Follicular stage-dependent regulation of apoptosis and steroidogenesis by prohibitin in rat granulosa cells

Journal of Ovarian Research

Volumn 6, Issue 1, 2013, Pages

  Wang, Qi ^a,b   Leader, Arthur ^a,b,c   Tsang, Benjamin K ^a,b,d  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c Ottawa Fertility Centre   (Canada)

^d Seoul National University   (South Korea)

Author keywords

Apoptosis; Prohibitin; Steroidogenesis

Indexed keywords

CASPASE 3; ESTRADIOL; GONADOTROPIN; PROGESTERONE; PROHIBITIN; PROTEIN KINASE B; STAUROSPORINE;

ADENOVIRUS INFECTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; FEMALE; GRANULOSA CELL; LOSS OF FUNCTION MUTATION; NONHUMAN; OVARY FOLLICLE; OVARY FOLLICLE MATURATION; OVARY INSUFFICIENCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS;

EID: 84875837088     PISSN: None     EISSN: 17572215     Source Type: Journal    
DOI: 10.1186/1757-2215-6-23     Document Type: Article

References (55)

1. Initial and cyclic recruitment of ovarian follicles. McGee EA, Hsueh AJ, Endocr Rev 2000 21 200 214 10.1210/er.21.2.200 10782364 (Pubitemid 32275595)
2. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Craig J, Orisaka M, Wang H, Orisaka S, Thompson W, Zhu C, Kotsuji F, Tsang BK, Front Biosci 2007 12 3628 3639 10.2741/2339 17485326
3. Actions of epidermal growth factor receptor/mitogen-activated protein kinase and protein kinase C signaling in granulosa cells from Gallus gallus are dependent upon stage of differentiation. Woods DC, Haugen MJ, Johnson AL, Biol Reprod 2007 77 61 70 10.1095/biolreprod.106.059394 17409374 (Pubitemid 46986397)
4. Hormonal control of gene expression in the ovary. Richards JS, Endocr Rev 1994 15 725 751 7705279
5. The role of prohibitin in cell signaling. Mishra S, Ande SR, Nyomba BL, FEBS J 2010 277 3937 3946 10.1111/j.1742-4658.2010.07809.x 20840588
6. Prohibitin: a potential target for new therapeutics. Mishra S, Murphy LC, Nyomba BL, Murphy LJ, Trends Mol Med 2005 11 192 197 10.1016/j.molmed.2005.02. 004 15823758
7. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. Fusaro G, Dasgupta P, Rastogi S, Joshi B, Chellappan S, J Biol Chem 2003 278 47853 47861 10.1074/jbc.M305171200 14500729 (Pubitemid 37523233)
8. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. Brasaemle DL, Dolios G, Shapiro L, Wang R, J Biol Chem 2004 279 46835 46842 10.1074/jbc.M409340200 15337753 (Pubitemid 39518334)
9. Differential immunization identifies PHB1/PHB2 as blood-borne tumor antigens. Mengwasser J, Piau A, Schlag P, Sleeman JP, Oncogene 2004 23 7430 7435 10.1038/sj.onc.1207987 15286703 (Pubitemid 39382145)
10. Prohibitin: a potential biomarker for tissue-based detection of gastric cancer. Kang X, Zhang L, Sun J, Ni Z, Ma Y, Chen X, Sheng X, Chen T, J Gastroenterol 2008 43 618 625 10.1007/s00535-008-2208-3 18709484
11. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Nuell MJ, Stewart DA, Walker L, Friedman V, Wood CM, Owens GA, Smith JR, Schneider EL, Dell' Orco R, Lumpkin CK, Mol Cell Biol 1991 11 1372 1381 1996099 (Pubitemid 21895493)
12. Cell cycle activity and expression of prohibitin mRNA. Roskams AJ, Friedman V, Wood CM, Walker L, Owens GA, Stewart DA, Altus MS, Danner DB, Liu XT, McClung JK, J Cell Physiol 1993 157 289 295 10.1002/jcp.1041570211 8227162 (Pubitemid 23332772)
