Activity and expression of different members of the caspase family in the rat corpus luteum during pregnancy and postpartum

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 5, 2007, Pages

  Peluffo, Marina C ^a   Stouffer, Richard L ^a,b   Tesone, Marta ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Apoptosis; Luteolysis

Indexed keywords

CASPASE 2; CASPASE 3; CASPASE 8; CASPASE 9; PROSTAGLANDIN F2 ALPHA; STEROID HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SIZE; CONTROLLED STUDY; CORPUS LUTEUM; ENZYME ACTIVITY; ENZYME DEGRADATION; FEMALE; GESTATIONAL AGE; HORMONE SYNTHESIS; IMMUNOHISTOCHEMISTRY; LUTEAL CELL; LUTEOLYSIS; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PUERPERIUM; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

EID: 36148935569     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00261.2007     Document Type: Article

References (73)

1. Abdo M, Hisheh S, Dharmarajan A. Role of tumor necrosis factor-alpha and the modulating effect of the caspases in rat corpus luteum apoptosis. Biol Reprod 68: 1241-1248, 2003.
2. Ahmad M, Srinivasula SM, Wang L, Talanian RV, Litwack G, Fernandes-Alnemri T, Alnemri ES. CRADD, a novel human apoptotic adaptor molecule for caspase-2, and FasL/tumor necrosis factor receptor-interacting protein RIP. Cancer Res 57: 615-619, 1997.
3. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J. Human ICE/CED-3 protease nomenclature. Cell 87: 171, 1996.
4. Andreu C, Parborell F, Vanzulli S, Chemes H, Tesone M. Regulation of follicular luteinization by a gonadotropin-releasing hormone agonist: relationship between steroidogenesis and apoptosis. Mol Reprod Dev 51: 287-294, 1998.
5. Bacci ML, Barazzoni AM, Forni M, Costerbosa GL. In situ detection of apoptosis in regressing corpus luteum of pregnant sow: evidence of an early presence of DNA fragmentation. Domest Anim Endocrinol 13: 361-372, 1996.
6. Bergeron L, Perez GI, Macdonald G, Shi L, Sun Y, Jurisicova A, Varmuza S, Latham KE, Flaws JA, Salter JC, Hara H, Moskowitz MA, Li E, Greenberg A, Tilly JL, Yuan J. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 12: 1304-1314, 1998.
7. Boone DL, Tsang BK. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol Reprod 58: 1533-1539, 1998.
8. Bowen J, Keyes P, Warren J, Townson D. Prolactin-induced regression of the rat corpus luteum: expression of monocyte chemoattractant protein-1 and invasion of macrophages. Biol Reprod 54: 1120-1127, 1996.
9. Bowen-Shauver JM, Gibori G. The corpus luteum of pregnancy. In: The Ovary, edited by Leung PCK and Adashi EY. San Diego, CA: Elseiver/ Academic, 2004, p. 201-230.
10. Brannstrom M, Giesecke L, Moore IC, van den Heuvel CJ, Robertson SA. Leukocyte subpopulations in the rat corpus luteum during pregnancy and pseudopregnancy. Biol Reprod 50: 1161-1167, 1994.
11. Carambula SF, Matikainen T, Lynch MP, Flavell RA, Goncalves PB, Rueda BR. Caspase-3 is a pivotal mediator of apoptosis during regression of the ovarian corpus luteum. Endocrinology 143: 1495-1501, 2002.
12. Carambula SF, Pru JK, Lynch MP, Matikainen T, Goncalves PB, Flavell RA, Tilly JL, Rueda BR. Prostaglandin F2alpha- and FAS-activating antibody-induced regression of the corpus luteum involves caspase-8 and is defective in caspase-3 deficient mice. Reprod Biol Endocrinol 1: 15, 2003.
13. Caulin C, Salvesen GS, Oshima RG. Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis. J Cell Biol 138: 1379-1394, 1997.
14. Colles SM, Woodford JK, Moncecchi D, Myers-Payne SC, McLean LR, Billheimer JT, Schroeder F. Cholesterol interaction with recombinant human sterol carrier protein-2. Lipids 30: 795-803, 1995.
