:11-18.
96. Bowen J.M., Towns R., Warren J.S., Keyes P.L. Luteal regression in the normally cycling rat: Apoptosis, monocyte chemoattractant protein-1, and inflammatory cell involvement. Biol. Reprod. 1999, 60:740-746.
97. Roughton S.A., Lareu R.R., Bittles A.H., Dharmarajan A.M. Fas and Fas ligand messenger ribonucleic acid and protein expression in the rat corpus luteum during apoptosis-mediated luteolysis. Biol. Reprod. 1999, 60:797-804.
98. Quirk S.M., Harman R.M., Huber S.C., Cowan R.G. Responsiveness of mouse corpora luteal cells to Fas antigen (CD95)-mediated apoptosis. Biol. Reprod. 2000, 63:49-56.
99. Morita Y., Perez G.I., Maravei D.V., Tilly K.I., Tilly J.L. Targeted expression of Bcl-2 in mouse oocytes inhibits ovarian follicle atresia and prevents spontaneous and chemotherapy-induced oocyte apoptosis in vitro. Mol. Endocrinol. 1999, 13:841-850.
100. Hakuno N., Koji T., Yano T., Kobayashi N., Tsutsumi O., Taketani Y., Nakane P.K. Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. Endocrinology 1996, 137:1938-1948.
101. Quirk S.M., Cowan R.G., Huber S.H. Fas antigen-mediated apoptosis of ovarian surface epithelial cells. Endocrinology 1997, 138:4558-4566.
102. Kim J.M., Boone D.L., Auyeung A., Tsang B.K. Granulosa cell apoptosis induced at the penultimate stage of follicular development is associated with increased levels of Fas and Fas ligand in the rat ovary. Biol. Reprod. 1998, 58:1170-1176.
103. Xu J.P., Li X., Mori E., Guo M.W., Mori T. Aberrant expression and dysfunction of Fas antigen in MRL/MpJlpr/lpr murine ovary. Zygote 1998, 6:359-367.
104. Kim J.M., Yoon Y.D., Tsang B.K. Involvement of the Fas/Fas ligand system in p53-mediated granulosa cell apoptosis during follicular development and atresia. Endocrinology 1999, 140:2307-2317.
105. Hsu H., Xiong J., Goeddel D.V. The TNF receptor 1-associated protein TRADD signals cell death and NF-κ activation. Cell 1995, 81:495-504.
106. Boldin M.P., Varfolomeev E.E., Pancer Z., Mett I.L., Camonis J.H., Wallach D. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J. Biol. Chem. 1995, 270:7795-7798.
107. Inoue J., Ishida T., Tsukamoto N., Kobayashi N., Naito A., Azuma S., Yamamoto T. Tumor necrosis factor receptor-associated factor (TRAF) family: Adapter proteins that mediate cytokine signaling. Exp. Cell. Res. 2000, 254:14-24.
108. Wajant H., Scheurich P. Tumor necrosis factor receptor-associated factor (TRAF) 2 and its role in TNF signaling. Int. J. Biochem. Cell. Biol. 2001, 33:19-32.
109. Stanger B.Z., Leder P., Lee T.H., Kim E., Seed B. RIP: A novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell 1995, 81:513-523.
110. Shu H.B., Takeuchi M., Goeddel D.V. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc. Natl. Acad. Sci. USA 1996, 93:13973-13978.
111. Arch R.H., Gedrich R.W., Thompson C.B. Tumor necrosis factor receptor-associated factors (TRAFs): A family of adapter proteins that regulates life and death. Genes Dev. 1998, 12:2821-2830.
112. Prange-Kiel J., Kreutzkamm C., Wehrenberg U., Rune G.M. Role of tumor necrosis factor in preovulatory follicles of swine. Biol. Reprod. 2001, 65:928-935.
113. Nakayama M., Manabe N., Inoue N., Matsui T., Miyamoto H. Changes in the expression of tumor necrosis factor (TNF) α, TNFα receptor (TNFR) 2 and TNFR-associated factor 2 in granulosa cells during atresia in pig ovaries. Biol. Reprod. 2003, 68:530-535.
114. Wiley S.R., Schooley K., Smolak P.J., Din W.S., Huang C.P., Nicholl J.K., Sutherland G.R., Smith T.D., Rauch C., Smith C.A., Goodwin R.G. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995, 3:673-682.
115. Pitti R.M., Marsters S.A., Ruppert S., Donahue C.J., Moore A., Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 1996, 271:12687-12690.
116. Marsters S.A., Pitti R.M., Donahue C., Ruppert S., Bauer K., Ashkenazi A. Activation of apoptosis by Apo-2 ligand is independent of FADD but blocked by CrmA. Curr. Biol. 1996, 6:750-752.
117. Pan G., O'Rourke K., Chinnaiyan A.M., Gentz R., Ebner R., Ni J., Dixit V.M. The receptor for the cytotoxic ligand TRAIL. Science 1997, 276:111-113.
