Signaling pathways of prohibitin and its role in diseases

Journal of Receptors and Signal Transduction

Volumn 33, Issue 1, 2013, Pages 28-36

  Zhou, Tian Biao ^a   Qin, Yuan Han ^a  

^a FIRST AFFILIATED HOSPITAL OF GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

Cancer; Digestive diseases; Drug resistance; kidney diseases; Liver diseases; Lung diseases; Prohibitin; Signaling pathways

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CASPASE 3; COLLAGEN TYPE 4; FIBRONECTIN; PACLITAXEL; PROHIBITIN; PROHIBITIN 1; PROHIBITIN 2; REACTIVE OXYGEN METABOLITE; THYROTROPIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

3' UNTRANSLATED REGION; ALLERGIC AIRWAY INFLAMMATION; APOPTOSIS; AUTOPHAGY; BREAST CANCER; CANCER PROGNOSIS; CANCER RESISTANCE; CELL AGING; CELL CYCLE REGULATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC OBSTRUCTIVE LUNG DISEASE; COLITIS; CYTOPLASM; DIFFUSE LEWY BODY DISEASE; DISTANT METASTASIS; ENTERITIS; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; GASTROINTESTINAL DISEASE; GENE MUTATION; GENE SILENCING; GENE THERAPY; HUMAN; INTERSTITIAL NEPHRITIS; KIDNEY DISEASE; KIDNEY FIBROSIS; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER INJURY; LUNG DISEASE; LYMPH NODE METASTASIS; MITOCHONDRION; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PHYSIOLOGICAL PROCESS; PLEIOTROPY; PRECANCER; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; DIGESTIVE SYSTEM DISEASES; HUMANS; KIDNEY DISEASES; LIVER DISEASES; LUNG DISEASES; NEOPLASMS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84873125618     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.3109/10799893.2012.752006     Document Type: Review

References (127)

1. Nadimpalli R, Yalpani N, Johal GS, et al. Prohibitins, stomatins, and plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 2000;275:29579-86. (Pubitemid 32043836)
2. Mishra S, Murphy LC, Murphy LJ. The prohibitins: emerging roles in diverse functions. J Cell Mol Med 2006;10:353-363. (Pubitemid 44870184)
3. Chowdhury I, Garcia-Barrio M, Harp D, et al. The emerging roles of prohibitins in folliculogenesis. Front Biosci (Elite Ed) 2012; 4:690-9.
4. Altus MS, Wood CM, Stewart DA, et al. Regions of evolutionary conservation between the rat and human prohibitin-encoding genes. Gene 1995;158:291-4.
5. Asamoto M, Cohen SM. Prohibitin gene is overexpressed but not mutated in rat bladder carcinomas and cell lines. Cancer Lett 1994; 83:201-7. (Pubitemid 24253539)
6. Sievers C, Billig G, Gottschalk K, et al. Prohibitins are required for cancer cell proliferation and adhesion. PLoS One 2010;5:127-35.
7. Rajalingam K, Rudel T. Ras-Raf signaling needs prohibitin. Cell Cycle 2005;4:1503-5.
8. Osman C, Haag M, Potting C, et al. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J Cell Biol 2009;184:583-96.
9. Thompson WE, Branch A, Whittaker JA, et al. Characterization of prohibitin in a newly established rat ovarian granulosa cell line. Endocrinology 2001;142:4076-85. (Pubitemid 32807700)
10. Kim SY, Kim Y, Hwang HY, et al. Altered expression of prohibitin in psoriatic lesions and its cellular implication. Biochem Biophys Res Commun 2007;360:653-8. (Pubitemid 47048149)
11. Takahashi S, Masuda J, Shimagami H, et al. Mild caloric restriction up-regulates the expression of prohibitin: a proteome study. Biochem Biophys Res Commun 2011;405:462-7.
12. Xu DH, Tang J, Li QF, et al. Positional and expressive alteration of prohibitin during the induced differentiation of human hepatocarcinoma SMMC-7721 cells. World J Gastroenterol 2008; 14:5008-5014.
