Heat shock proteins in prostate cancer: from tumorigenesis to the clinic

References

• Delongchamps NB, Singh A, Hass GP. Epidemiology of prostate cancer in Africa: Another step in the understanding of the disease?. Curr Probl Cancer 2007; 31: 226–236
   PubMedGoogle Scholar
• Rubin MA. Targeted therapy of cancer: New roles for pathologists – prostate cancer. Mod Pathol 2008; 21: S44–55
   PubMed Web of Science ®Google Scholar
• Sharifi N, Dahut WL, Figg WD. Secondary hormonal therapy for prostate cancer: What lies on the horizon?. BJU Int 2008; 101: 271–274
   PubMed Web of Science ®Google Scholar
• Brawley OW, Ankerst DP, Thompson IM. Screening for prostate cancer. CA Cancer J Clin 2009; 59: 264–273
   PubMed Web of Science ®Google Scholar
• Shinohara K. Thermal ablation of prostate diseases: Advantages and limitations. Int J Hyperthermia 2004; 20: 679–697
   PubMed Web of Science ®Google Scholar
• Hurwitz MD, Kaplan ID, Hansen JL, Prokopios-Davos S, Topulos GP, Wishnow K, Manola J, Bornstein BA, Hynynen K. Hyperthermia combined with radiation treatment of locally advanced prostate cancer is associated with favourable toxicity profile. Int J Hyperthermia 2005; 21: 649–656
   PubMed Web of Science ®Google Scholar
• Latorre M, Rinaldi C. Application of magnetic nanoparticles in medicine: Magnetic fluid hyperthermia. P R Health Sci 2009; 28: 227–238
   PubMed Web of Science ®Google Scholar
• Baronzio G, Gramaglia A, Fiorentini G. Review. Current role and future perspectives of hyperthermia for prostate cancer treatment. In vivo 2009; 23: 143–146
   Google Scholar
• Schlesinger MJ. How the cell copes with stress and the function of heat shock proteins. Pediatr Res 1994; 36: 1–6
   PubMed Web of Science ®Google Scholar
• Khoei S, Goliaei B, Neshasteh-Riz A, Deizadji A. The role of heat shock protein 70 in the thermoresistance of prostate cancer cell line spheroids. FEBS Lett 2004; 561: 144–148
   PubMed Web of Science ®Google Scholar
• Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: Chaperones of tumorigenesis. Trends Biochem Sci 2006; 31: 164–172
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Fanelli MA, Cuello-Carrion FD, Calderwood SK. Implications of heat shock proteins in carcinogenesis and cancer progression. In: Calderwood SK, Sherman MY, Ciocca DR, editors. Heat Shock Proteins in Cancer. The Netherlands, Dordrecht: Springer; 2007. pp 31–51.
   Google Scholar
• Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Chetham ME, Chen B, Hightower LE. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009; 14: 105–111
   PubMed Web of Science ®Google Scholar
• Linquist S, Craig EA. The heat shock proteins. Ann Rev Genet 1988; 22: 631–637
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Oesterreich GC, Chamness GC, McGuire WL, Fuqua SAW. Heat shock protein 27,000 (HSP 27): Biological and clinical implications. J Natl Cancer Inst 1993; 85: 1558–1570
   PubMed Web of Science ®Google Scholar
• Wegele H, Müller L, Buchner J. Hsp70 and Hsp90 – A relay team for protein folding. Rev Physiol Biochem Pharmacol 2004; 151: 1–44
   PubMed Web of Science ®Google Scholar
• Sandqvist A, Björk JK, Akerfelt M, Chitikova Z, Grichine A, Vourćh C, Jolly C, Salminen TA, Nymalm Y, Sistonen L. Heterotrimerization of heat-shock factors 1 and 2 provided a transcriptional switch in response to distinct stimuli. Mol Biol Cell 2009; 20: 1340–1347
   PubMed Web of Science ®Google Scholar
• Westerheide SD, Anckar J, Stevens SM, Jr, Sistonen L, Morimoto RI. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 2009; 323: 1063–1066
   PubMed Web of Science ®Google Scholar
• Khaleque MA, Bharti A, Gong J, Gary PJ, Sachdev V, Ciocca DR, Stati A, Fanelli MA, Calderwood SK. Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene 2008; 27: 1886–1893
   PubMed Web of Science ®Google Scholar
• Calderwood SK, Ciocca DR, Gray PJ, Zaarur N, Lepchammer S, Sherman MY. The elevated levels of heat shock proteins in cancer: A suitable case for treatment? In: Calderwood SK, Sherman MY, Ciocca DR, editors. Heat Shock Proteins in Cancer. The Netherlands, Dordrecht: Springer. 2007. pp 351–365.