118. McFarlane M., Ahmad M., Srinivasula S.M., Fernandes-Alnemri T., Choen G.M., Alnemri E.S. Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J. Biol. Chem. 1997, 272:25417-25420.
119. Schneider P., Bodmer J.L., Thome M., Hofman K., Hohller N., Tschopp J. Characterization of two receptors for TRAIL. FEBS Lett. 1997, 416:329-334.
120. Marsters S.A., Sheridan J.P., Pitti R.M., Huang A., Skubatch M., Baldwin D., Yuan J., Gurney A., Godowski P., Ashkenazi A. A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr. Biol. 1997, 7:1003-1006.
121. Walczak H., Degli-Esposti M.A., Johonson R.S., Smolak P.J., Waugh J.Y., Boiani N., Timour M.S., Gerhart M.J., Schooley K.A., Smith C.A. TRAIL-R2: A novel apoptosis-mediating receptor for TRAIL. EMBO J. 1997, 16:5386-5397.
122. Pan G., Ni J., Wei Y-F, Yu G-L, Gentz R., Dixit V.M. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 1997, 277:815-818.
123. Sheridan J.P., Marsters S.A., Pitti R.M., Gerney A., Skubatch M., Baldwin D., Ramakrishnan L., Gray C.L., Baker K., Wood W.I., Goodard A.D., Godowski P., Ashkenazi A. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997, 277:818-821.
124. Degli-Esposti M.A., Smolak P.J., Walczak H., Waugh J.Y., Huang C.P., Dubose R.F., Goodwin R.G., Smith C.A. Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J. Exp. Med. 1997, 186:1165-1170.
125. Degli-Esposti M.A., Dougall W.C., Smolak P.J., Waugh J.Y., Smith C.A., Goodwin R.G. The novel receptor TRAIL-R4 induces NF-κ and protects against TRAIL-mediated apoptosis, yet retrains an incomplete death domain. Immunity 1997, 7:813-820.
126. Mongkolsapaya J., Cowper A., Xu X.N., Morris G., McMichael A., Bell J.I., Screaton G.R. Lymphocyte inhibitor of TRAIL: A new receptor protecting lymphocytes from the death ligand TRAIL. J. Immunol. 1998, 160:3-6.
127. Pan G., Ni J., Yu L., Wei Y-F, Dixit V.M. TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signaling. FEBS Lett. 1998, 424:41-45.
128. Degli-Esposti M.A. To die or not to die-the quest of the TRAIL receptors. J. Leukoc. Biol. 1999, 65:535-542.
129. Emery J.G., McDonnell P., Burke M.B., Deen K.C., Lyn S., Silverman C., Dul E., Appelbaum E.R., Eichman C., Diprinzio R., Dodds R.A., James I.E., Rosenberg M., Lee J.C., Young P.R. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J. Biol. Chem. 1998, 273:14363-14367.
130. Truneh A., Sharma S., Silverman C., Khandekar S., Reddy M.P., Deen K.C., Mclaughlin M.M., Srinivasula S.M., Livi G.P., Marshall L.A., Alnemri E.S., Williams W.V., Doyle M.L. Temperature-sensitive differential affinity of TRAIL for its receptors. DR5 is the highest affinity receptor. J. Biol. Chem. 2000, 275:23319-23325.
131. Cleveland J.L., Ihle J.N. Contenders in FasL/TNF death signaling. Cell 1995, 81:479-482.
132. Lynch D., Ramsdell F., Alderson M.R. Fas and FasL in the homeostatic regulation of immune responses. Immunol. Today 1995, 16:569-573.
133. Nagata S., Golstein P. The Fas death factor. Science 1995, 267:1449-1456.
134. Walczak H., Krammer P.H. The CD95 (APO-1/Fas) and the TRAIL (APO-2L) apoptosis systems. Exp. Cell. Res. 2000, 256:58-66.
135. Ozoren N., Fisher M.J., Kim K., Liu C.X., Genin A., Shifman Y., Dicker D.T., Spinner N.B., Lisitsyn N.A., EI-Deiry W.S. Homozygous deletion of the death receptor DR4 gene in a nasopharyngeal cancer cell line is associated with TRAIL resistance. Int. J. Oncol. 2000, 16:917-925.
136. Zhang X.D., Nguyen T., Thomas W.D., Sanders J.E., Hersey P. Mechanisms of resistance of normal cells to TRAIL induced apoptosis vary between different cell types. FEBS Lett. 2000, 482:193-199.
137. Chaudhary P.M., Eby M., Jasmin A., Bookwalter A., Murray J., Hood L. Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-κ pathway. Immunity 1997, 7:812-830.
138. Schneider P., Thome M., Burns K., Bodmer J.L., Hofmann K., Kataoka T., Holler N., Tschopp J. TRAIL receptors 1 (DR4) and 2 (DR5) signal FADD-dependent apoptosis and activate NF-κ. Immunity 1997, 7:831-836.