13. Shi SL, Li QF, Liu QR, et al. Nuclear matrix protein, prohibitin, was down-regulated and translocated from nucleus to cytoplasm during the differentiation of osteosarcoma MG-63 cells induced by ginsenoside Rg1, cinnamic acid, and tanshinone IIA (RCT). J Cell Biochem 2009;108:926-34.
14. Chander H, Halpern M, Resnick-Silverman L, et al. Skp2B overexpression alters a prohibitin-p53 axis and the transcription of PAPP-A, the protease of insulin-like growth factor binding protein 4. PLoS One 2011;6:224-56.
15. Wang S, Fusaro G, Padmanabhan J, et al. Prohibitin co-localizes with Rb in the nucleus and recruits N-CoR and HDAC1 for transcriptional repression. Oncogene 2002;21:8388-96. (Pubitemid 36054881)
16. Dixit VD, Sridaran R, Edmonsond MA, et al. Gonadotropinreleasing hormone attenuates pregnancy-associated thymic involution and modulates the expression of antiproliferative gene product prohibitin. Endocrinology 2003;144:1496-505. (Pubitemid 36428492)
17. Bourges I, Ramus C, de Mousson CB, et al. Structural organization of mitochondrial human complex I: role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem J 2004;383:491-9. (Pubitemid 39546119)
18. Rastogi S, Joshi B, Dasgupta P, et al. Prohibitin facilitates cellular senescence by recruiting specific corepressors to inhibit E2F target genes. Mol Cell Biol 2006;26:4161-71. (Pubitemid 43788018)
19. Osman C, Wilmes C, Tatsuta T, et al. Prohibitins interact genetically with Atp23, a novel processing peptidase and chaperone for the F1Fo-ATP synthase. Mol Biol Cell 2007;18:627-35. (Pubitemid 46213230)
20. Kuramori C, Azuma M, Kume K, et al. Capsaicin binds to prohibitin 2 and displaces it from the mitochondria to the nucleus. Biochem Biophys Res Commun 2009;379:519-25.
21. Rizwani W, Alexandrow M, Chellappan S. Prohibitin physically interacts with MCM proteins and inhibits mammalian DNA replication. Cell Cycle 2009;8:1621-9.
22. Paris LL, Hu J, Galan J, et al. Regulation of Syk by phosphorylation on serine in the linker insert. J Biol Chem 2010; 285:39844-54.
23. Ande SR, Mishra S. Palmitoylation of prohibitin at cysteine 69 facilitates its membrane translocation and interaction with Eps 15 homology domain protein 2 (EHD2). Biochem Cell Biol 2010; 88:553-8.
24. Choi D, Lee SJ, Hong S, et al. Prohibitin interacts with RNF2 and regulates E2F1 function via dual pathways. Oncogene 2008; 27:1716-25. (Pubitemid 351380260)
25. Christie DA, Lemke CD, Elias IM, et al. Stomatin-like protein 2 binds cardiolipin and regulates mitochondrial biogenesis and function. Mol Cell Biol 2011;31:3845-56.
26. Sun L, Liu L, Yang XJ, et al. Akt binds prohibitin 2 and relieves its repression of MyoD and muscle differentiation. J Cell Sci 2004; 117:3021-9. (Pubitemid 39117676)
27. Roskams AJ, Friedman V, Wood CM, et al. Cell cycle activity and expression of prohibitin mRNA. J Cell Physiol 1993;157:289-95. (Pubitemid 23332772)
28. Wang S, Nath N, Adlam M, et al. Prohibitin, a potential tumor suppressor, interacts with RB and regulates E2F function. Oncogene 1999;18:3501-10. (Pubitemid 29317345)
29. Tyc J, Faktorova D, Kriegova E, et al. Probing for primary functions of prohibitin in Trypanosoma brucei. Int J Parasitol 2010;40:73-83.
30. Ross JA, Nagy ZS, Kirken RA. The PHB1/2 phosphocomplex is required for mitochondrial homeostasis and survival of human T cells. J Biol Chem 2008;283:4699-713.
