Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells

Life Sciences

Volumn 89, Issue 9-10, 2011, Pages 295-303

  Chowdhury, Indrajit ^a   Branch, Alicia ^a   Olatinwo, Moshood ^a,b   Thomas, Kelwyn ^a   Matthews, Roland ^a   Thompson, Winston E ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b Summit ObGyn   (United States)

Author keywords

Apoptosis; Ceramide; Granulosa cells; Mitochondria; Prohibitin

Indexed keywords

CASPASE 3; CERAMIDE; CYTOCHROME C; PROHIBITIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEMALE; GRANULOSA CELL; NONHUMAN; OVARY FOLLICLE ATRESIA; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CASPASE 3; CELL CULTURE TECHNIQUES; CELL SURVIVAL; CELLS, CULTURED; CERAMIDES; CULTURE MEDIA, SERUM-FREE; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION; GRANULOSA CELLS; MICROSCOPY, PHASE-CONTRAST; MITOCHONDRIA; RATS; RATS, SPRAGUE-DAWLEY; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; TIME FACTORS;

ADENOVIRIDAE; RATTUS;

EID: 80051688824     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2011.06.022     Document Type: Article

References (49)

1. M. Artal-Sanz, W.Y. Tsang, E.M. Willems, L.A. Grivell, B.D. Lemire, and H. van der Spek The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans J Biol Chem 278 2003 32091 32099 (Pubitemid 37048398)
2. C. Bezombes, S. Grazide, C. Garret, C. Fabre, A. Quillet-Mary, and S. Müller Rituximab antiproliferative effect in B-lymphoma cells is associated with acid-sphingomyelinase activation in raft microdomains Blood 104 4 2004 1166 1173 (Pubitemid 39038039)
3. D.L. Boone, and B.K. Tsang Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression Biol Reprod 58 1998 1533 1539 (Pubitemid 28248772)
4. L.Y. Bourguignon, E. Gilad, and K. Peyrollier Heregulin-mediated ErbB2-ERK signaling activates hyaluronan synthases leading to CD44-dependent ovarian tumor cell growth and migration J Biol Chem 282 2007 19426 19441 (Pubitemid 47100114)
5. G.M. Cereghetti, and L. Scorrano The many shapes of mitochondrial death Oncogene 25 2006 4717 4724 (Pubitemid 44187621)
6. I. Chowdhury, B. Tharakan, and G.K. Bhat Current concepts in apoptosis: the physiological suicide program revisited Cell Mol Biol Lett 11 4 2006 506 525 (Pubitemid 46708878)
7. I. Chowdhury, W. Xu, J.K. Stiles, A. Zeleznik, X. Yao, and R. Matthews Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus-directed overexpression of prohibitin Endocrinology 148 1 2007 206 217 (Pubitemid 46021452)
8. I. Chowdhury, B. Tharakan, and G.K. Bhat Caspases-an update Comp Biochem Physiol B Biochem Mol Biol 151 1 2008 10 27
9. Chowdhury, I., Garcia-Barrio, M., Harp, H., Thomas, K., Matthews, R., Thompson, W.E. 2011. The emerging roles of prohibitins in folliculogenesis. Front. Biosci. (in press).
10. P.J. Coates, R. Nenutil, A. McGregor, S.M. Picksley, D.H. Crouch, and P.A. Hall Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence Exp Cell Res 265 2001 262 273 (Pubitemid 32980214)
11. J. Craig, M. Orisaka, H.M. Wang, S. Orisaka, W. Thompson, and C. Zhu Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death Front Biosci 12 2007 3628 3639
12. E. Eliyahu, N. Shtraizent, K. Martinuzzi, J. Barritt, X. He, and H. Wei Acid ceramidase improves the quality of oocytes and embryos and the outcome of in vitro fertilization FASEB J 24 4 2010 1229 1238
13. A. Gomez-Munez Modulation of cell signaling by ceramides Biochim Biophys Acta 1391 1998 92 109