139. Kischkel F.C., Lawrence D.A., Chuntharapai A., Schow P., Kim J., Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000, 12:611-620.
140. Wada S., Manabe N., Inoue N., Nakayama M., Matsui T., Miyamoto H. TRADD is involved in apoptosis induction in granulosa cells during atresia in pig ovaries. J. Reprod. Dev. 2002, 48:175-181.
141. Wada S., Manabe N., Inoue N., Nakayama M., Matsui T., Miyamoto H. TRAIL-decoy receptor-1 disappears in granulosa cells of atretic follicles in porcine ovaries. J. Reprod. Dev. 2002, 48:167-173.
142. Wada S., Manabe N., Nakayama M., Inoue N., Matsui T., Miyamoto H. TRAIL-decoy receptor 1 plays inhibitory role in apoptosis of granulosa cells from pig ovarian follicules. J. Vet. Med. Sci. 2002, 64:435-439.
143. Myoumoto A., Manabe N., Imai Y., Kimura Y., Sugimoto M., Okamura Y., Fukumoto M., Sakamaki K., Niwano Y., Miyamoto H. Monoclonal antibodies against pig ovarian follicular granulosa cells induce apoptotic cell death in cultured granulosa cells. J. Vet. Med. Sci. 1997, 59:641-649.
144. Manabe N., Kimura Y., Uchio K., Tajima C., Matsushita H., Nakayama M., Sugimoto M., Miyamoto H. Regulatory mechanisms of granulosa cell apoptosis in ovarian follicle atresia: Role of granulosa cell apoptosis in porcine ovarian follicle atresia. Animal Cell Technology 1999, 343-347. Kluwer Academic, Dordrecht, The Netherlands. K. Iikura, M. Nagao, S. Masuda, R. Sasaki (Eds.).
145. Manabe N., Myoumoto A., Tajima C., Fukumoto M., Nakayama M., Uchio K., Yamaguchi M., Miyamoto H. Immunochemical characteristics of a novel cell death receptor and a decoy receptor on granulosa cells of porcine ovarian follicles. Cytotechnology 2000, 33:189-201.
146. Manabe N., Myoumoto A., Tajima C., Nakayama M., Yamaguchi M., Yamada-Uchio K., Miyamoto H. Monoclonal antibodies recognize a novel cell death receptor and a decoy receptor on granulosa cells of porcine ovarian follicles. J. Mamm. Ova. Res. 2001, 18:1-13.
147. Manabe N., Sugimoto M., Nakayama M., Inoue N., Matsui T., Yamaguchi M., Yamada-Uchio K., Miyamoto H. Histological and biochemical profiles of granulosa cell apoptosis in follicular atresia of porcine ovaries. Reproductive Biotechnology 2001, 61-72. Hokuto Publications, Kyoto, Japan. H. Miyamoto, N. Manabe (Eds.).
148. Oi V.T., Herzenberg L.A. Immunoglobulin producing hybrid cell lines. Selected Methods in Cellular Immunology 1980, 351-372. Freeman Publications, San Francisco. B.B. Mishell, S.M. Shiiji (Eds.).
149. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S-I, Sameshima M., Hase A., Seto Y., Nagata S. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991, 66:233-243.
150. Yoo J., Stone R.T., Beattie C.W. Cloning and characterization of the bovine Fas. DNA Cell Biol. 1996, 15:227-234.
151. Stauber G.B., Aiyer R.A., Aggatwal B.B. Human tumor necrosis factor-alpha receptor purification by immunoaffinity chromatography and initial characterization. J. Biol. Chem. 1988, 263:190-198.
152. Murdoch W.J. Immunolocalization of a gonadotropin-releasing hormone receptor site in murine endometrium that mediates apoptosis. Cell Tissue Res. 1995, 282:527-529.
153. Yamada T., Horiuchi M., Dzau V.J.S.O. Angiotensin II type 2 receptor mediates programmed cell death. Proc. Natl. Acad. Sci. USA 1996, 93:156-160.
154. Chicheportiche Y., Bourdon P.R., Xu H., Hsu Y.M., Scott H., Hession C., Garcia I., Brownin J.L. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 1997, 272:32401-32410.
155. Marsters S.A., Sheridan J.P., Pitti R.M., Brush J., Goddard A., Ashkenazi A. Identification of a ligand for the death-domain-containing receptor Apo3. Curr. Biol. 1998, 8:525-528.
156. Hsu S.Y., Kaipia A., McGee E., Lomeli M., Hsueh A.J.W. Bok is a pro-apoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective antiapoptotic Bcl-2 family members. Proc. Natl. Acad. Sci. USA 1997, 94:12401-12406.
157. Hsu S.Y., Hsueh A.J. 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. 1998, 12:1432-1440.
158. Song Q., Kuang Y., Dixit V.M., Vincenz C. Boo, a novel negative regulator of cell death, interacts with Apaf-1. EMBO J. 1999, 18.