Estradiol-mediated suppression of apoptosis in the rabbit corpus luteum is associated with a shift in expression of bcl-2 family members favoring cellular survival

Biology of Reproduction

Volumn 59, Issue 4, 1998, Pages 820-827

  Goodman, S B ^a,b   Kugu, K ^b,c   Chen, S H ^a,b   Preutthipan, S ^b,d   Tilly, K I ^e,f   Tilly, J L ^e,f   Dharmarajan, A M ^b,g  

^a School of Medicine ^*  (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d MAHIDOL UNIVERSITY   (Thailand)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CORPUS LUTEUM; DNA DETERMINATION; HORMONAL REGULATION; LUTEAL CELL; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROGESTERONE RELEASE; PSEUDOPREGNANCY; RABBIT; REGULATORY MECHANISM;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, NORTHERN; CELL SURVIVAL; CORPUS LUTEUM; DNA; DNA FRAGMENTATION; DNA PROBES; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; GENES, BCL-2; NUCLEOSOMES; PERFUSION; PROGESTERONE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PSEUDOPREGNANCY; RABBITS; RNA PROBES;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0031657520     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod59.4.820     Document Type: Article

References (44)

1. Niswender GD, Nett TM. Corpus luteum and its control in infraprimate species. In: Knobil E, Neill JD (eds.), Physiology of Reproduction. New York: Raven Press; 1994: 781-816.
2. Bill II CH, Keyes PL. 17β-Estradiol maintains normal function of corpora lutea throughout pseudo-pregnancy in hypophysectomized rabbits. Biol Reprod 1983; 28:608-617.
3. Dharmarajan AM, Zanagnolo VL, Dasko LM, Zirkin BR, Ewing LL, Wallach EE. Estradiol regulation of the rabbit corpus luteum: in vivo and in vitro studies. Endocrinology 1991; 128:2678-2684.
4. Bender EM, Miller JB, Possley RM, Keyes PL. Steroidogenic effect of 17β-estradiol in the rabbit: stimulation of progesterone synthesis in prematurely regressing corpora lutea. Endocrinology 1978; 103:1937-1943.
5. Hesla JS, Miyazaki T, Dasko LM, Wallach EE, Dharmarajan AM. Superoxide activity, lipid peroxide production and corpus luteum steroidogenesis during natural luteolysis and regression induced by oestradiol deprivation of the ovary in pseudopregnant rabbits. J Reprod Fertil 1992; 95:915-924.
6. Bagavandos P, Wiggins RC, Kunkel SL, Remick DG, Keyes PL. Tumor necrosis factor production and accumulation of inflammatory cells in the corpus luteum of pseudopregnancy and pregnancy in rabbits. Biol Reprod 1990; 42:367-376.
7. Moutos D, Schryer B, Hurn P, Dharmarajan AM. Effect of exogenous oestrogen on blood flow and quantitative histology of the corpora lutea of the pseudopregnant rabbits. J Reprod Fertil 1995; 103:357-362.
8. ++ dependent endonuclease activity in rat granulosa and luteal cells. Endocrinology 1989; 125:2218-2220.
9. Hughes FM Jr, Gorospe WC. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991; 129: 2415-2422.
10. Tilly JL, Kowalski KI, Johnson AL, Hsueh AJW. Involvement of apoptosis in ovarian follicular atresia and postovulatorv regression. Endocrinology 1991; 129:2799-2801.
11. Tilly JL. Apoptosis and ovarian function. Rev Reprod 1996; 1:162-172.
12. Rueda BR, Wegner JA, Marion SL, Wahlen DD, Hoyer PB. Internucleosomal DNA fragmentation in ovine luteal tissue associated with luteolysis. In vivo and in vitro analysis. Biol Reprod 1995; 52:305-312.
13. Rueda BR, Tilly KI, Hansen TR, Hover PB, Tilly JL. Expression of Superoxide dismutase, catalase and glutathione peroxidase in the bovine corpus luteum: evidence supporting a role for oxidative stress in luteolysis. Endocrine 1995; 3:227-232.
14. Rueda BR, Tilly K, Botros IW, Jolly PD, Hansen TR, Hover PB, Tilly JL. Increased bax and interleukin-1β-converting enzyme (Ice) messenger ribonucleic acid levels coincide with apoptosis in the bovine corpus luteum during structural regression. Biol Reprod 1997; 56: 186-193.
15. Dharmarajan AM, Goodman SB, Tilly KI, Tilly JL. Apoptosis during functional corpus luteum regression: evidence of a role for chorionic gonadotropin in promoting luteal cell survival. Endocrine 1994; 2: 295-303.
16. Fraser HM, Lunn SF, Cowen GM, Illingworth PJ. Induced luteal regression in the primate: evidence for apoptosis and changes in c-myc protein. J Endocrinol 1995; 147:131-137.
17. Shikone T, Yamoto M, Kokawa 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.
