Prohibitins role in cellular survival through Ras-Raf-MEK-ERK pathway

Journal of Cellular Physiology

Volumn 229, Issue 8, 2014, Pages 998-1004

  Chowdhury, Indrajit ^a   Thompson, Winston E ^a   Thomas, Kelwyn ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; CYTOCHROME C; EPIDERMAL GROWTH FACTOR; FOLLITROPIN; INTERLEUKIN 6; MITOCHONDRIAL DNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROHIBITIN; PROTEIN 14 3 3; PROTEIN BCL 2; PROTEIN BCL XL; RAF PROTEIN; RAS PROTEIN; STAT3 PROTEIN;

CELL FRACTIONATION; CELL PROTECTION; CELL SURVIVAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEGENERATIVE DISEASE; DOWN REGULATION; ENDOPLASMIC RETICULUM; GLUCOSE HOMEOSTASIS; GRANULOSA CELL; HUMAN; INSULIN RELEASE; INTRACELLULAR SIGNALING; INTRACELLULAR SPACE; ISOELECTRIC POINT; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RETINA GANGLION CELL; REVIEW; RNA INTERFERENCE; T LYMPHOCYTE ACTIVATION;

ANIMALS; CELL SURVIVAL; HUMANS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84899070398     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24531     Document Type: Review

References (107)

1. Ahn CS, Lee JH, Reum Hwang A, Kim WT, Pai HS. 2006. Prohibitin is involved in mitochondrial biogenesis in plants. Plant J 46:658-667.
2. Akepati VR, Müller EC, Otto A, Strauss HM, Portwich M, Alexander C. 2008. Characterization of OPA1 isoforms isolated from mouse tissues. J Neurochem 106:372-383.
3. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, Rodriguez M, Kellner U, Leo-Kottler B, Auburger G, Bhattacharya SS, Wissinger B. 2000. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26:211-215.
4. Altus MS, Wood CM, Stewart DA, Roskams AJ, Friedman V, Henderson T, Owens GA, Danner DB, Jupe ER, Dell'Orco RT, Keith McClung J. 1995. Regions of evolutionary conservation between the rat and human prohibitin-encoding genes. Gene 158:291-294.
5. Ande SR, Mishra S. 2009. Prohibitin interacts with phosphatidylinositol 3, 4, 5-triphosphate (PIP3) and modulates insulin signaling. Biochem Biophys Res Commun 390:1023-1028.
6. Ande SR, Gu Y, Nyomba BL, Mishra S. 2009. Insulin induced phosphorylation of prohibitin at tyrosine 114 recruits Shp1. Biochim Biophys Acta 1793:1372-1378.
7. Ansari-Lari MA, Shen Y, Muzny DM, Lee W, Gibbs RA. 1997. Large-scale sequencing in human chromosome 12p13: Experimental and computational gene structure determination. Genome Res 7:268-280.
8. Artal-Sanz M, Tavernarakis N. 2009. Prohibitin couples diapause signalling to mitochondrial metabolism during ageing in C. elegans. Nature 461:793-797.
9. Artal-Sanz M, Tsang WY, Willems EM, Grivell LA, Lemire BD, van der Spek H, Nijtmans LG. 2003. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem 278:32091-32099.
10. Back JW, Sanz MA, De Jong L, De Koning LJ, Nijtmans LG, De Koster CG, Grivell LA, Van Der Spek H, Muijsers AO. 2002. A structure for the yeast prohibitin complex: Structure prediction and evidence from chemical crosslinking and mass spectrometry. Protein Sci 11:2471-2478.
11. Berger KH, Yaffe MP. 1998. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 8:4043-4052.
12. Bernstein HG, Smalla KH, Dürrschmidt D, Keilhoff G, Dobrowolny H, Steiner J, Schmitt A, Kreutz MR, Bogerts B. 2012. Increased density of prohibitin-immunoreactive oligodendrocytes in the dorsolateral prefrontal white matter of subjects with schizophrenia suggests extraneuronal roles for the protein in the disease. Neuromolecular Med 14:270-280.
13. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R. 2010. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105:771-785.
