The emerging roles of prohibitins in folliculogenesis

Frontiers in Bioscience - Elite

Volumn 4 E, Issue 2, 2012, Pages 690-699

  Chowdhury, Indrajit ^a   Garcia Barrio, Minerva ^a   Harp, Djana ^a   Thomas, Kelwyn ^a   Matthews, Roland ^a   Thompson, Winston E ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

Mitochondria; Nucleus; PHB; PHB2; Prohibitins; REA; Repressor of estrogen receptor action; Review

Indexed keywords

CASPASE 3; CYTOCHROME C; EPHRIN RECEPTOR B2; FOLLITROPIN; FOLLITROPIN RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROHIBITIN; PROTEIN BCL 2; PROTEIN BCL XL; RAF PROTEIN; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; AUTOSOMAL DOMINANT OPTIC ATROPHY; CANCER GROWTH; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATIONAL TRANSITION; ENZYME ACTIVATION; EXON; EXTRACELLULAR MATRIX; FEMALE FERTILITY; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; INTRACELLULAR SPACE; INTRON; ISOELECTRIC POINT; METAPHASE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OVARY CANCER; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RNA INTERFERENCE; UPREGULATION;

ANIMALIA; EUKARYOTA; FUNGI; PROKARYOTA; PROTISTA;

