Bid and Bax are involved in granulosa cell apoptosis during follicular atresia in porcine ovaries

Journal of Reproduction and Development

Volumn 57, Issue 3, 2011, Pages 421-427

  Sai, Takafumi ^a   Goto, Yasufumi ^a   Yoshioka, Ryousuke ^a   Maeda, Akihisa ^a   Matsuda, Fuko ^a   Sugimoto, Miki ^b   Wongpanit, Kannika ^a   Jin, Hua Zi ^a   Li, Jun You ^a   Manabe, Noboru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Bcl 2 associated x protein (Bax); BH3 interacting domain death agonist (Bid); Follicular atresia; Mitochondrion dependent type II apoptotic cell; Pig ovary

Indexed keywords

PROTEIN BAX; PROTEIN BID;

ANIMAL; APOPTOSIS; ARTICLE; FEMALE; GRANULOSA CELL; METABOLISM; OVARY; OVARY FOLLICLE ATRESIA; PHYSIOLOGY; SIGNAL TRANSDUCTION; SWINE;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; FEMALE; FOLLICULAR ATRESIA; GRANULOSA CELLS; OVARY; SIGNAL TRANSDUCTION; SWINE;

SUIDAE; SUS;

EID: 79960117704     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.11-007H     Document Type: Article

References (55)

