Prohibitin silencing reverses stabilization of mitochondrial integrity and chemoresistance in ovarian cancer cells by increasing their sensitivity to apoptosis

International Journal of Cancer

Volumn 122, Issue 9, 2008, Pages 1923-1930

  Gregory Bass, Rosalind C ^a   Olatinwo, Moshood ^a,b   Xu, Wei ^a   Matthews, Roland ^a   Stiles, Jonathan K ^a   Thomas, Kelwyn ^a   Liu, Dong ^a   Tsang, Benjamin ^c,d   Thompson, Winston E ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF OTTAWA   (Canada)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

Adenovirus; Gene silencing; Mitochondria; Ovarian cancer; Prohibitin

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 3; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; PROHIBITIN; SMALL INTERFERING RNA; STAUROSPORINE; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; RECOMBINANT PROTEIN; REPRESSOR PROTEIN;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CANCER SURVIVAL; CARCINOGENESIS; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL GROWTH; CHEMOSENSITIVITY; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO; ENDOMETRIOID CARCINOMA; ENZYME ACTIVITY; EPITHELIUM; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; MITOCHONDRION; MOLECULAR STABILITY; OVARY ADENOCARCINOMA; OVARY CANCER; OVARY CARCINOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; TIME; WESTERN BLOTTING; ADENOVIRUS; CELL CYCLE; CELL SURVIVAL; CHEMISTRY; DRUG EFFECT; DRUG RESISTANCE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE VECTOR; GENETICS; METABOLISM; OVARY; OVARY TUMOR; PAPILLARY CARCINOMA; TUMOR CELL LINE; UPREGULATION;

ADENOVIRIDAE; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, ENDOMETRIOID; CARCINOMA, PAPILLARY; CASPASE 3; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; FEMALE; G0 PHASE; G1 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENETIC VECTORS; HUMANS; KI-67 ANTIGEN; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; OVARIAN NEOPLASMS; OVARY; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; STAUROSPORINE; UP-REGULATION;

EID: 40749104734     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23351     Document Type: Article

References (36)