EID: 84883349621     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. J. Craig, M. Orisaka, H. Wang, S. Orisaka, W.E. Thompson, C. Zhu, F. Kotsuji, B.K. Tsang. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Front Biosci. 12, 3628-3639 (2007)
2. W.E. Thompson, A. Sanbuissho, G.Y. Lee, E. Anderson. Steroidogenic acute regulatory (StAR) protein (p25) and prohibitin (p28) from cultured rat ovarian granulosa cells. J Reprod Fertil 109, 337-348 (1997)
3. W.E. Thompson, J.M. Powell, J.A. Whittaker, R. Sridaran, K.H. Thomas. Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Anat Rec 256, 40-48 (1999)
4. W.E. Thompson, E. Asselin, A. Branch, J.K. Stiles, P. Sutovsky, L. Lai, G-S. Im, R.S. Prather, S.C. Isom, E. Rucker III, B. Tsang. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biol Reprod 71, 282-290 (2004)
5. W.E. Thompson, A. Branch, J.A. Whittaker, D. Lyn, M. Zilberstein, K.E. Mayo, K. Thomas. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 142:4076-4085 (2001)
6. I. Chowdhury, W. Xu, J.K. Stiles, A. Zeleznik, X. Yao, R. Matthews, K. Thomas, W.E. Thompson. Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus directed overexpression of prohibitin. Endocrinology 148, 206-217 (2006)
7. R. Nadimpalli, N. Yalpani, G.S. Johal, C.R. Simmons. Prohibitins, stomatins and plant desease response genes compose a superfamily that controls cell proliferation, ion channels regulation and death. J Biol Chem 275, 29579-29586 (2000)
8. S. Mishra, L.C. Murphy, L.J. Murphy. The Prohibitins: emerging roles in diverse functions. J Cell Mol Med 10:353-363 (2006)
9. T. Sato, H. Saito, J. Swensen, A. Olifant, C. Wood, D. Danner, T. Sakamoto, K. Takita, F. Kasumi, Y. Miki, M. Skolnick, Y. Nakamura. The human prohibitin gene located on chromosome 17q21 is mutated in sporadic breast cancer. Cancer Res, 52, 1643-1646 (1992)
10. M.S. Altus, C.M. Wood, D.A. Stewart, A.J. Roskams, V. Friedman, T. Henderson, G.A. Owens, D.B. Danner, E.R. Jupe, R.T. Dell'Orco, J. Keith McClung. Regions of evolutionary conservation between the rat and human prohibitin-encoding genes. Gene 158, 291-294 (1995)
11. B. He, Q. Feng, A. Mukherjee, D.M. Lonard, F.J. DeMayo, B.S. Katzenellenbogen, J.P. Lydon, B.W. O'Malley. A repressive role for prohibitin in estrogen signaling. Mol Endocrinol. 22, 344-60 (2008)
12. M. Terashima, K.M. Kim, T. Adachi, P.J. Nielsen, K.G. Reth, M.C. Lamers. The IgM antigen receptor of B lymphocytes is associated with prohibitin and a prohibitinrelated protein. EMBO J 13, 3782-3792 (1994)
13. M.A. Ansari-Lari, Y. Shen, D.M. Muzny, W. Lee, R.A. Gibbs. Large-scale sequencing in human chromosome 12p13: experimental and computational gene structure determination. Genome Res 7, 268-280 (1997)
14. G. Steglich, W. Neupert, T. Langer. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 19, 3435-42 (1999)
15. M.J. Nuell, D.A. Stewart, L. Walker, V. Friedman, C.M. Wood, G.A. Owens, J.R. Smith, E.L. Schneider, R. Dell' Orco, C.K. Lumpkin, D.B. Danner, J.K. McClung. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol. Cell. Biol 11, 1372-1381 (1991)
16. L.G. Nijtmans, L. de Jong, M. Artal Sanz, P.J. Coates, J.A. Berden, J.W. Back, A.O. Muijsers, H. van der Spek, L.A. Grivell. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19, 2444-51(2000)
17. L.G. Nijtmans, S.M. Artal, L.A. Grivell, P.J. Coates. The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 59, 143-155 (2002)
18. S. Wang, B. Zhang, D.V. Faller. Prohibitin requires Brg-1 and Brm for the repression of E2F and cell growth. EMBO J 21, 3019-3028 (2002)
19. S. Wang, N. Nath, G. Fusaro, S. Chellappan. Rb and prohibitin target distinct regions of E2F1 for repression and respond to different upstream signals. Mol Cell Biol 19, 7447-7460 (1999)
20. M.M. Montano, K. Ekena, R. Delage-Mourroux, W. Chang, P. Martini, B.S. Katzenellenbogen. An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc Natl Acad Sci U S A 96, 6947-52 (1999)