15. Curlewis JD, Tam SP, Lau P, Kusters DH, Barclay JL, Anderson ST, Waters MJ. A prostaglandin f(2alpha) analog induces suppressors of cytokine signaling-3 expression in the corpus luteum of the pregnant rat: a potential new mechanism in luteolysis. Endocrinology 143: 3984-3993, 2002.
16. Davis JS, Rueda BR. The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci 7: 1978, 2002.
17. Dimmeler S, Haendeler J, Galle J, Zeiher AM. Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases. A mechanistic clue to the "response to injury" hypothesis. Circulation 95: 1760-1763, 1997.
18. Duan H, Dixit VM. RAIDD is a new "death" adaptor molecule. Nature 385: 86-89, 1997.
19. Friedman A, Weiss S, Levy N, Meidan R. Role of tumor necrosis factor alpha and its type I receptor in luteal regression: induction of programmed cell death in bovine corpus luteum-derived endothelial cells. Biol Reprod 63: 1905-1912, 2000.
20. Gaytan F, Bellido C, Morales C, Sanchez-Criado JE. Both prolactin and progesterone in proestrus are necessary for the induction of apoptosis in the regressing corpus luteum of the rat. Biol Reprod 59: 1200-1206, 1998.
21. Gaytan F, Morales C, Bellido C, Aguilar E, Sanchez-Criado JE. Role of prolactin in the regulation of macrophages and in the proliferative activity of vascular cells in newly formed and regressing rat corpora lutea. Biol Reprod 57: 478-486, 1997.
22. Gaytan F, Morales C, Bellido C, Aguilar R, Millan Y, Martin De Las Mulas J, Sanchez-Criado JE. Progesterone on an oestrogen background enhances prolactin-induced apoptosis in regressing corpora lutea in the cyclic rat: possible involvement of luteal endothelial cell progesterone receptors. J Endocrinol 165: 715-724, 2000.
23. Goodman SB, Kugu K, Chen SH, Preutthipan S, Tilly KI, Tilly JL, Dharmarajan AM. 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. Biol Reprod 59: 820-827, 1998.
24. Goyeneche AA, Deis RP, Gibori G, Telleria CM. Progesterone promotes survival of the rat corpus luteum in the absence of cognate receptors. Biol Reprod 68: 151-158, 2003.
25. Goyeneche AA, Harmon JM, Telleria CM. Cell death induced by serum deprivation in luteal cells involves the intrinsic pathway of apoptosis. Reproduction 131: 103-111, 2006.
26. Goyeneche AA, Martinez IL, Deis RP, Gibori G, Telleria CM. In vivo hormonal environment leads to differential susceptibility of the corpus luteum to apoptosis in vitro. Biol Reprod 68: 2322-2330, 2003.
27. Guo K, Wolf V, Dharmarajan AM, Feng Z, Bielke W, Saurer S, Friis R. Apoptosis-associated gene expression in the corpus luteum of the rat. Biol Reprod 58: 739-746, 1998.
28. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 277: 13430-13437, 2002.
29. Hasumoto K, Sugimoto Y, Yamasaki A, Morimoto K, Kakizuka A, Negishi M, Ichikawa A. Association of expression of mRNA encoding the PGF2 alpha receptor with luteal cell apoptosis in ovaries of pseudo-pregnant mice. J Reprod Fertil 109: 45-51, 1997.
30. Hehnke KE, Christenson LK, Ford SP, Taylor M. Macrophage infiltration into the porcine corpus luteum during prostaglandin F2 alpha-induced luteolysis. Biol Reprod 50: 10-15, 1994.
31. Irusta G, Parborell F, Peluffo M, Manna PR, Gonzalez-Calvar SI, Calandra R, Stocco DM, Tesone M. Steroidogenic acute regulatory protein in ovarian follicles of gonadotropin-stimulated rats is regulated by a gonadotropin-releasing hormone agonist. Biol Reprod 68: 1577-1583, 2003.
32. Kuranaga E, Kanuka H, Bannai M, Suzuki M, Nishihara M, Takahashi M. 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, 1999.
33. Martin SJ, Green DR. Protease activation during apoptosis: death by a thousand cuts? Cell 82: 349-352, 1995.