1. Black D, Solomon E. The search for the familial breast/ovarian cancer gene. Trends Genet 1993;9:22-6.
2. Roskams AJ, Friedman V, Wood CM, Walker L, Owens GA, Stewart DA, Altus MS, Danner DB, Liu XT, McClung JK. Cell cycle activity and expression of prohibitin mRNA. J Cell Physiol 1993;157:289-95.
3. Thompson WE, Sanbuissho A, Lee GY, Anderson E. Steroidogenic acute regulatory (StAR) protein (p25) and prohibitin (p28) from cultured rat ovarian granulosa cells. J Reprod Fertil 1997;109:337-48.
4. Thompson WE, Powell JM, Whittaker JA, Sridaran R, Thomas KH. Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Anat Rec 1999;256:40-8.
5. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, Thomas K. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 2001;142:4076-85.
6. Dixit VD, Sridaran R, Edmonsond MA, Taub D, Thompson WE. Gonadotropin-releasing hormone attenuates pregnancy-associated thymic involution and modulates the expression of antiproliferative gene product prohibitin. Endocrinology 2003;144:1496-505.
7. Fusaro G, Wang S, Chellappan S. Differential regulation of Rb family proteins and prohibitin during camptothecin-induced apoptosis. Oncogene 2002;21:4539-48.
8. Vander Heiden MG, Choy JS, VanderWeele DJ, Brace JL, Harris MH, Bauer DE, Prange B, Kron SJ, Thompson CB, Rudin CM. Bcl-x(L) complements Saccharomyces cerevisiae genes that facilitate the switch from glycolytic to oxidative metabolism. J Biol Chem 2002;277:44870-6.
9. Fraser M, Leung B, Jahani-Asl A, Yan X, Thompson WE, Tsang BK. Chemoresistance in human ovarian cancer: the role of apoptotic regulators. Reprod Biol Endocrinol 2003;1:66.
10. Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im G-S, Prather RS, Isom SC, Rucker E, III, Tsang B. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biol Reprod 2004;71:282-90.
11. Chowdhury I, Xu W, Stiles JK, Zeleznik A, Yao X, Matthews R, Thomas K, Thompson WE. Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus-directed overexpression of prohibitin. Endocrinology 2007;148:206-17.
12. Craig J, Orisaka M, Wang H, Orisaka S, Thompson W, Zhu C, Kotsuji F, Tsang B. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Front Biosci 2007;12:3628-39.
13. Dell'Orco RT, McClung JK, Jupe ER, Liu XT. Prohibitin and the senescent phenotype. Exp Gerontol 1996;31:245-52.
14. Coates PJ, Nenutil R, McGregor A, Picksley SM, Crouch DH, Hall PA, Wright EG. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp Cell Res 2001;265:262-73.
15. 0-arrested cells. Mech. Ageing Dev 2002;123:287-9.
16. Kurzeder C, Sauer G, Deissler H. Molecular targets of ovarian carcinomas with acquired resistance to platinum/taxane chemotherapy. Curr Cancer Drug Targets 2006;6:207-27.
17. Gorski K, Cameiro M, Scheibler U. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 1986;47:767-76.
18. Somers JP, DeLoia JA, Zeleznik AJ. 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 1999;13:1364-72.
19. L underlies the molecular basis for resistance to staurosporine-induced apoptosis in PC-3 cells. Cancer Res 2001;61:1600-706.
20. Xue L, Chiu S, Oleinick N. Staurosporine-induced death of MCF-7 human breast cancer cells: a distinction between caspase-3-dependent steps of apoptosis and the critical lethal lesions. Exp Cell Res 2003;283:135-45.
21. Runnebaum IB, Brüning A. Glucocorticoids inhibit cell death in ovarian cancer and up-regulate caspase inhibitor cIAP2. Clin Cancer Res 2005;11:6325-32.
22. Gamble SC, Chotai D, Odontiadis M, Dart DA, Brooke GN, Powell SM, Reebye V, Varela-Carver A, Kawano Y, Waxman J, Bevan CL. Prohibitin, a protein downregulated by androgens, represses androgen receptor activity. Oncogene 2007;26:1757-68.
23. Gamble SC, Odontiadis M, Waxman J, Westbrook JA, Dunn MJ, Wait R, Lam EW, Bevan CL. Androgens target prohibitin to regulate proliferation of prostate cancer cells. Oncogene 2004;23:2996-3004.
24. Wang S, Zhang B, Faller DV. BRG1/BRM and prohibitin are required for growth suppression by estrogen antagonists. EMBO J 2004;23:2293-303.
25. Mishra S, Murphy LC, Nyomba BL, Murphy LJ. Prohibitin: a potential target for new therapeutics. Trends. Mol Med 2005;11:192-7.
26. He QY, Cheung YH, Leung SY, Yuen ST, Chu KM, Chiu JF. Diverse proteomic alterations in gastric adenocarcinoma. Proteomics 2004;4:3276-87.
27. Asamoto M, Cohen SM. Prohibitin gene is overexpressed but not mutated in rat bladder carcinomas and cell lines. Cancer Lett 1994;83:201-7.
28. Ha TU, Segev DL, Barbie D, Masiakos PT, Tran TT, Dombkowski D, Glander M, Clarke TR, Lorenzo HK, Donahoe PK, Maheswaran S. Mullerian inhibiting substance inhibits ovarian cell growth through an Rb-independent mechanism. J Biol Chem 2000;275:37101-9.
29. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 2000;19:2444-51.
30. Rajalingam K, Wunder C, Brinkmann V, Churin Y, Hekman M, Sievers C, Rapp UR, Rudel T. Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat Cell Biol 2005;7:837-43.
31. Bourguignon LY, Gilad E, Peyrollier K. Heregulin-mediated ErbB2-ERK signaling activates hyaluronan synthases leading to CD44-dependent ovarian tumor cell growth and migration. J Biol Chem 2007;282:19426-41.
32. Whitehurst AW, Bodemann BO, Cardenas J, Ferguson D, Girard L, Peyton M, Minna JD, Michnoff C, Hao W, Roth MG, Xie XJ, White MA. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature 2007;446:815-9.
33. Karbowski M, Youle RJ. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 2003;8:870-80.
34. Kasashima K, Ohta E, Kagawa Y, Endo H. Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2. J Biol Chem 2006;281:36401-10.
35. Tatsuta T, Model K, Langer T. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 2005;16:248-59.
36. Artal-Sanz M, Tsang WY, Willems EM, Grivell LA, Lemire BD, van der Spek H, Nijtmans LG. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem 2003;278:32091-9.