31. Sun Q, Miao M, Jia X, et al. Subproteomic analysis of the mitochondrial proteins in rats 24 h after partial hepatectomy. J Cell Biochem 2008;105:176-84.
32. Berger KH, Yaffe MP. Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 1998;18:4043-52. (Pubitemid 28287928)
33. Thompson WE, Ramalho-Santos J, Sutovsky P. Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 2003;69:254-60. (Pubitemid 36806830)
34. Steglich G, Neupert W, Langer T. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 1999;19:3435-42. (Pubitemid 29193803)
35. Kasashima K, Sumitani M, Satoh M, et al. Human prohibitin 1 maintains the organization and stability of the mitochondrial nucleoids. Exp Cell Res 2008;314:988-96.
36. Mao HT, Wang DH, Lan Z, et al. Gene expression profiles of prohibitin in testes of Octopus tankahkeei (ot-phb) revealing its possible role during spermiogenesis. Mol Biol Rep 2012; 39:5519-28.
37. Mao H, Wang DH, Zhou H, et al. Characterization and expression analysis of prohibitin in the testis of Chinese mitten crab Eriocheir sinensis. Mol Biol Rep 2012;39:7031-9.
38. Zhou P, Qian L, D'Aurelio M, et al. Prohibitin reduces mitochondrial free radical production and protects brain cells from different injury modalities. J Neurosci 2012;32:583-92.
39. Kathiria AS, Butcher LD, Feagins LA, et al. Prohibitin 1 modulates mitochondrial stress-related autophagy in human colonic epithelial cells. PLoS One 2012;7:312-31.
40. Liu D, Lin Y, Kang T, et al. Mitochondrial Dysfunction and Adipogenic Reduction by Prohibitin Silencing in 3T3-L1 Cells. PLoS One 2012;7:34315.
41. Chowdhury I, Branch A, Olatinwo M, et al. Prohibitin (PHB) acts as a potent survival factor against ceramide induced apoptosis in rat granulosa cells. Life Sci 2011;89:295-303.
42. Jia YH, Zhang YX, Li LJ, et al. Dingxin recipe () prevents ischemia/reperfusion-induced arrhythmias via up-regulating prohibitin and suppressing inflammatory responses. Chin J Integr Med 2012;18:120-9.
43. Liu X, Ren Z, Zhan R, et al. Prohibitin protects against oxidative stress-induced cell injury in cultured neonatal cardiomyocyte. Cell Stress Chaperones 2009;14:311-19.
44. Lee JH, Nguyen KH, Mishra S, et al. Prohibitin is expressed in pancreatic beta-cells and protects against oxidative and proapoptotic effects of ethanol. FEBS J 2010;277:488-500.
45. Ande SR, Mishra S. Nuclear coded mitochondrial protein prohibitin is an iron regulated iron binding protein. Mitochondrion 2011; 11:40-7.
46. Dong P, Flores J, Pelton K, et al. Prohibitin is a cholesterolsensitive regulator of cell cycle transit. J Cell Biochem 2010;111:1367-74.
47. He B, Kim TH, Kommagani R, et al. Estrogen-regulated prohibitin is required for mouse uterine development and adult function. Endocrinology 2011;152:1047-56.
48. Coates PJ, Nenutil R, McGregor A, et al. Mammalian prohibitin proteins respond to mitochondrial stress and decrease during cellular senescence. Exp Cell Res 2001;265:262-73. (Pubitemid 32980214)
49. Jia L, Yi XF, Zhang ZB, et al. Prohibitin as a novel target protein of luteinizing hormone in ovarian epithelial carcinogenesis. Neoplasma 2011;58:104-9.
50. Ande SR, Gu Y, Nyomba BL, et al. Insulin induced phosphorylation of prohibitin at tyrosine 114 recruits Shp1. Biochim Biophys Acta 2009;1793:1372-78.
51. Zhang W, Ambati S, Della-Fera MA, et al. Leptin modulated changes in adipose tissue protein expression in ob/ob mice. Obesity (Silver Spring) 2011;19:255-61.
52. Ande SR, Xu Z, Gu Y, et al. Prohibitin has an important role in adipocyte differentiation. Int J Obes (Lond) 2012;36:1236-44.