1. Kaipia A, Hsueh AJ. Regulation of ovarian follicle atresia. Annu Rev Physiol 1997; 59: 349-363.
2. Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, Miyano T. Regulation mechanism of selective atresia in porcine follicles: Regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004; 50: 493-514.
3. Manabe N, Inoue N, Miyano T, Sakamaki K, Sugimoto M, Miyamoto H. Ovarian follicle selection in mammalian ovaries. In: Leung PK, Adashi E (eds.), The Ovary 2nd ed. Amsterdam, Academic Press; 2003: 369-385.
4. Matsuda F, Inoue N, Goto Y, Manabe N. The regulation of ovarian granulosa cell death by pro- and antiapoptotic molecules. J Reprod Dev 2006; 52: 695-705.
5. Manabe N, Matsuda F, Goto Y, Maeda A, Cheng Y, Nakagawa N, Inoue N, Wongpanit K, Jin H, Gonda H, Li J. Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Dom Anim 2008; 43: 268-272.
6. Matsuda F, Maeda A, Cheng Y, Sai T, Gonda H, Goto Y, Manabe N. Regulation of granulosa cell apoptosis by death ligand-receptor signaling. Anim Sci J 2008; 7: 1-10.
7. 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.
8. Sugimoto M, Manabe N, Kimura Y, Myomoto A, Imai Y, Ohno H, Miyamoto H. Ultrastructural changes in granulosa cells in porcine antral follicles undergoing atresia indicate apoptotic cell death. J Reprod Dev 2000; 46: 325-334.
9. Nagata S. Apoptosis by death factor. Cell 1997; 88: 355-365.
10. Ashkenzaki A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281: 1305-1308.
11. Thorburn A. Death receptor-induced cell killing. Cell Signal 2004; 16: 139-144.
12. Cohen GM. Caspases: The executioners of apoptosis. Biochem J 1997; 15: 1-16.
13. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, Debatin KM, Krammer PH, Peter ME. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998; 16: 1675-1687.
14. Hangertrner MO. The biochemistry of apoptosis. Nature 2000; 407: 770-776.
15. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004; 5: 897-907.
16. Danial NN, Korsmeyer SJ. Cell death: Critical control points. Cell 2004; 116: 205-219.
17. Yan N, Shi Y. Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 2005; 21: 35-56.
18. Fulda S, Pervaiz S. Apoptosis signaling in cancer stem cells. Int J Biochem Cell Biol 2010; 42: 31-38.
19. Barnhart BC, Alappat EC, Peter ME. The CD95 type I/type II model. Semin Immunol 2003; 15: 185-193.
20. Yin XM. Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Research 2000; 10: 161-167.
21. Yao Y, Bobkov AA, Plesniak LA, Marassi FM. Mapping the interaction of proapoptotic tBid with pro-survival Bcl-XL. Biochemistry 2009; 48: 8704-8711.
22. Schafer B, Quispe J, Choudhary V, Chipuk JE, Ajero TG, Du H, Schneiter R, Kuwana T. Mitochondrial outer membrane proteins assist Bid in Bax-mediated lipidic pore formation. Mol Biol Cell 2009; 20: 2276-2285.
23. Ott M, Norberg E, Zhivotovsky B, Orrenius S. Mitochondrial targeting of tBid/Bax: A role for the Tom complex? Cell Death Differ 2009; 16: 1075-1082.
24. Tomicic MJ, Christmann M, Kaina B. Topotecan triggers apoptosis in p53-deficient cells by forcing degradation of XIAP and survivin thereby activating caspase-3-mediated Bid cleavage. J Pharmacol Exp Ther 2010; 332: 316-325.
25. Goncharenko-Khaider N, Lane D, Matte I, Rancourt C, Piché A. The inhibition of Bid expression by Akt leads to resistance to TRAIL-induced apoptosis in ovarian cancer cells. Oncogene 2010; 29: 1-14.
26. Zaltsman Y, Shachnai L, Yivgi-Ohana N, Schwarz M, Maryanovich M, Houtkooper RH, Vaz FM, De Leonardis F, Fiermonte G, Palmieri F, Gillissen B, Daniel PT, Jimenez E, Walsh S, Koehler CM, Roy SS, Walter L, Hajnóczky G, Gross A. Mtch2/ Mimp is a major facilitator of tBid recruitment to mitochondria. Nat Cell Biol 2010; 12: 553-562.
27. Miyashita T, Kitada S, Krajewski S, Horne WA, Delia D, Reed JC. Overexpression of the Bcl-2 protein increases the half-life of p21 Bax. J Biol Chem 1995; 270: 26049-26052.
28. Antonsson B. Bax and other proapoptotic Bcl-2 family "killer-proteins" and their victim the mitochondrion. Cell Tissue Res 2001; 306: 347-361.
29. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The Bcl-2 family reunion. Mol Cell 2010; 37: 299-310.
30. Crompton M. Mitochondrial intermembrane junctional complexes and their role in cell death. J Physiol 2000; 529: 11-21.
31. Wang C, Youle RJ. The role of mitochondria in apoptosis. Annu Rev Genet 2009; 43: 95-118.
32. Jourdaina A, Martinou JC. Mitochondrial outer-membrane permeabilization and remodelling in apoptosis. Int J Biochem Cell Biol 2009; 41: 1884-1889.