   Google Scholar
• Ciocca DR, Fanelli MA, Cuello-Carrion FD, Castro GN. Small stress proteins, biomarkers of cancer. In: Arrigo AP, Simon S, editors. Small Stress Proteins in Human Diseases. New York: Nova Science Pub. 2010 (in press).
   Google Scholar
• Takahashi A, Yamakawa N, Mori E, Ohnishi K, Yokota S, Sugo N, Aratani Y, Koyama H, Ohnishi T. Development of thermotolerance requires interaction between polymerase-beta and heat shock proteins. Cancer Sci 2008; 99: 973–978
   PubMed Web of Science ®Google Scholar
• Teimourian S, Jalal R, Sohrabpour M, Goliaei B. Down-regulation of Hsp27 radiosensitizes prostate cancer cells. Internat J Urology 2006; 13: 1221–1225
   PubMedGoogle Scholar
• Rocchi P, Jugpal P, So A, Sinneman S, Ettinger S, Fazli L, Nelson C, Gleave M. Small interference RNA targeting heat shock protein 27 inhibits the growth of prostatic cell lines and induces apoptosis via caspase-3 activation in vitro. BJU International 2006; 98: 1082–1089
   PubMed Web of Science ®Google Scholar
• Andrieu C, Taieb D, Baylot V, Ettinger S, Soubeyran P, De-Thonel A, Nelson C, Garrido C, So A, Fazli L, et al. Heat shock protein 27 confers resistance to androgen ablation and chemotherapy in prostate cancer cells through eIF4E. Oncogene 2010;29:1883–1896.
   Google Scholar
• Aagaard L, Rossi JJ. RNAi therapeutics: Principles, prospects and challenges. Adv Drug Delivery Rev 2007; 59: 75–86
   PubMed Web of Science ®Google Scholar
• Zhou JH, Wu JY, Hafdi N, Behr J-P, Erbacher P, Peng L. PAMAM dendrimers for efficient siRNA delivery and potent gene silencing. Chem Commun 2006; 22: 2362–2364
   PubMed Web of Science ®Google Scholar
• Liu X, Rocchi P, Qu F, Zheng S, Liang Z, Gleave M, Iovanna J, Peng L. PAMAM dendrimers mediate siRNA delivery to target Hsp27 and produce potent antiproliferative effects on prostate cancer cells. Chem Med Chem 2009; 4: 1302–1310
   Web of Science ®Google Scholar
• Lu S, Tan Z, Wortman M, Lu S, Dong Z. Regulation of heat shock protein 70-1 expression by androgen receptor and its signaling in human prostate cancer cells. Int J Oncol 2010; 36: 459–467
   PubMed Web of Science ®Google Scholar
• Solit DB, Scher HI, Rosen N. Hsp90 as a therapeutic target in prostate cancer. Semin Oncol 2003; 30: 709–716
   PubMed Web of Science ®Google Scholar
• Matthews S, Vielhauer G, Manthe C, Chaguturu V, Szabla K Matts R, Donnelly A, Blagg B, Holzbeiertein J. Characterization of a novel novobiocin analogue as a putative C-teminal inhibitor of heat shock protein 90 in prostate cancer cells. Prostate 2010; 70: 27–36
   PubMed Web of Science ®Google Scholar
• Aalinkeel R, Bindukumar B, Reynolds J, Sykes D, Mahaian S, Chadha K, Schwartz S. The dietary bioflavonoid, quercetin, selectively induces apoptosis of prostate cancer cells by down regulating the expression of heat shock protein 90. Prostate 2008; 68: 1773–1789
   PubMed Web of Science ®Google Scholar
• Ai J, Wang Y, Dar JA, Liu J, Liu L, Nelson JB, Wang Z. HDAC6 regulates androgen receptor hypersensitivity and nuclear localization via modulating Hsp90 acetylation in castration-resistant prostate cancer. Mol Endocrinol 2009; 23: 1963–1972
   PubMedGoogle Scholar
• Leav I, Plescia J, Goel HL, Li J, Jiang Z, Cohen RJ, Languino LR, Altieri DC. Cytoprotective mitochondrial chaperone TRAP-1 as a novel molecular target in localized and metastatic prostate cancer. Am J Pathol 2010;176:393–401.