53. Liu T, Tang H, Lang Y, et al. MicroRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett 2009;273:233-42.
54. Mooso B, Madhav A, Johnson S, et al. Androgen receptor regulation of Vitamin D receptor in response of castration-resistant prostate cancer cells to 1alpha-Hydroxyvitamin D5 - a calcitriol analog. Genes Cancer 2010;1:927-40.
55. Da CS, Parone PA, Gonzalo P, et al. SLP-2 interacts with prohibitins in the mitochondrial inner membrane and contributes to their stability. Biochim Biophys Acta 2008; 1783:904-11.
56. Pabona JM, Velarde MC, Zeng Z, et al. Nuclear receptor co-regulator Kruppel-like factor 9 and prohibitin 2 expression in estrogen-induced epithelial cell proliferation in the mouse uterus. J Endocrinol 2009;200:63-73.
57. Liu YH, Peck K, Lin JY. Involvement of prohibitin upregulation in abrin-triggered apoptosis. Evid-Based Complement Alternat Med 2012;2012:605154.
58. Jia Y, Zhou F, Deng P, et al. Interleukin 6 protects H(2) O(2)-induced cardiomyocytes injury through upregulation of prohibitin via STAT3 phosphorylation. Cell Biochem Funct 2012; 30:426-31.
59. Theiss AL, Obertone TS, Merlin D, et al. Interleukin-6 transcriptionally regulates prohibitin expression in intestinal epithelial cells. J Biol Chem 2007;282:12804-12. (Pubitemid 47100634)
60. Han EK, Mcgonigal T, Butler C, et al. Characterization of Akt overexpression in MiaPaCa-2 cells: prohibitin is an Akt substrate both in vitro and in cells. Anticancer Res 2008;28:957-63. (Pubitemid 351578942)
61. Heron-Milhavet L, Mamaeva D, Rochat A, et al. Akt2 is implicated in skeletal muscle differentiation and specifically binds prohibitin2/ REA. J Cell Physiol 2008;214:158-65. (Pubitemid 350220070)
62. Kategaya LS, Hilliard A, Zhang L, et al. Casein kinase 1 proteomics reveal prohibitin 2 function in molecular clock. PLoS One 2012;7:31987.
63. Dart DA, Spencer-Dene B, Gamble SC, et al. Manipulating prohibitin levels provides evidence for an in vivo role in androgen regulation of prostate tumours. Endocr Relat Cancer 2009;16:1157-69.
64. Gamble SC, Chotai D, Odontiadis M, et al. Prohibitin, a protein downregulated by androgens, represses androgen receptor activity. Oncogene 2007;26:1757-68. (Pubitemid 46426196)
65. Fusaro G, Wang S, Chellappan S. Differential regulation of Rb family proteins and prohibitin during camptothecin-induced apoptosis. Oncogene 2002;21:4539-48. (Pubitemid 34785730)
66. Joshi B, Rastogi S, Morris M, et al. Differential regulation of human YY1 and caspase 7 promoters by prohibitin through E2F1 and p53 binding sites. Biochem J 2007;401:155-66. (Pubitemid 46114609)
67. Artal-Sanz M, Tsang WY, Willems EM, et al. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem 2003;278:32091-9. (Pubitemid 37048398)
68. Kirchman PA, Miceli MV, West RL, et al. Prohibitins and Ras2 protein cooperate in the maintenance of mitochondrial function during yeast aging. Acta Biochim Pol 2003;50:1039-56. (Pubitemid 38608834)
69. Ahn CS, Lee JH, Reum HA, et al. Prohibitin is involved in mitochondrial biogenesis in plants. Plant J 2006;46:658-67.
70. Chen JC, Jiang CZ, Reid MS. Silencing a prohibitin alters plant development and senescence. Plant J 2005;44:16-24.
71. Vessal M, Mishra S, Moulik S, et al. Prohibitin attenuates insulinstimulated glucose and fatty acid oxidation in adipose tissue by inhibition of pyruvate carboxylase. FEBS J 2006;273:568-76.