14. A.J. Hsueh, H. Billig, and A. Tsafriri Ovarian follicle atresia: a hormonally controlled apoptotic process Endocr Rev 15 1994 707 724
15. M.R. Hussein Apoptosis in the ovary: molecular mechanisms Hum Reprod Update 11 2 2005 162 177
16. A. Kaipia, S.Y. Chun, K. Eisenhauer, and A.J. Hsueh Tumor necrosis factor-alpha and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles Endocrinology 137 11 1996 4864 4870 (Pubitemid 26403329)
17. M. Karabowski, and R.J. Youle Dynamics of mitochondrial morphology in healthy cells and during apoptosis Cell Death Differ 8 2003 870 880 (Pubitemid 36939697)
18. N. Karasavvas, R.K. Erukulla, R. Bittman, R. Lockshin, and Z. Zakeri Stereospecific induction of apoptosis in U937 cells by N-octonoyl-spingosine stereoisomers and N-octyl-spingosine. The ceramide amide group is not required for apoptosis Eur J Biochem 236 1996 729 737
19. K. Kasashima, E. Ohta, Y. Kagawa, and H. Endo Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2 J Biol Chem 281 2006 36401 36410 (Pubitemid 46041374)
20. J.H. Kim, J.S. Han, and Y.D. Yoon Biochemical and morphological identification of ceramide-induced cell cycle arrest and apoptosis in cultured granulosa cells Tissue Cell 31 6 1999 531 539
21. V. Kurtev, R. Margueron, K. Kroboth, E. Ogris, V. Cavailles, and C. Seiser Transcriptional regulation by the repressor of estrogen receptor activity via recruitment of histone deacetylases J Biol Chem 279 2004 24834 24843 (Pubitemid 38725351)
22. T. Matikainen, G.I. Perez, T.S. Zheng, T.R. Kluzak, B.R. Rueda, and R.A. Flavell Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary Endocrinology 142 2001 2468 2480 (Pubitemid 32473103)
23. F. Matsuda-Minehata, N. Inoue, Y. Goto, and N. Manabe The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules J Reprod Dev 52 6 2006 695 705 (Pubitemid 46150826)
24. S. Mishra, L.C. Murphy, and L.J. Murphy The prohibitins: emerging roles in diverse functions J Cell Mol Med 10 2 2005 353 363
25. Y. Morita, G.I. Perez, F. Paris, S.R. Miranda, D. Ehleiter, and A. Haimovitz-Friedman Oocyte apoptosis is suppressed by disruption of the acid spingomyelinase gene or by spingosine-1-phosphate pathway Nat Med 6 2000 1109 1114
26. L.G. Nijtmans, L. de Jong, M. Artal Sanz, P.J. Coates, J.A. Berden, and J.W. Back Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins EMBO J 19 2000 2444 2451 (Pubitemid 30323534)
27. L.G.J. Nijtmans, M. Artal Sanz, L.A. Grivell, and P.J. Coates The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, aging and degenerative disease CMLS Cell Mol Life Sci 59 2002 143 155 (Pubitemid 34117362)
28. L.M. Obeid, and Y.A. Hannun Ceramide: a stress signal and mediator of growth suppression and apoptosis J Cell Biochem 58 2 1995 191 198
29. L.M. Obeid, C.M. Linardic, L.A. Karolak, and Y.A. Hannun Programmed cell death induced by ceramide Science 259 5102 1993 1769 1771 (Pubitemid 23114667)
30. S. Pandey, R.F. Murphy, and D.K. Agrawal Recent advances in the immunobiology of ceramide Exp Mol Biol 82 3 2006 298 309 (Pubitemid 46686655)
31. G.I. Perez, A. Jurisicova, T. Matikainen, T. Moriyama, M.R. Kim, and Y. Takai A central role of ceramide in the age-related acelaration of apoptosis in the female germline FASEB J 19 2005 860 862 (Pubitemid 40617409)
32. R. Robles, X.J. Tao, A.M. Trbovich, D.V. Maravel, R. Nahum, and G.I. Perez Localization, regulation and possible consequences of apoptotic protease-activating factor-1 (Apaf-1) expression in granulosa cells of the mouse ovary Endocrinology 140 1999 2641 2644 (Pubitemid 32245142)