14. Chiu CF, Ho MY, Peng JM, Hung SW, Lee WH, Liang CM, Liang SM. 2013. Raf activation by Ras and promotion of cellular metastasis require phosphorylation of prohibitin in the raft domain of the plasma membrane. Oncogene 32:777-787.
15. Chowdhury I, Bhat GK. 2010. Mitochondria-In cellular life and death, Chapter 5. Svensson OL, editor. In mitochondria structure, functions and dysfunctions. USA: NOVA Publishers. pp 247-376.
16. Chowdhury I, Tharakan B, Bhat GK. 2006. Current concepts in apoptosis: The physiological suicide program revisited. Cell Mol Biol Lett 11:506-525.
17. Chowdhury I, Xu W, Stiles JK, Zeleznik A, Yao X, Matthews R, Thomas K, Thompson WE. 2007. Apoptosis of rat granulosa cells after staurosporine and serum withdrawal is suppressed by adenovirus-directed overexpression of prohibitin. Endocrinology 148:206-217.
18. Chowdhury I, Tharakan B, Bhat GK. 2008. Caspases-An update. Comp Biochem Physiol B Biochem Mol Biol 151:10-27.
19. Chowdhury I, Branch A, Olatinwo M, Thomas K, Matthews R, Thompson WE. 2011. Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells. Life Sci 89:295-303.
20. Chowdhury I, Garcia-Barrio M, Harp D, Thomas K, Matthews R, Thompson WE. 2012. The emerging roles of prohibitins in folliculogenesis. Front Biosci (Elite Ed) 4:690-699.
21. Chowdhury I, Thompson WE, Welch C, Thomas K, Matthews R. 2013. Prohibitin (PHB) inhibits apoptosis in rat granulosa cells (GCs) through the extracellular signal-regulated kinase 1/2 (ERK1/2) and the Bcl family of proteins. Apoptosis 18:1513-1525.
22. Coates PJ, Nenutil R, McGregor A, Picksley SM, Crouch DH, Hall PA, Wright EG. 2001. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp Cell Res 265:262-273.
23. Czarnecka AM, Campanella C, Zummo G, Cappello F. 2006. Mitochondrial chaperones in cancer: From molecular biology to clinical diagnostics. Cancer Biol Ther 5:714-720.
24. Da Cruz S, Parone PA, Gonzalo P, Bienvenut WV, Tondera D, Jourdain A, Quadroni M, Martinou JC. 2008. SLP-2 interacts with prohibitins in the mitochondrial inner membrane and contributes to their stability. Biochim Biophys Acta 1783:904-911.
25. Dart DA, Spencer-Dene B, Gamble SC, Waxman J, Bevan CL. 2009. Manipulating prohibitin levels provides evidence for an in vivo role in androgen regulation of prostate tumours. Endocr Relat Cancer 16:1157-1169.
26. de Monbrison F, Picot S. 2002. Introducing antisense oligonucleotides into Pneumocystis carinii. J Microbiol Methods 50:211-213.
27. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, Astarie-Dequeker C, Lasquellec L, Arnaud B, Ducommun B, Kaplan J, Hamel CP. 2000. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26:207-210.
28. Delettre C, Griffoin JM, Kaplan J, Dollfus H, Lorenz B, Faivre L, Lenaers G, Belenguer P, Hamel CP. 2001. Mutation spectrum and splicing variants in the OPA1 gene. Hum Genet 109:584-591.
29. Dhillon AS, Meikle S, Yazici Z, Eulitz M, Kolch W. 2002. Regulation of Raf-1 activation and signalling by dephosphorylation. EMBO J 21:64-71.
30. Ding Q, Vaynman S, Souda P, Whitelegge JP, Gomez-Pinilla F. 2006. Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 24:1265-1276.
31. Edman JC, Sogin ML. 1994. Molecular phylogeny of Pneumocystis carinnii. In: Pneumocystis carinii pneumonia. Walzer PD, editor. New York, NY: Marcel Dekker, Inc. pp 91-107.