72. Sanchez-Quiles V, Santamaria E, Segura V, et al. Prohibitin deficiency blocks proliferation and induces apoptosis in human hepatoma cells: molecular mechanisms and functional implications. Proteomics 2010;10:1609-20.
73. Muraguchi T, Kawawa A, Kubota S. Prohibitin protects against hypoxia-induced H9c2 cardiomyocyte cell death. Biomed Res 2010;31:113-22.
74. Yang P, Jia YH, Li J, et al. Study of anti-myocardial cell oxidative stress action and effect of tanshinone IIA on prohibitin expression. J Tradit Chin Med 2010;30:259-64.
75. Theiss AL, Vijay-Kumar M, Obertone TS, et al. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology 2009;137:199-208.
76. Theiss AL, Laroui H, Obertone TS, et al. Nanoparticle-based therapeutic delivery of prohibitin to the colonic epithelial cells ameliorates acute murine colitis. Inflamm Bowel Dis 2011; 17:1163-76.
77. Schleicher M, Shepherd BR, Suarez Y, et al. Prohibitin-1 maintains the angiogenic capacity of endothelial cells by regulating mitochondrial function and senescence. J Cell Biol 2008; 180:101-12.
78. Tsutsumi T, Matsuda M, Aizaki H, et al. Proteomics analysis of mitochondrial proteins reveals overexpression of a mitochondrial protein chaperon, prohibitin, in cells expressing hepatitis C virus core protein. Hepatology 2009;50:378-86.
79. Fusaro G, Dasgupta P, Rastogi S, et al. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. J Biol Chem 2003;278:47853-61. (Pubitemid 37523233)
80. He B, Feng Q, Mukherjee A, et al. A repressive role for prohibitin in estrogen signaling. Mol Endocrinol 2008;22:344-60. (Pubitemid 351185935)
81. Sato S, Murata A, Orihara T, et al. Marine natural product aurilide activates the OPA1-mediated apoptosis by binding to prohibitin. Chem Biol 2011;18:131-9.
82. Merkwirth C, Dargazanli S, Tatsuta T, et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1- dependent cristae morphogenesis in mitochondria. Genes Dev 2008;22:476-88. (Pubitemid 351272755)
83. Ko KS, Tomasi ML, Iglesias-Ara A, et al. Liver-specific deletion of prohibitin 1 results in spontaneous liver injury, fibrosis, and hepatocellular carcinoma in mice. Hepatology 2010;52:2096-108.
84. Rajalingam K, Wunder C, Brinkmann V, et al. Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat Cell Biol 2005;7:837-43. (Pubitemid 41079057)
85. Kasashima K, Ohta E, Kagawa Y, et al. Mitochondrial functions and estrogen receptor-dependent nuclear translocation of pleiotropic human prohibitin 2. J Biol Chem 2006;281:36401-10. (Pubitemid 46041374)
86. Ande SR, Mishra S. Prohibitin interacts with phosphatidylinositol 3,4,5-triphosphate (PIP3) and modulates insulin signaling. Biochem Biophys Res Commun 2009;390:1023-8.
87. Wang S, Zhang B, Faller DV. Prohibitin requires Brg-1 and Brm for the repression of E2F and cell growth. Embo J 2002;21:3019-28. (Pubitemid 34670386)
88. Chander H, Halpern M, Resnick-Silverman L, et al. Skp2B attenuates p53 function by inhibiting prohibitin. EMBO Rep 2010;11:220-5.
89. Sun L, Cao X, Liu B, et al. CaMK IV phosphorylates prohibitin 2 and regulates prohibitin 2-mediated repression of MEF2 transcription. Cell Signal 2011;23:1686-90.
90. Mengwasser J, Piau A, Schlag P, et al. Differential immunization identifies PHB1/PHB2 as blood-borne tumor antigens. Oncogene 2004;23:7430-5. (Pubitemid 39382145)
91. Kang X, Zhang L, Sun J, et al. Prohibitin: a potential biomarker for tissue-based detection of gastric cancer. J Gastroenterol 2008; 43:618-25.