21. V. Kurtev, R. Margueron, K. Kroboth, E. Ogris, V. Cavailles, C. Seiser. Transcriptional regulation by the repressor of estrogen receptor activity via recruitment of histone deacetylases. J Biol Chem 279, 24834-43 (2004)
22. Martini PG, Delage-Mourroux R, Kraichely DM, Katzenellenbogen BS. Prothymosin alpha selectively enhances estrogen receptor transcriptional activity by interacting with a repressor of estrogen receptor activity. 2000; 20:6224-6232.
23. S. Narasimhan, M. Armstrong, J.K. McClung, F.F. Richards, E.K. Spicer. Prohibitin, a putative negative control element present in Pneumocystis carinii. Infect Immun 65, 5125-30 (1997)
24. J.C. Edman, M.L. Sogin. Molecular phylogeny of Pneumocystis carinnii. In: Pneumocystis carinii Pneumonia. Walzer, P.D. (ed), Marcel Dekker, Inc. New York, NY. 91-107 (1994)
25. F. de Monbrison, S. Picot. Introducing antisense oligonucleotides into Pneumocystis carinii. J Microbiol Methods 50, 211-213 (2002)
26. W.A. Snedden, Fromm, H. Characterization of the plant homologue of prohibitin, a gene associated with antiproliferative activity in mammalian cells. Plant Mol Biol 33, 753-6 (1997)
27. A. Takahashi, T. Kawasaki, H.L. Wong, U. Suharsono, H. Hirano, K. Shimamoto. Hyperphosphorylation of a mitochondrial protein, prohibitin, is induced by calyculin A in a rice lesion-mimic mutant cdr1. Plant Physiol 132, 1861-9 (2003)
28. S.C. Welburn, N.B. Murphy. Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death Differ 5, 615-22 (1998)
29. K.H. Berger, M.P. Yaffe. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 8, 4043-52 (1998)
30. P.A. Kirchman, M.V. Miceli, R.L. West, J.C. Jiang, S. Kim, S.M. Jazwinski. Prohibitins and Ras2 protein cooperate in the maintenance of mitochondrial function during yeast aging. Acta Biochim Pol 50, 1039-56 (2003)
31. T. Tatsuta, K. Model, T. Langer. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16, 248-59 (2005)
32. D.D. Eveleth Jr, J.L. Marsh. Sequence and expression of the Cc gene, a member of the dopa decarboxylase gene cluster of Drosophila: Possible translational regulation. Nucleic Acids Res 14, 6169-6183 (1986)
33. S.E. Park, J. Xu, A. Frolova, L. Liao, B.W. O'Malley, B.S. Katzenellenbogen. Genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo. Mol Cell Biol 25, 1989-99 (2005)
34. M. Artal-Sanz, W.Y. Tsang, E.M. Willems, L.A. Grivell, B.D. Lemire, H. van der Spek, L.G. Nijtmans. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem 278(34), 32091-32099 (2003)
35. A.J.W. Hsueh, E.Y. Adashi, P.B.C. Jones, T.H. Welsh Jr. Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocrine Reviews 5, 76-110 (1984)
36. R.C. Gregory-Bass, M. Olatinwo, W. Xu, R. Matthews, J.K. Stiles, K. Thomas, D. Liu, B. Tsang, W.E. Thompson. Prohibitin silencing reverses stabilization of mitochondrial integrity and chemoresistance in ovarian cancer cells by increasing their sensitivity to apoptosis. Int J Cancer 122(9), 1923-30 (2008)
37. N.M. Choongkittaworn, K.H. Kim, D.B. Danner, M.D. Griswold. Expression of prohibitin in rat seminiferous epithelium. Biol Reprod, 49, 300-310 (1993)
38. E. Bonnet, A. Fostier, J. Bobe. Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics 8, 55 (2007)
39. R. Bukowski, G.D. Hankins, G.R. Saade, G.D. Anderson, S. Thornton. Labor-associated gene expression in the human uterine fundus, lower segment, and cervix. PLoS Med, 3(6), e169 (2006)
40. C. Merkwirth, S. Dargazanli, T. Tatsuta, S. Geimer, B. Löwer, F.T. Wunderlich, J.C. von Kleist-Retzow, A. Waisman, B. Westermann, T. Langer. Prohibitins control cell proliferation and apoptosis by regulating OPA1- dependent cristae morphogenesis in mitochondria. Genes Dev 22(4), 476-88 (2008)
41. D. Choi, S.J. Lee, S. Hong, I.H. Kim, S. Kang. Prohibitin interacts with RNF2 and regulates E2F1 function via dual pathways. Oncogene 27, 1716-25 (2008)