33. P. Santana, L. Llanes, I. Hernandez, G. Gallardo, J. Quintana, and J. Gonzalez Ceramide mediates tumor necrosis factor effects on P450-aromatase activity in cultured granulosa cells Endocrinology 136 5 1995 2345 2348
34. H. Sasaki, Y. Sheng, F. Kotsuji, and B.K. Tsang Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells Cancer Res 60 2000 5659 5666
35. R. Shao, E. Markstrom, P.A. Friberg, M. Johansson, and H. Billig Expression of progesterone receptor (PR) A and B isoforms in mouse granulosa cells: stage-dependent PRs-mediated regulation of apoptosis and cell proliferation Biol Reprod 68 2003 914 921 (Pubitemid 36245836)
36. C. Sheridan, P. Delivani, S.P. Cullen, and S.J. Martin Bax- or Bak-induced mitochondrial fission can be uncoupled from cytochrome C release Mol Cell 31 4 2008 570 585
37. J.P. Somers, J.A. DeLoia, and A.J. Zeleznik Adenovirus-directed expression of a nonphosphorylatable mutant of CREB (cAMP response element-binding protein) adversely affects the survival, but not the differentiation, of rat granulosa cells Mol Endocrinol 13 1999 1364 1372 (Pubitemid 30645292)
38. P. Sutovsky, R.D. Moreno, J. Ramalho-Santos, T. Dominko, C. Simerly, and G. Schatten Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos Biol Reprod 63 2000 582 590 (Pubitemid 30639950)
39. Y. Takai, J. Canning, G.I. Perez, J.K. Pru, J.J. Schlezinger, and D.H. Sherr Bax, caspase-2, and caspase-3 are required for ovarian follicle loss caused by 4-vinylcyclohexene diepoxide exposure of female mice in vivo Endocrinology 144 1 2003 69 74 (Pubitemid 36076094)
40. T. Tatsuta, K. Model, and T. Langer Formation of membrane-bound ring complexes by prohibitins in mitochondria Mol Biol Cell 16 2005 248 259 (Pubitemid 40024307)
41. W.E. Thompson, A. Sanbuissho, G.Y. Lee, and E. Anderson Steroidogenic acute regulatory (StAR) protein (p25) and prohibitin (p28) from cultured rat ovarian granulosa cells J Reprod Fertil 109 1997 337 348
42. W.E. Thompson, J.M. Powell, J.A. Whittaker, R. Sridaran, and K.H. Thomas Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries Anat Rec 256 1999 40 48 (Pubitemid 29402665)
43. W.E. Thompson, A. Branch, J.A. Whittaker, D. Lyn, M. Zilberstein, and K.E. Mayo Characterization of prohibitin in a newly established rat ovarian granulosa cell line Endocrinology 142 2001 4076 4085 (Pubitemid 32807700)
44. W.E. Thompson, E. Asselin, A. Branch, J.K. Stiles, P. Sutovsky, and L. Lai Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary Biol Reprod 71 2004 282 290 (Pubitemid 38915335)
45. M.G. Vander Heiden, J.S. Choy, D.J. VanderWeele, J.L. Brace, M.H. Harris, and D.E. Bauer Bcl-xL complements Saccharomyces cerevisiae genes that facilitate the switch from glycolytic to oxidative metabolism J Biol Chem 277 2002 44870 44876 (Pubitemid 36159082)
46. M.E. Venable, Y.L. Lee, M.J. Smith, A. Bielawska, and L.M. Obeid Role of ceramide in senescence J Biol Chem 67 1995 27 38
47. A.W. Whitehurst, B.O. Bodemann, J. Cardenas, D. Ferguson, L. Girard, and M. Peyton Synthetic lethal screen identification of chemosensitizer loci in cancer cells Nature 446 2007 815 819 (Pubitemid 46582032)
48. J.P. Witty, J.T. Bridgham, and A.L. Johnson Induction of apoptotic cell death in hen granulosa cells by ceramide Endocrinology 137 1996 5269 5277 (Pubitemid 26423084)
49. S. Zao, Y.A. Yang, and J.G. Song Ceramide induces caspase-dependent and independent apoptosis in A-431 cells J Cell Physiol 199 2004 47 56