13. Prohibitin: potential role in senescence, development, and tumor suppression. McClung JK, Jupe ER, Liu XT, Dell'Orco RT, Exp Gerontol 1995 30 99 124 10.1016/0531-5565(94)00069-7 8591812
14. Prohibitin facilitates cellular senescence by recruiting specific corepressors to inhibit E2F target genes. Rastogi S, Joshi B, Dasgupta P, Morris M, Wright K, Chellappan S, Mol Cell Biol 2006 26 4161 4171 10.1128/MCB.02142-05 16705168 (Pubitemid 43788018)
15. Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2. Kasashima K, Ohta E, Kagawa Y, Endo H, J Biol Chem 2006 281 36401 36410 10.1074/jbc.M605260200 17008324 (Pubitemid 46041374)
16. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA, EMBO J 2000 19 2444 2451 10.1093/emboj/19.11.2444 10835343 (Pubitemid 30323534)
17. Prohibitin interacts with RNF2 and regulates E2F1 function via dual pathways. Choi D, Lee SJ, Hong S, Kim IH, Kang S, Oncogene 2008 27 1716 1725 10.1038/sj.onc.1210806 17873902 (Pubitemid 351380260)
18. A repressive role for prohibitin in estrogen signaling. He B, Feng Q, Mukherjee A, Lonard DM, DeMayo FJ, Katzenellenbogen BS, Lydon JP, O'Malley BW, Mol Endocrinol 2008 22 344 360 17932104 (Pubitemid 351185935)
19. Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells. Chowdhury I, Branch A, Olatinwo M, Thomas K, Matthews R, Thompson WE, Life Sci 2011 89 295 303 10.1016/j.lfs.2011. 06.022 21763324
20. Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus-directed overexpression of prohibitin. Chowdhury I, Xu W, Stiles JK, Zeleznik A, Yao X, Matthews R, Thomas K, Thompson WE, Endocrinology 2007 148 206 217 17038561 (Pubitemid 46021452)
21. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im GS, Prather RS, Isom SC, Rucker E 3rd, Tsang BK, Biol Reprod 2004 71 282 290 10.1095/biolreprod.103.024125 15028627 (Pubitemid 38915335)
22. The emerging roles of prohibitins in folliculogenesis. Chowdhury I, Garcia-Barrio M, Harp D, Thomas K, Matthews R, Thompson WE, Front Biosci (Elite Ed) 2012 4 690 699
23. Inhibitory roles of prohibitin and chemerin on FSH-induced rat granulosa cell steroidogenesis. Wang Q, Leader A, Tsang BK, Endocrinology 2013 154 956 967 10.1210/en.2012-1836 23254195
24. Ovarian granulosa cells isolated with EGTA and hypertonic sucrose: cellular integrity and function. Campbell KL, Biol Reprod 1979 21 773 786 10.1095/biolreprod21.4.773 118773 (Pubitemid 10216244)
25. Role and regulation of nodal/activin receptor-like kinase 7 signaling pathway in the control of ovarian follicular atresia. Wang H, Jiang JY, Zhu C, Peng C, Tsang BK, Mol Endocrinol 2006 20 2469 2482 10.1210/me.2005-0446 16709598 (Pubitemid 44496415)
26. Luteinizing hormone receptor, steroidogenesis acute regulatory protein, and steroidogenic enzyme messenger ribonucleic acids are overexpressed in thecal and granulosa cells from polycystic ovaries. Jakimiuk AJ, Weitsman SR, Navab A, Magoffin DA, J Clin Endocrinol Metab 2001 86 1318 1323 10.1210/jc.86.3.1318 11238527 (Pubitemid 32323023)