32. Eveleth DD, Jr., Marsh JL. 1986. 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.
33. Gomez L, Paillard M, Price M, Chen Q, Teixeira G, Spiegel S, Lesnefsky EJ. 2011. A novel role for mitochondrial sphingosine-1-phosphate produced by sphingosine kinase-2 in PTP-mediated cell survival during cardioprotection. Basic Res Cardiol 106:1341-1353.
34. Gratia S, Kay L, Potenza L, Seffouh A, Novel-Chaté V, Schnebelen C, Sestili P, Schlattner U, Tokarska-Schlattner M. 2012. Inhibition of AMPK signalling by doxorubicin: At the crossroads of the cardiac responses to energetic, oxidative, and genotoxic stress. Cardiovasc Res 95:290-299.
35. Gregory-Bass RC, Olatinwo M, Xu W, Matthews R, Stiles JK, Thomas K, Liu D, Tsang B, Thompson WE. 2008. Prohibitin silencing reverses stabilization of mitochondrial integrity and chemoresistance in ovarian cancer cells by increasing their sensitivity to apoptosis. Int J Cancer 122:1923-1930.
36. Griparic L, van der Wel NN, Orozco IJ, Peters PJ, van der Bliek AM. 2004. Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J Biol Chem 279:18792-18798.
37. Guillery O, Malka F, Landes T, Guillou E, Blackstone C, Lombès A, Belenguer P, Arnoult D, Rojo M. 2008. Metalloprotease-mediated OPA1 processing is modulated by the mitochondrial membrane potential. Biol Cell 100:315-325.
38. Hájek P, Chomyn A, Attardi G. 2007. Identification of a novel mitochondrial complex containing mitofusin 2 and stomatin-like protein 2. J Biol Chem 282:5670-5681.
39. Han EK, McGonigal T, Butler C, Giranda VL, Luo Y. 2008. Characterization of Akt overexpression in MiaPaCa-2 cells: Prohibitin is an Akt substrate both in vitro and in cells. Anticancer Res 28:957-963.
40. He B, Feng Q, Mukherjee A, Lonard DM, DeMayo FJ, Katzenellenbogen BS, Lydon JP, O'Malley BW. 2008. A repressive role for prohibitin in estrogen signaling. Mol Endocrinol 22:344-360.
41. Henschke P, Vorum H, Honoré B, Rice GE. 2006. Protein profiling the effects of in vitro hyperoxic exposure on fetal rabbit lung. Proteomics 6:1957-1962.
42. Hoppins S, Lackner L, Nunnari J. 2007. The machines that divide and fuse mitochondria. Annu Rev Biochem 76:751-780.
43. Ichishita R, Tanaka K, Sugiura Y, Sayano T, Mihara K, Oka T. 2008. An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J Biochem 143:449-454.
44. Ishihara N, Fujita Y, Oka T, Mihara K. 2006. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 25:2966-2977.
45. Jones DP. 2008. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295:C849-C868.
46. Kang X, Zhang L, Sun J, Ni Z, Ma Y, Chen X, Sheng X, Chen T. 2008. Prohibitin: A potential biomarker for tissue-based detection of gastric cancer. J Gastroenterol 43:618-625.
47. Karnoub AE, Weinberg RA. 2008. Ras oncogenes: Split personalities. Nat Rev Mol Cell Biol 9:517-531.
48. Kasashima K, Ohta E, Kagawa Y, Endo H. 2006. Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin. J Biol Chem 281:36401-36410.
49. Kathiria AS, Neumann WL, Rhees J, Hotchkiss E, Cheng Y, Genta RM, Meltzer SJ, Souza RF, Theiss AL. 2012. Prohibitin attenuates colitis-associated tumorigenesis in mice by modulating p53 and STAT3 apoptotic responses. Cancer Res 72:5778-5789.
50. Kim N, Lee Y, Kim H, Joo H, Youm JB, Park WS, Warda M, Cuong DV, Han J. 2006. Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics 6:1237-1249.
51. Kim YH, Lee H, Kim TY, Hwang HR, Lee SC. 2009. Differential expression of prohibitin and regulation of apoptosis in wild-type and COX-2 null mouse embryonic fibroblasts. J Dermatol Sci 53:157-159.