42. K. Rikova, A. Guo, Q. Zeng, A. Possemato, J. Yu, H. Haack, J. Nardone, K. Lee, C. Reeves, Y. Li, Y. Hu, Z. Tan, M. Stokes, L. Sullivan, J. Mitchell, R. Wetzel, J. Macneill, J.M. Ren, J. Yuan, C.E. Bakalarski, J. Villen, J.M Kornhauser, B. Smith, D. Li, X. Zhou, S.P. Gygi, T.L. Gu, R.D. Polakiewicz, J. Rush, M.J. Comb. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131(6), 1190-203 (2007)
43. K. Rajalingam, C. Wunder, V. Brinkmann, Y. Churin, M. Hekman, C. Sievers, U.R. Rapp, T. Rudel. Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat Cell Biol 7, 837-843 (2005)
44. V.D. Dixit, R. Sridaran, M.A. Edmonsond, D. Taub, W.E. Thompson. Gonadotropin releasing hormone attenuates pregnancy-associated thymic involution and modulates the expression of antiproliferative gene product prohibitin. Endocrinology 144, 1496-1505 (2003)
45. D.L. Boone, J.A. Carnegie, P.U. Rippstein, B.K. Tsang. Induction of apoptosis in equine chorionic gonadotropin (eCG)-primed rat ovaries by anti-eCG antibody. Biol Reprod 57, 420-427 (1997)
46. A. Palumbo, J. Yeh. In situ localization of apoptosis in the rat ovary during follicular atresia. Biol Reprod 51, 888- 895 (1994)
47. J.L. Tilly, K.I. Kowalski, A.L. Johnson, A.J. Hsueh. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129, 2799-2801 (1991)
48. J.Y. Jiang, C.K. Cheung, Y. Wang, B.K. Tsang. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 8, 222-237 (2003)
49. Z. Jin, W.S. El-Deiry. Overview of cell death signaling pathways. Cancer Biol Ther 4, 139-163 (2005)
50. T. Matikainen, G.I. Perez, T.S. Zheng, T.R. Kluzak, B.R. Rueda, R.A. Flavell, J.L. Tilly. Caspase-3 Gene Knockout Defines Cell Lineage Specificity for Programmed Cell Death Signaling in the Ovary. Endocrinol 142, 2468-2480 (2001)
51. C. Osman, C. Merkwirth, T. Langer. Prohibitins and the functional compartmentalization of mitochondrial membranes. J Cell Sci 122(Pt 21), 3823-3830 (2009)
52. K. Kasashima, E. Ohta, Y. Kagawa, H. Endo. Mitochondrial Functions and Estrogen Receptor-dependent Nuclear Translocation of Pleiotropic Human Prohibitin. J Biol Chem 281, 36401-36410 (2006)
53. C. Merkwirth, S. Dargazanli, T. Tatsuta, S. Geimer, B. Löwer, F.T. Wunderlich, J.C. von Kleist-Retzow, A. Waisman, B. Westermann, T. Langer. Prohibitins control cell proliferation and apoptosis by regulating OPA1- dependent cristae morphogenesis in mitochondria. Genes Dev 22(4), 476-88 (2008)
54. S. Hoppins, L. Lackner, J. Nunnari. The machines that divide and fuse mitochondria. Annu Rev Biochem 76, 751- 780 (2007)
55. C. Alexander, M. Votruba, U.E. Pesch, D.L. Thiselton, S. Mayer, A. Moore, M. Rodriguez, U. Kellner, B. Leo- Kottler, G. Auburger, S.S. Bhattacharya, B.Wissinger. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26(2), 211-5 (2000)
56. C. Delettre, G. Lenaers, J.M. Griffoin, N. Gigarel, C. Lorenzo, P. Belenguer, L. Pelloquin, J. Grosgeorge, C. Turc-Carel, E. Perret, C. Astarie-Dequeker, L. Lasquellec, B. Arnaud, B. Ducommun, J. Kaplan, C.P. Hamel. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26(2), 207-10 (2000)
57. V.R. Akepati, E.C. Müller, A. Otto, H.M. Strauss, M. Portwich, C. Alexander. Characterization of OPA1 isoforms isolated from mouse tissues. J Neurochem, 106(1), 372-83 (2008)
58. C. Delettre, J.M. Griffoin, J. Kaplan, H. Dollfus, B. Lorenz, L. Faivre, G. Lenaers, P. Belenguer, C.P. Hamel. Mutation spectrum and splicing variants in the OPA1 gene. Hum Genet 109(6), 584-91 (2001)
59. N. Ishihara, Y. Fujita, T. Oka, K. Mihara. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 25(13), 2966-2977 (2006)
60. M. Satoh, T. Hamamoto, N. Seo, Y. Kagawa, H. Endo. Differential sublocalization of the dynamin-related protein OPA1 isoforms in mitochondria. Biochem Biophys Res Commun 300(2), 482-493 (2003)
61. Z. Song, H. Chen, M. Fiket, C. Alexander, D.C. Chan. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178(5), 749-755 (2007)
62. L. Sun, L. Liu, X.J. Yang, Wu, Z. Akt binds prohibitin 2 and relieves its repression of MyoD and muscle differentiation. J Cell Sci 117, 3021-3029 (2004)
63. G. Song, G. Ouyang, S. Bao, The activation of Akt / PKB signaling pathway and cell survival. J Cell Mol Med 9, 59-71 (2005)