92. Ren HZ, Wang JS, Wang P, et al. Increased expression of prohibitin and its relationship with poor prognosis in esophageal squamous cell carcinoma. Pathol Oncol Res 2010;16:515-22.
93. Chen D, Chen F, Lu X, et al. Identification of prohibitin as a potential biomarker for colorectal carcinoma based on proteomics technology. Int J Oncol 2010;37:355-65.
94. Kakehashi A, Ishii N, Shibata T, et al. Mitochondrial prohibitins and septin 9 are implicated in the onset of rat hepatocarcinogenesis. Toxicol Sci 2011;119:61-72.
95. Xu Z, Wu J, Zha X. Up-regulation of prohibitin 1 is involved in the proliferation and migration of liver cancer cells. SCI China Life Sci 2011;54:121-7.
96. Tsai HW, Chow NH, Lin CP, et al. The significance of prohibitin and c-Met/hepatocyte growth factor receptor in the progression of cervical adenocarcinoma. Hum Pathol 2006;37: 198-204.
97. Peng X, Mehta R, Wang S, et al. Prohibitin is a novel target gene of vitamin D involved in its antiproliferative action in breast cancer cells. Cancer Res 2006;66:7361-9. (Pubitemid 44197720)
98. Peng X, Mehta RG. Differential expression of prohibitin is correlated with dual action of Vitamin D as a proliferative and antiproliferative hormone in breast epithelial cells. J Steroid Biochem Mol Biol 2007;103:446-50. (Pubitemid 46401287)
99. Jupe ER, Liu XT, Kiehlbauch JL, et al. Prohibitin in breast cancer cell lines: loss of antiproliferative activity is linked to 30 untranslated region mutations. Cell Growth Differ 1996;7:871-8. (Pubitemid 26360726)
100. Zhu B, Fukada K, Zhu H, et al. Prohibitin and cofilin are intracellular effectors of transforming growth factor beta signaling in human prostate cancer cells. Cancer Res 2006;66:8640-7. (Pubitemid 44449179)
101. Fletcher CE, Dart DA, Sita-Lumsden A, et al. Androgen-regulated processing of the oncomir MiR-27a, which targets prohibitin in prostate cancer. Hum Mol Genet 2012;21:3112-27.
102. Ummanni R, Junker H, Zimmermann U, et al. Prohibitin identified by proteomic analysis of prostate biopsies distinguishes hyperplasia and cancer. Cancer Lett 2008;266:171-85.
103. Wu TF, Wu H, Wang YW, et al. Prohibitin in the pathogenesis of transitional cell bladder cancer. Anticancer Res 2007;27: 895-900. (Pubitemid 46586996)
104. Franzoni A, Dima M, D'Agostino M, et al. Prohibitin is overexpressed in papillary thyroid carcinomas bearing the BRAF(V600E) mutation. Thyroid 2009;19:247-55.
105. Woodlock TJ, Bethlendy G, Segel GB. Prohibitin expression is increased in phorbol ester-treated chronic leukemic B-lymphocytes. Blood Cells Mol Dis 2001;27:27-34. (Pubitemid 32299751)
106. Jakubowska A, Gronwald J, Gorski B, et al. The 30 untranslated region C4T polymorphism of prohibitin is a breast cancer risk modifier in Polish women carrying a BRCA1 mutation. Breast Cancer Res Treat 2007;104:67-74. (Pubitemid 46976630)
107. Manjeshwar S, Branam DE, Lerner MR, et al. Tumor suppression by the prohibitin gene 30 untranslated region RNA in human breast cancer. Cancer Res 2003;63:5251-6. (Pubitemid 37139838)
108. Campbell IG, Allen J, Eccles DM. Prohibitin 30 untranslated region polymorphism and breast cancer risk. Cancer Epidemiol Biomarkers Prev 2003;12:1273-4. (Pubitemid 37499458)
109. Karakus N, Kara N, Ulusoy AN. Lack of association between prohibitin 30 untranslated region C-4T polymorphism and breast cancer in a Turkish population. Dna Cell Biol 2008;27: 449-52.