34. Matikainen T, Perez GI, Zheng TS, Kluzak TR, Rueda BR, Flavell RA, Tilly JL. Capase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology 142: 2468-2480, 2001.
35. Matsuyama S, Chang KT, 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 54: 1245-1251, 1996.
36. McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event. Physiol Rev 79: 263-323, 1999.
37. McGuire WJ, Juengel JL, Niswender GD. Protein kinase C second messenger system mediates the antisteroidogenic effects of prostaglandin F2 alpha in the ovine corpus luteum in vivo. Biol Reprod 51: 800-806, 1994.
38. Nackley AC, Shea-Eaton W, Lopez D, McLean MP. Repression of the steroidogenic acute regulatory gene by the multifunctional transcription factor Yin Yang 1. Endocrinology 143: 1085-1096, 2002.
39. Naftalin DM, Bove SE, Keyes PL, Townson DH. Estrogen withdrawal induces macrophage invasion in the rabbit corpus luteum. Biol Reprod 56: 1175-1180, 1997.
40. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 6: 1028-1042, 1999.
41. Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW. Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 80: 1-29, 2000.
42. Okuda K, Korzekwa A, Shibaya M, Murakami S, Nishimura R, Tsubouchi M, Woclawek-Potocka I, Skarzynski DJ. Progesterone is a suppressor of apoptosis in bovine luteal cells. Biol Reprod 71: 2065-2071, 2004.
43. Olson KK, Anderson LE, Wiltbank MC, Townson DH. Actions of prostaglandin F2alpha and prolactin on intercellular adhesion molecule-1 expression and monocyte/macrophage accumulation in the rat corpus luteum. Biol Reprod 64: 890-897, 2001.
44. Papadopoulos V, Dharmarajan AM, Li H, Culty M, Lemay M, Sridaran R. Mitochondrial peripheral-type benzodiazepine receptor expression. Correlation with gonadotropin-releasing hormone (GnRH) agonist-induced apoptosis in the corpus luteum. Biochem Pharmacol 58: 1389-1393, 1999.
45. Pate JL. Cellular components involved in luteolysis. J Anim Sci 72: 1884-1890, 1994.
46. Pate JL. Involvement of immune cells in regulation of ovarian function. J Reprod Fertil Suppl 49: 365-377, 1995.
47. Peluffo MC, Bussmann L, Stouffer RL, Tesone M. Expression of caspase-2, -3, -8 and -9 proteins and enzyme activity in the corpus luteum of the rat at different stages during the natural estrous cycle. Reproduction 132: 465-475, 2006.
48. Peluffo MC, Young KA, Stouffer RL. Dynamic expression of caspase-2, -3, -8, and -9 proteins and enzyme activity, but not messenger ribonucleic acid, in the monkey corpus luteum during the menstrual cycle. J Clin Endocrinol Metab 90: 2327-2335, 2005.
49. Pharriss B. Prostaglandin induction of luteolysis. Ann NY Acad Sci 180: 436-444, 1971.
50. Pharriss BB, Tillson SA, Erickson RR. Prostaglandins in luteal function. Recent Prog Horm Res 28: 51-89, 1972.
51. Pharriss BB, Wyngarden LJ. The effect of prostaglandin F 2alpha on the progestogen content of ovaries from pseudopregnant rats. Proc Soc Exp Biol Med 130: 92-94, 1969.
52. Pru JK, Lynch MP, Davis JS, Rueda BR. Signaling mechanisms in tumor necrosis factor alpha-induced death of microvascular endothelial cells of the corpus luteum. Reprod Biol Endocrinol 1: 17, 2003.
53. Rueda BR, Hendry IR, Tilly JL, Hamernik DL. Accumulation of caspase-3 messenger ribonucleic acid and induction of caspase activity in the ovine corpus luteum following prostaglandin F2alpha treatment in vivo. Biol Reprod 60: 1087-1092, 1999.
54. Rueda BR, Tilly KI, Botros IW, Jolly PD, Hansen TR, Hoyer PB, Tilly JL. Increased bax and interleukin-1beta-converting enzyme messenger ribonucleic acid levels coincide with apoptosis in the bovine corpus luteum during structural regression. Biol Reprod 56: 186-193, 1997.