33. Galluzzi L, Blomgren K, Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 2009; 10: 481-494.
34. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans Ced-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997; 90: 405-413.
35. Robles R, Tao XJ, Trbovich AM, Maravel DV, Nahum R, Perez GI, Tilly KI, Tilly JL. 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.
36. Goto Y, Matsuda-Minehata F, Inoue N, Matsui T, Maeda A, Manabe N. Porcine (Sus scrofa) Cellular FLICE-like inhibitory protein (cFLIP): Molecular cloning and comparison with the human and murine cFLIP. J Reprod Dev 2004; 50: 549-555.
37. Matsuda F, Goto Y, Inoue N, Sakamaki K, Chedrese PJ, Manabe N. Antiapoptotic activity of porcine cFLIP in ovarian granulosa cell lines. Mol Reprod Dev 2007; 73: 1165-1170.
38. Matsuda F, Inoue N, Goto Y, Maeda A, Cheng Y, Sakamaki K, Manabe N. cFLIP regulates death receptor-mediated apoptosis in an ovarian granulosa cell line by inhibiting procaspase-8 cleavage. J Reprod Dev 2008; 54: 314-320.
39. Hojo T, Al-Zi'abi MO, Komiyama J, Manabe N, Acosta TJ, Okuda K. Expression and localization of cFLIP, an antiapoptotic factor, in the bovine corpus luteum. J Reprod Dev 2010; 56: 230-235.
40. Cheng Y, Maeda A, Goto Y, Matsuda F, Miyano T, Manabe N. Changes in expression and localization of X-linked inhibitor of apoptosis protein (XIAP) in follicular granulosa cells during atresia in porcine ovaries. J Reprod Dev 2008; 54: 454-459.
41. Matsui T, Manabe N, Goto Y, Inoue N, Nishihara S, Miyamoto H. Expression and activity of Apaf1 and caspase-9 in granulosa cells during follicular atresia in pig ovaries. Reproduction 2003; 126: 113-120.
42. Inoue N, Maeda A, Matsuda F, Fukuta K, Manabe N. Changes in expression levels and localization of Fas ligand and Fas during atresia in porcine ovarian follicles. J Reprod Dev 2006; 52: 723-730.
43. Maeda A, Goto Y, Matsuda F, Cheng Y, Inoue N, Manabe N. Changes in expression of interleukin-6 receptors in granulosa cells during follicular atresia in pig ovaries. J Reprod Dev 2007; 53: 481-490.
44. Maeda A, Matsuda F, Cheng Y, Inoue N, Manabe N. The role of interleukin-6 in the regulation of granulosa cell apoptosis during follicular atresia in pig ovaries. J Reprod Dev 2007; 53: 727-736.
45. Sugimoto M, Kagawa N, Morita M, Kume S, Wongpanit K, Jin H, Manabe N. Changes in the expression of decoy receptor 3 (DcR3) in granulosa cells during atresia in porcine ovaries. J Reprod Dev 2010; 56: 467-474.
46. Guthrie HD, Cooper BS, Welch GR, Zakaria AD, Johnson LA. 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.
47. Inoue N, Matsuda F, Goto Y, Sakamaki K, Manabe N. Molecular characteristics of porcine Fas-associated death domain (FADD) and procaspase-8. J Reprod Dev 2007; 53: 427-436.
48. Cheng Y, Maeda A, Goto Y, Matsuda F, Manabe N. Molecular cloning of porcine (Sus scrofa) tumor necrosis factor receptor 2. J Reprod Dev 2007; 53: 1291-1297.
49. Maeda A, Matsuda F, Goto Y, Cheng Y, Gonda H, Inoue N, Nakagawa S, Manabe N. Molecular cloning of a porcine (Sus scrofa) apoptosis inhibitory ligand, Netrin-1, and its receptor, p53RDL1. J Reprod Dev 2008; 54: 275-280.
50. Tomicic MT, Friedrichs C, Christmann M, Wutzler P, Thust R, Kaina B. Apoptosis induced by (E)-5-(2-bromovinyl)-2'-deoxyuridine in varicella zoster virus thymidine kinase-expressing cells is driven by activation of c-Jun/activator protein-1 and Fas ligand/caspase-8. Mol Pharmacol 2003; 63: 439-449.
51. Goyeneche AA, Harmon JM, Telleria CM. Cell death induced by serum deprivation in luteal cells involves the intrinsic pathway of apoptosis. Reproduction 2006; 131: 103-111.
52. Slot KA, Voorendt M, Boer-Brouwer M, Vugt HH, Teerds KJ. Estrous cycle dependent changes in expression and distribution of Fas, Fas ligand, Bcl-2, Bax, and proand active-caspase-3 in the rat ovary. J Endocrinol 2006; 188: 179-192.
53. Puthalakath H, Strasser A. Keeping killers on a tight leash: Transcriptional and posttranslational control of the proapoptotic activity of BH3-only proteins. Cell Death Differ 2002; 9: 505-512.
54. Yadav VK, Lakshmi G, Medhamurthy R. Prostaglandin F2-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis. J Biol Chem 2005; 280: 10357-10367.
55. Lea RG, Andrade LP, Rae MT, Hannah LT, Kyle CE, Murray JF, Rhind SM, Miller DW. Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary. Reproduction 2006; 131: 113-124.