110. Grimm C, Polterauer S, Zeillinger R, et al. The prohibitin 30 untranslated region polymorphism in patients with ovarian cancer. Eur J Obstet Gynecol Reprod Biol 2008;137:236-9. (Pubitemid 351423456)
111. Jakubowska A, Gronwald J, Menkiszak J, et al. Ovarian cancer risk in Polish BRCA1 mutation carriers is not associated with the prohibitin 30 untranslated region polymorphism. BMC Cancer 2008;8:90.
112. Spurdle AB, Purdie DM, Chen X, et al. The prohibitin 30 untranslated region polymorphism is not associated with risk of ovarian cancer. Gynecol Oncol 2003;90:145-9. (Pubitemid 37338089)
113. Tanno S, Fukuda I, Saito Y, et al. Prohibitin expression is decreased in the regenerating liver but not in chemically induced hepatic tumors in rats. Jpn J Cancer Res 1997;88:1155-64. (Pubitemid 28048262)
114. Wang B, Wang S, Shao C, et al. Proteomic characterization of the late and persistent effects of cadmium at low doses on the rat liver. J Appl Toxicol 2011. doi: 10.1002/jat.1757.
115. Guo W, Xu H, Chen J, et al. Prohibitin suppresses renal interstitial fibroblasts proliferation and phenotypic change induced by transforming growth factor-beta1. Mol Cell Biochem 2007; 295:167-77. (Pubitemid 46157999)
116. Guo W, Xu H, Huang WY, et al. Prohibitin suppresses renal interstitial fibroblasts proliferation and phenotypic change induced by transforming growth factor-beta1. Zhonghua Yi Xue Za Zhi 2007;87:1660-5. (Pubitemid 47316229)
117. Wu HZ, Guo L, Mak YF, et al. Proteomics investigation on aristolochic acid nephropathy: a case study on rat kidney tissues. Anal Bioanal Chem 2011;399:3431-9.
118. Zhou TB, Qin YH, Zhou C, et al. Less expression of prohibitin is associated with increased Caspase-3 expression and cell apoptosis in renal interstitial fibrosis rats. Nephrology (Carlton) 2012; 17:189-96.
119. Zhou TB, Qin YH, Li ZY, et al. All-trans retinoic Acid treatment is associated with prohibitin expression in renal interstitial fibrosis rats. Int J Mol Sci 2012;13:2769-82.
120. Soulitzis N, Neofytou E, Psarrou M, et al. Downregulation of lung mitochondrial prohibitin in COPD. Respir Med 2012;106: 954-61.
121. Agrawal T, Gupta GK, Agrawal DK. Vitamin D deficiency decreases the expression of VDR and prohibitin in the lungs of mice with allergic airway inflammation. Exp Mol Pathol 2012;93:74-81.
122. Smalla KH, Mikhaylova M, Sahin J, et al. A comparison of the synaptic proteome in human chronic schizophrenia and rat ketamine psychosis suggest that prohibitin is involved in the synaptic pathology of schizophrenia. Mol Psychiatry 2008; 13:878-96.
123. Ferrer I, Perez E, Dalfo E, et al. Abnormal levels of prohibitin and ATP synthase in the substantia nigra and frontal cortex in Parkinson's disease. Neurosci Lett 2007;415:205-9. (Pubitemid 46420396)
124. Gregory-Bass RC, Olatinwo M, Xu W, et al. Prohibitin silencing reverses stabilization of mitochondrial integrity and chemoresistance in ovarian cancer cells by increasing their sensitivity to apoptosis. Int J Cancer 2008;122:1923-30. (Pubitemid 351441180)
125. Cao L, Li X, Zhang Y, et al. Proteomic analysis of human ovarian cancer paclitaxel-resistant cell lines. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2010;35:286-94.
126. Zubovych IO, Straud S, Roth MG. Mitochondrial dysfunction confers resistance to multiple drugs in Caenorhabditis elegans. Mol Biol Cell 2010;21:956-69.
127. Dai Z, Yin J, He H, et al. Mitochondrial comparative proteomics of human ovarian cancer cells and their platinum-resistant sublines. Proteomics 2010;10:3789-99.