52. Kirchman PA, Miceli MV, West RL, Jiang JC, Kim S, Jazwinski SM. 2003. Prohibitins and Ras2 protein cooperate in the maintenance of mitochondrial function during yeast aging. Acta Biochim Pol 50:1039-1056.
53. Kurtev V, Margueron R, Kroboth K, Ogris E, Cavailles V, Seiser C. 2004. Transcriptional regulation by the repressor of estrogen receptor activity via recruitment of histone deacetylases. J Biol Chem 279:24834-24843.
54. Lee JH, Nguyen KH, Mishra S, Nyomba BL. 2010a. Prohibitin is expressed in pancreatic beta-cells and protects against oxidative and proapoptotic effects of ethanol. FEBS J 277:488-500.
55. Lee H, Arnouk H, Sripathi S, Chen P, Zhang R, Bartoli M, Hunt RC, Hrushesky WJ, Chung H, Lee SH, Jahng WJ. 2010b. Prohibitin as an oxidative stress biomarker in the eye. Int J Biol Macromol 47:685-690.
56. Liu XH, Qian LJ, Gong JB, Shen J, Zhang XM, Qian XH. 2004. Proteomic analysis of mitochondrial proteins in cardiomyocytes from chronic stressed rat. Proteomics 4:3167-3176.
57. Liu X, Ren Z, Zhan R, Wang X, Wang X, Zhang Z, Leng X, Yang Z, Qian L. 2009. Prohibitin protects against oxidative stress-induced cell injury in cultured neonatal cardiomyocyte. Cell Stress Chaperones 14:311-319.
58. Martini PG, Delage-Mourroux R, Kraichely DM, Katzenellenbogen BS. 2000. Prothymosin alpha selectively enhances estrogen receptor transcriptional activity by interacting with a repressor of estrogen receptor activity. Mol Cell Biol 20:6224-6232.
59. Matallanas D, Birtwistle M, Romano D, Zebisch A, Rauch J, von Kriegsheim A, Kolch W. 2011. Raf family kinases: Old dogs have learned new tricks. Genes Cancer 2:232-260.
60. Matikainen T, Perez GI, Zheng TS, Kluzak TR, Rueda BR, Flavell RA, Tilly JL. 2001. Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology 142:2468-2480.
61. Merkwirth C, Langer T. 2009. Prohibitin function within mitochondria: Essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta 1793:27-32.
62. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Löwer B, Wunderlich FT, von Kleist-Retzow JC, Waisman A, Westermann B, Langer T. 2008. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 22:476-488.
63. Merkwirth C, Martinelli P, Korwitz A, Morbin M, Brönneke HS, Jordan SD, Rugarli EI, Langer T. 2012. Loss of prohibitin membrane scaffolds impairs mitochondrial architecture and leads to tau hyperphosphorylation and neurodegeneration. PLoS Genet 8:e1003021.
64. Mishra S, Murphy LC, Murphy LJ. 2006. The prohibitins: Emerging roles in diverse functions. J Cell Mol Med 10:353-363.
65. Montano MM, Ekena K, Delage-Mourroux R, Chang W, Martini P, Katzenellenbogen BS. 1999. An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc Natl Acad Sci USA 96:6947-6952.
66. Muraguchi T, Kawawa A, Kubota S. 2010. Prohibitin protects against hypoxia-induced H9c2 cardiomyocyte cell death. Biomed Res 31:113-122.
67. Nadimpalli R, Yalpani N, Johal GS, Simmons CR. 2000. Prohibitins, stomatins and plant disease response genes compose a superfamily that controls cell proliferation, ion channels regulation and death. J Biol Chem 275:29579-29586.
68. Narasimhan S, Armstrong M, McClung JK, Richards FF, Spicer EK. 1997. Prohibitin, a putative negative control element present in Pneumocystis carinii. Infect Immun 65:5125-5130.
69. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA. 2000. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J 19:2444-2451.
70. Nijtmans LG, Artal SM, Grivell LA, Coates PJ. 2002. The mitochondrial PHB complex: Roles in mitochondrial respiratory complex assembly, ageing and degenerative disease. Cell Mol Life Sci 59:143-155.