27. The follicular excess in polycystic ovaries, due to intra-ovarian hyperandrogenism, may be the main culprit for the follicular arrest. Jonard S, Dewailly D, Hum Reprod Update 2004 10 107 117 10.1093/humupd/dmh010 15073141 (Pubitemid 38519332)
28. Chemerin, a novel regulator of follicular steroidogenesis and its potential involvement in polycystic ovarian syndrome. Wang Q, Kim JY, Xue K, Liu JY, Leader A, Tsang BK, Endocrinology 2012 153 5600 5611 10.1210/en.2012-1424 22948218
29. X-linked inhibitor of apoptosis protein activates the phosphatidylinositol 3-kinase/Akt pathway in rat granulosa cells during follicular development. Asselin E, Wang Y, Tsang BK, Endocrinology 2001 142 2451 2457 10.1210/en.142.6.2451 11356694 (Pubitemid 32473101)
30. Differential regulation of Rb family proteins and prohibitin during camptothecin-induced apoptosis. Fusaro G, Wang S, Chellappan S, Oncogene 2002 21 4539 4548 10.1038/sj.onc.1205551 12085232 (Pubitemid 34785730)
31. Expression and regulation of transcripts encoding two members of the NR5A nuclear receptor subfamily of orphan nuclear receptors, steroidogenic factor-1 and NR5A2, in equine ovarian cells during the ovulatory process. Boerboom D, Pilon N, Behdjani R, Silversides DW, Sirois J, Endocrinology 2000 141 4647 4656 10.1210/en.141.12.4647 11108279 (Pubitemid 32055144)
32. Expression of LRH-1 and SF-1 in the mouse ovary: localization in different cell types correlates with differing function. Hinshelwood MM, Repa JJ, Shelton JM, Richardson JA, Mangelsdorf DJ, Mendelson CR, Mol Cell Endocrinol 2003 207 39 45 10.1016/S0303-7207(03)00257-0 12972182 (Pubitemid 37102952)
33. Transcriptional regulation of the StAR gene. Reinhart AJ, Williams SC, Stocco DM, Mol Cell Endocrinol 1999 151 161 169 10.1016/S0303-7207(98)00257-3 10411331 (Pubitemid 29295524)
34. cAMP-dependent regulation of CYP19 gene in rabbit preovulatory granulosa cells and corpus luteum. Andrieu T, Pezzi V, Sirianni R, Le Bas R, Feral C, Benhaim A, Mittre H, J Steroid Biochem Mol Biol 2009 116 110 117 10.1016/j.jsbmb.2009.05.003 19460434
35. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Ny T, Wahlberg P, Brandstrom IJ, Mol Cell Endocrinol 2002 187 29 38 10.1016/S0303-7207(01)00711-0 11988309 (Pubitemid 34441038)
36. Intrafollicular distribution of plasminogen activators and their hormonal regulation in vitro. Reich R, Miskin R, Tsafriri A, Endocrinology 1986 119 1588 1593 10.1210/endo-119-4-1588 3093196 (Pubitemid 17170524)
37. Follicular stage-dependent regulation of rat granulosa cell plasminogen activator system by transforming growth factor-alpha in vitro. Karakji EG, Tsang BK, Biol Reprod 1995 52 411 418 10.1095/biolreprod52.2.411 7711210
38. Tumor necrosis factor alpha inhibits rat granulosa cell plasminogen activator activity in vitro during follicular development. Karakji EG, Tsang BK, Biol Reprod 1995 52 745 752 10.1095/biolreprod52.4.745 7779996
39. B-type natriuretic peptide receptor expression and activity are hormonally regulated in rat ovarian cells. Noubani A, Farookhi R, Gutkowska J, Endocrinology 2000 141 551 559 10.1210/en.141.2.551 10650935 (Pubitemid 32250478)
40. Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Thompson WE, Powell JM, Whittaker JA, Sridaran R, Thomas KH, Anat Rec 1999 256 40 48 10.1002/(SICI)1097- 0185(19990901)256:1<40::AID-AR6>3.0.CO;2-X 10456984 (Pubitemid 29402665)
41. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Simoni M, Gromoll J, Nieschlag E, Endocr Rev 1997 18 739 773 10.1210/er.18.6.739 9408742 (Pubitemid 28009566)
42. Follicle-stimulating hormone regulation on its receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Minegishi T, Tano M, Kishi H, Kameda T, Miyamoto K, Biochim Biophys Acta 1997 1359 165 173 10.1016/S0167-4889(97)00095-5 9409813 (Pubitemid 27507818)
43. Granulosa cells are refractory to FSH action in individuals with a low antral follicle count. Scheetz D, Folger JK, Smith GW, Ireland JJ, Reprod Fertil Dev 2012 24 327 336 10.1071/RD11020 22281079
44. Anti-Mullerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Pellatt L, Rice S, Dilaver N, Heshri A, Galea R, Brincat M, Brown K, Simpson ER, Mason HD, Fertil Steril 2011 96 1246 1251 e1241 10.1016/j.fertnstert.2011.08.015 21917251
45. Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Wayne CM, Fan HY, Cheng X, Richards JS, Mol Endocrinol 2007 21 1940 1957 10.1210/me.2007-0020 17536007 (Pubitemid 47173802)
46. CREB coactivator CRTC2/TORC2 and its regulator calcineurin crucially mediate follicle-stimulating hormone and transforming growth factor beta1 upregulation of steroidogenesis. Fang WL, Lee MT, Wu LS, Chen YJ, Mason J, Ke FC, Hwang JJ, J Cell Physiol 2012 227 2430 2440 10.1002/jcp.22978 21826657
47. Transcriptional regulation by the phosphorylation-dependent factor CREB. Mayr B, Montminy M, Nat Rev Mol Cell Biol 2001 2 599 609 10.1038/35085068 11483993 (Pubitemid 33674011)
48. Liver receptor homolog-1 and steroidogenic factor-1 have similar actions on rat granulosa cell steroidogenesis. Saxena D, Escamilla-Hernandez R, Little-Ihrig L, Zeleznik AJ, Endocrinology 2007 148 726 734 17095585 (Pubitemid 46150778)
49. Prohibitin has an important role in adipocyte differentiation. Ande SR, Xu Z, Gu Y, Mishra S, Int J Obes (Lond) 2012 36 1236 1244 10.1038/ijo.2011.227
50. Regulation of Akt/PKB Ser473 phosphorylation. Bayascas JR, Alessi DR, Mol Cell 2005 18 143 145 10.1016/j.molcel.2005.03.020 15837416
51. Priming procedure and hormone preparations influence rat granulosa cell response. Liu WK, Bousfield GR, Moore WT Jr, Ward DN, Endocrinology 1985 116 1454 1459 10.1210/endo-116-4-1454 3918855 (Pubitemid 15081017)
52. Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Zeleznik AJ, Saxena D, Little-Ihrig L, Endocrinology 2003 144 3985 3994 10.1210/en.2003-0293 12933673 (Pubitemid 37088754)
53. Inhibition of rat granulosa cell differentiation by overexpression of Galphaq. Escamilla-Hernandez R, Little-Ihrig L, Zeleznik AJ, Endocrine 2008 33 21 31 10.1007/s12020-008-9064-z 18401763
54. Androgens augment FSH-induced progesterone secretion by cultured rat granulosa cells. Armstrong DT, Dorrington JH, Endocrinology 1976 99 1411 1414 10.1210/endo-99-5-1411 1033061 (Pubitemid 8001958)
55. Factors influencing follicle-stimulating hormone-responsive steroidogenesis in marmoset granulosa cells: effects of androgens and the stage of follicular maturity. Harlow CR, Shaw HJ, Hillier SG, Hodges JK, Endocrinology 1988 122 2780 2787 10.1210/endo-122-6-2780 3131124