55. Sandhoff TW, McLean MP. Repression of the rat steroidogenic acute regulatory (StAR) protein gene by PGF2alpha is modulated by the negative transcription factor DAX-1. Endocrine 10: 83-91, 1999.
56. Saragueta PE, Lanuza GM, Baranao JL. Inhibitory effect of gonadotrophin-releasing hormone (GnRH) on rat granulosa cell deoxyribonucleic acid synthesis. Mol Reprod Dev 47: 170-174, 1997.
57. Siegel RM. Caspases at the crossroads of immune-cell life and death. Nat Rev Immunol 6: 308-317, 2006.
58. Stocco C, Callegari E, Gibori G. Opposite effect of prolactin and prostaglandin F(2 alpha) on the expression of luteal genes as revealed by rat cDNA expression array. Endocrinology 142: 4158-4161, 2001.
59. Stocco C, Telleria C, Gibori G. The molecular control of corpus luteum formation, function and regression. Endocr Rev 28: 117-149, 2007.
60. Stocco CO, Zhong L, Sugimoto Y, Ichikawa A, Lau LF, Gibori G. Prostaglandin F2alpha-induced expression of 20alpha-hydroxysteroid dehydrogenase involves the transcription factor NUR77. J Biol Chem 275: 37202-37211, 2000.
61. Stouffer RL. The function and regulation of cell populations comprising the corpus luteum during the ovarian cycle. In: The Ovary, edited by Leung PCK and Adashi EY. San Diego, CA: Elsevier/Academic, 2004, p. 169-184.
62. Strauss JF 3rd, Sokoloski J, Caploe P, Duffy P, Mintz G, Stambaugh RL. On the role of prostaglandins in parturition in the rat. Endocrinology 96: 1040-1043, 1975.
63. Svensson EC, Markstrom E, Shao R, Andersson M, Billig H. Progesterone receptor antagonists Org 31710 and RU 486 increase apoptosis in human periovulatory granulosa cells. Fertil Steril 76: 1225-1231, 2001.
64. Takiguchi S, Sugino N, Esato K, Karube-Harada A, Sakata A, Nakamura Y, Ishikawa H, Kato H. Differential regulation of apoptosis in the corpus luteum of pregnancy and newly formed corpus luteum after parturition in rats. Biol Reprod 70: 313-318, 2004.
65. Telleria CM, Goyeneche AA, Cavicchia JC, Stati AO, Deis RP. Apoptosis induced by antigestagen RU486 in rat corpus luteum of pregnancy. Endocrine 15: 147-155, 2001.
66. Telleria CM, Parmer TG, Zhong L, Clarke DL, Albarracin CT, Duan WR, Linzer DI, Gibori G. The different forms of the prolactin receptor in the rat corpus luteum: developmental expression and hormonal regulation in pregnancy. Endocrinology 138: 4812-4820, 1997.
67. Telleria CM, Stocco CO, Stati AO, Deis RP. Progesterone receptor is not required for progesterone action in the rat corpus luteum of pregnancy. Steroids 64: 760-766, 1999.
68. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81: 801-809, 1995.
69. Tilly JL, Pru JK, Rueda BR. Apoptosis in ovarian development, function, and failure. In: The Ovary, edited by Leung PCK and Adashi EY. San Diego, CA: Elsevier/Academic, 2004, p. 321-352.
70. Townson DH, O'Connor CL, Pru JK. Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod 66: 361-366, 2002.
71. Townson DH, Warren JS, Flory CM, Naftalin DM, Keyes PL. Expression of monocyte chemoattractant protein-1 in the corpus luteum of the rat. Biol Reprod 54: 513-520, 1996.
72. Villavicencio A, Iniguez G, Johnson MC, Gabler F, Palomino A, Vega M. Regulation of steroid synthesis and apoptosis by insulin-like growth factor I and insulin-like growth factor binding protein 3 in human corpus luteum during the midluteal phase. Reproduction 124: 501-508, 2002.
73. Yadav VK, Lakshmi G, Medhamurthy R. Prostaglandin F2alpha-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis: involvement of caspase-activated DNase. J Biol Chem 280: 10357-10367, 2005.