71. Nuell MJ, Stewart DA, Walker L, Friedman V, Wood CM, Owens GA, Smith JR, Schneider EL, Dell' Orco R, Lumpkin CK, Danner DB, McClung JK. 1991. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol Cell Biol 11:1372-1381.
72. Osman C, Merkwirth C, Langer T. 2009. Prohibitins and the functional compartmentalization of mitochondrial membranes. J Cell Sci 122:3823-3830.
73. Park SE, Xu J, Frolova A, Liao L, O'Malley BW, Katzenellenbogen BS. 2005. Genetic deletion of the repressor of estrogen receptor activity (REA) enhances the response to estrogen in target tissues in vivo. Mol Cell Biol 25:1989-1999.
74. Park B, Yang J, Yun N, Choe KM, Jin BK, Oh YJ. 2010. Proteomic analysis of expression and protein interactions in a 6-hydroxydopamine-induced rat brain lesion model. Neurochem Int 57:16-32.
75. Patel N, Chatterjee SK, Vrbanac V, Chung I, Mu CJ, Olsen RR, Waghorne C, Zetter BR. 2010. Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc Natl Acad Sci USA 107:2503-2508.
76. Peng X, Mehta R, Wang S, Chellappan S, Mehta RG. 2006. Prohibitin is a novel target gene of vitamin D involved in its antiproliferative action in breast cancer cells. Cancer Res 66:7361-7369.
77. Rajalingam K, Rudel T. 2005. Ras-Raf signaling needs prohibitin. Cell Cycle 4:1503-1505.
78. Rajalingam K, Wunder C, Brinkmann V, Churin Y, Hekman M, Sievers C, Rapp UR, Rudel T. 2005. Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat Cell Biol 7:837-843.
79. Ross JA, Nagy ZS, Kirken RA. 2008. The PHB1/2 phosphocomplex is required for mitochondrial homeostasis and survival of human T cells. J Biol Chem 283:4699-4713.
80. Sato T, Saito H, Swensen J, Olifant A, Wood C, Danner D, Sakamoto T, Takita K, Kasumi F, Miki Y, Skolnick M, Nakamura Y. 1992. The human prohibitin gene located on chromosome 17q21 is mutated in sporadic breast cancer. Cancer Res 52:1643-1646.
81. Satoh M, Hamamoto T, Seo N, Kagawa Y, Endo H. 2003. Differential sublocalization of the dynamin-related protein OPA1 isoforms in mitochondria. Biochem Biophys Res Commun 300:482-493.
82. Sievers C, Billig G, Gottschalk K, Rudel T. 2010. Prohibitins are required for cancer cell proliferation and adhesion. PLoS ONE 5:e12735.
83. Snedden WA, Fromm H. 1997. Characterization of the plant homologue of prohibitin, a gene associated with antiproliferative activity in mammalian cells. Plant Mol Biol 33:753-756.
84. Sripathi SR, He W, Atkinson CL, Smith JJ, Liu Z, Elledge BM, Jahng WJ. 2011. Mitochondrial-nuclear communication by prohibitin shuttling under oxidative stress. Biochemistry 50:8342-8351.
85. Steglich G, Neupert W, Langer T. 1999. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 19:3435-3442.
86. Strub GM, Paillard M, Liang J, Gomez L, Allegood JC, Hait NC, Maceyka M, Price MM, Chen Q, Simpson DC, Kordula T, Milstien S, Lesnefsky EJ, Spiegel S. 2011. Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J 25:600-612.
87. Supale S, Thorel F, Merkwirth C, Gjinovci A, Herrera PL, Scorrano L, Meda P, Langer T, Maechler P. 2013. Loss of prohibitin induces mitochondrial damages altering β-cell function and survival and is responsible for gradual diabetes development. Diabetes 62:3488-3499.
88. Takahashi A, Kawasaki T, Wong HL, Suharsono U, Hirano H, Shimamoto K. 2003. Hyperphosphorylation of a mitochondrial protein, prohibitin, is induced by calyculin A in a rice lesion-mimic mutant cdr1. Plant Physiol 132:1861-1869.