18. Matsuyama S, Chang K-T, Kanuka H, Ohnishi M, Ikeda A, Nishihara M, Takahashi M. Occurrence of deoxyribonucleic acid fragmentation during prolactin induced structural luteolysis in cycling rats. Biol Reprod 1996; 54:1245-1251.
19. Dharmarajan AM, Goodman SB, Atiya N, Parkinson SP, Tilly JL. Role of apoptosis in functional luteolysis in the pregnant rabbit corpus luteum: evidence of a role for placental-derived factors in promoting luteal cell survival. In: Program of the 40th annual meeting of the Endocrine Society of Australia; 1997; Canberra, Australia. Abstract 35.
20. Yang E, Korsmeyer SJ. Molecular thanatopsis: a discourse on the BCL-2 family and cell death. Blood 1996; 88:386-401.
21. long messenger ribonucleic acid levels. Endocrinology 1995; 136:232-241.
22. Kugu K, Rails VS, Piquette GN, Tilly KI, Tao X-J, Martimbeau S, Aberdeen GW, Krajewski S, Reed JC, Pepe GJ, Albrecht ED, Tilly JL. Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 1998; 5:67-76.
23. Raits VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 1995; 136:3665-3668.
24. Knudson CM, Tung KSK, Tourtellotte WG, Brown GAJ, Korsmeyer SJ. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 1995; 270:96-99.
25. Perez GI, Knudson CM, Leykin L, Korsmeyer SJ, Tilly JL. Apoptosis-associated signaling pathways are required tor chemotherapy-mediated female germ cell destruction. Nat Med 1997; 3:1228-1232.
26. Tilly JL, Tilly KI, Perez GI, The genes of cell death and cellular susceptibility to apoptosis in the ovary: a hypothesis. Cell Death Differ 1997; 4:180-187.
27. Browning JY, Keyes PL, Wolfe RC. A comparison of serum progesterone 20α-dihydroprogesterone, and estradiol-17β in pregnant and pseudopregnant rabbits: evidence for post-implantation recognition of pregnancy. Biol Reprod 1980; 23:1014-1019.
28. Dharmarajan AM, Yoshimura Y, Sueoka K, Atlas SJ, Duhin NH, Zirkin BR, Ewing LL, Wallach EE. Progesterone secretion by the isolated perfused luteal ovary during pseudopregnancy in the rabbit. Biol Reprod 1988; 38:1137-1143.
29. Ahren K, Janson PO, Selstam G. Perfusion of ovaries in vitro and in vivo. Acat Endocrinol 1972; 158:285-309.
30. Gross-Bellard M, Oudet P, Chambon P. Isolation of high-molecularweight DNA from mammalian cells. Eur J Biochem 1973; 36:32-38.
31. Tilly JL, Hsueh AJW. Microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic DNA fragmentation. J Cell Physiol 1993; 154:519-526.
32. Gavrieli Y, Sherman Y, Ben-Sasson S. Identification of programmed cell death in situ via a specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119:493-501.
33. Tilly JL. Use of terminal transferase DNA labeling reaction for the biochemical and in situ analysis of apoptosis. In: Cells JE (ed.), Cell Biology: A Laboratory Handbook. San Diego: Academic Press; 1994: 330-337.
34. Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 1983; 132:6-13.
35. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-159.
36. Sridaran R, Hisheh S, Dharmarajan AM. Induction of apoptosis by a gonadotropin-releasing hormone agonist during early pregnancy in the rat. Apoptosis 1998; 3:51-57.
37. Tilly JL, Tilly KI. Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 1995; 136:242-252.
38. Wiltbank MC, Dysko RC, Gallagher KP, Keyes PL. Regulation of blood flow to the rabbit corpus luteum: effect of estradiol and human chorionic gonadotropin. Endocrinology 1989; 124:605-611.
39. Juengel JL, Garverick HA, Johnson AL, Youngquist RS, Smith ME. Apoptosis during luteal regression in cattle. Endocrinology 1993; 132: 249-254.
40. Murdoch WJ. Temporal relationship between stress protein induction, progesterone withdrawal, and apoptosis in corpora lutea of ewes treated with prostaglandin F2 alpha. J Anim Sci 1995; 73:1789-1792.
41. Holt JA. Regulation of progesterone production in the rabbit corpus luteum. Biol Reprod 1989; 40:201-208.
42. Miller JB, Keyes PL. Transition of the rabbit corpus luteum to estrogen dependence during early luteal development. Endocrinology 1978; 102:31-38.
43. Yuh K-CM, Keyes PL. Properties of nuclear and cytoplasmic estrogen receptor in the rabbit corpus luteum: evidence for translocation. Endocrinology 1979; 105:690-696.
44. Bagchi MK, Tsai M-J, O'Malley BW, Tsai SY. Analysis of the mechanism of steroid hormone receptor-dependent gene activation in cell-free systems. Endocr Rev 1992; 13:525-535.