89. Tatsuta T, Model K, Langer T. 2005. Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16:248-259.
90. Tavernarakis N, Driscoll M, Kyrpides NC. 1999. The SPFH domain: Implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem Sci 24:425-427.
91. Terashima M, Kim KM, Adachi T, Nielsen PJ, Reth KG, Lamers MC. 1994. The IgM antigen receptor of B lymphocytes is associated with prohibitin and a prohibitin-related protein. EMBO J 13:3782-3792.
92. Theiss AL, Idell RD, Srinivasan S, Klapproth JM, Jones DP, Merlin D, Sitaraman SV. 2007. Prohibitin protects against oxidative stress in intestinal epithelial cells. FASEB J 21:197-206.
93. Theiss AL, Vijay-Kumar M, Obertone TS, Jones DP, Hansen JM, Gewirtz AT, Merlin D, Sitaraman SV. 2009. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology 137:199-208.
94. Thompson WE, Sanbuissho A, Lee GY, Anderson E. 1997. Steroidogenic acute regulatory (StAR) protein (p25) and prohibitin (p28) from cultured rat ovarian granulosa cells. J Reprod Fertil 109:337-348.
95. Thompson WE, Powell JM, Whittaker JA, Sridaran R, Thomas KH. 1999. Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries. Anat Rec 256:40-48.
96. Thompson WE, Branch A, Whittaker JA, Lyn D, Zilberstein M, Mayo KE, Thomas K. 2001. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 142:4076-4085.
97. Thompson WE, Asselin E, Branch A, Stiles JK, Sutovsky P, Lai L, Im G-S, Prather RS, Isom SC, Rucker E III, Tsang B. 2004. Regulation of prohibitin expression during follicular development and atresia in the mammalian ovary. Biol Reprod 71:282-290.
98. Thuaud F, Ribeiro N, Nebigil CG. Désaubry L 2013. Prohibitin ligands in cell death and survival: Mode of action and therapeutic potential. Chem Biol 20:316-331.
99. Tsutsumi T, Matsuda M, Aizaki H, Moriya K, Miyoshi H, Fujie H, Shintani Y, Yotsuyanagi H, Miyamura T, Suzuki T, Koike K. 2009. Proteomics analysis of mitochondrial proteins reveals overexpression of a mitochondrial protein chaperon, prohibitin, in cells expressing hepatitis C virus core protein. Hepatology 50:378-386.
100. Ummanni R, Junker H, Zimmermann U, Venz S, Teller S, Giebel J, Scharf C, Woenckhaus C, Dombrowski F, Walther R. 2008. Prohibitin identified by proteomic analysis of prostate biopsies distinguishes hyperplasia and cancer. Cancer Lett 266:171-185.
101. Wang S, Nath N, Fusaro G, Chellappan S. 1999. Rb and prohibitin target distinct regions of E2F1 for repression and respond to different upstream signals. Mol Cell Biol 19:7447-7460.
102. Wang S, Zhang B, Faller DV. 2002. Prohibitin requires Brg-1 and Brm for the repression of E2F and cell growth. EMBO J 21:3019-3028.
103. Wang Q, Leader A, Tsang BK. 2013. Follicular stage-dependent regulation of apoptosis and steroidogenesis by prohibitin in rat granulosa cells. J Ovarian Res 6:23.
104. Welburn SC, Murphy NB. 1998. Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death Differ 5:615-622.
105. Wu TF, Wu H, Wang YW, Chang TY, Chan SH, Lin YP, Liu HS, Chow NH. 2007. Prohibitin in the pathogenesis of transitional cell bladder cancer. Anticancer Res 27:895-900.
106. Zhou TB, Qin YH, Zhou C, Lei FY, Zhao YJ, Chen J, Su LN, Huang WF. 2012. Less expression of prohibitin is associated with increased caspase-3 expression and cell apoptosis in renal interstitial fibrosis rats. Nephrology (Carlton) 17:189-196.
107. Zhu B, Zhai J, Zhu H, Kyprianou N. 2010. Prohibitin regulates TGF-beta induced apoptosis as a downstream effector of Smad-dependent and -independent signaling. Prostate 70:17-26.