   Google Scholar
• Zhang H, Kim JK, Edwards CA, Xu Z, Taichman R, Wang CY. Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 2005; 7: 909–915
   PubMed Web of Science ®Google Scholar
• Steinberg J, Oyasu R, Lang S, Sintich S, Rademaken A, Lee C, Kozlowski JM, Sensiban JA. Intracellular levels of SGP-2 (Clusterin) correlate with tumor grade in prostate cancer. Clin Cancer Res 1997; 3: 1707–1711
   PubMed Web of Science ®Google Scholar
• July LV, Akbari M, Zellweger T, Jones EC, Goldenberg SL, Gleave ME. Clusterin expression is significantly enhanced in prostate cancer cells following androgen withdrawal therapy. Prostate 2002; 50: 179–188
   PubMed Web of Science ®Google Scholar
• Sowery R, Hadaschik B, So A, Zoubeidi A, Fazli L, Hurtado-Coll A, Gleave M. Clusterin knockdown using the antisense oligonucleotide OGX-011 re-sensitizes docetaxel-refractory prostate cancer PC-3 cells to chemotherapy. Br J Urol Int 2008; 102: 389–397
   Google Scholar
• Glen A, Gan C, Hamdy F, Eaton C, Cross S, Catto J, Wright P, Rehman I. iTRAQ-facilitated proteomic analysis of human prostate cancer cells identifies proteins associated with progression. J Proteome Res 2008; 7: 897–907
   PubMed Web of Science ®Google Scholar
• Mintz PJ, Kim J, Do KA, Wang X, Zinner RG, Cristofanilli M, Arap MA, Hong WK, Troncoso P, Logothetis CJ, Pasqualini R, Arap W. Fingerprinting the circulating repertoire of antibodies from cancer patients. Nat Biotechnol 2003; 21: 57–63
   PubMed Web of Science ®Google Scholar
• Wu Y, Zhang H, Dong Y, Park YM, Ip C. Endoplasmic reticulum stress signal mediators are targets of selenium action. Cancer Res 2005; 65: 9073–9079
   PubMed Web of Science ®Google Scholar
• Pootrakul L, Datar RH, Shi SR, Cai J, Hawes D, Groshen SG, Lee AS, Cote RJ. Expression of stress response protein Grp78 is associated with the development of castration-resistant prostate cancer. Clin Cancer Res 2006; 12: 5987–5993
   PubMed Web of Science ®Google Scholar
• Miyake H, Hara I, Arakawa S, Kamidono S. Stress protein GRP78 prevents apoptosis induced by calcium ionophore, ionomycin, but not by glycosylation inhibitor, tunicamycin, in human prostate cancer cells. J Cell Biochem 2000; 77: 396–408
   PubMed Web of Science ®Google Scholar
• Yang Y, Li Z. Roles of heat shock protein gp96 in the ER quality control: Redundant or unique function. Mol Cells 2005; 20: 173–182
   PubMed Web of Science ®Google Scholar
• PeibinY, Shude Y, Changzhi H. Heat shock protein gp96 and cancer immunotherapy. Chin Med Sci J 2002; 17: 251–256
   PubMedGoogle Scholar
• Suriano R, Ghosh S K, Ashok BT, Mittelman A, Chen Y, Banerjee A, Tiwari RK. Differences in glycosylation patterns of heat shock protein, gp96: Implications for prostate cancer prevention. Cancer Res 2005; 65: 6466–6475
   PubMed Web of Science ®Google Scholar
• Gao P, Sun X, Chen X, Subjeck J, Wang X. Secretion of stress protein grp170 promotes immune-mediated inhibition of murine prostate tumor. Cancer Immunol Immunother 2009; 58: 1319–1328
   PubMed Web of Science ®Google Scholar
• Lipinski K, Pelech S, Mountain A, Irvine A, Kraaij R, Bangma C, Mills K, Todryk S. Nitroreductase-based therapy of prostate cancer, enhanced by raising expression of heat shock protein 70, acts through increased anti-tumour immunity. Cancer Immunol Immunother 2006; 55: 347–354
   PubMed Web of Science ®Google Scholar
• Gonzalez-Gronow M, Cuchacovich M, Llanos C, Urzua C, Gawdi G, Pizzo1 S. Prostate cancer cell proliferation in vitro is modulated by antibodies against glucose-regulated protein 78 isolated from patient serum. Cancer Res 2006; 66: 11424–11431
   PubMed Web of Science ®Google Scholar
• Byun J, Logothetis CJ, Gorlov IP. Housekeeping genes in prostate tumorigenesis. Int J Cancer 2009; 125: 2603–2608
   PubMed Web of Science ®Google Scholar
• Ummanni R, Junker H, Zimmermann U, Venz S, Teller S, Giebel J, Scharf C, Woenckhaus C, Dombrowski F, Walther R. Prohibitin identified by proteomic analysis of prostate biopsies distinguishes hyperplasia and cancer. Cancer Lett 2008; 266: 171–185
   PubMed Web of Science ®Google Scholar
• Lin JF, Xu J, Tian HY, Gao X, Chen QX, Gu Q, Xu GJ, Song JD, Zhao FK. Identification of candidate prostate cancer biomarkers in prostate needle biopsy specimens using proteomic analysis. Int J Cancer 2007; 121: 2596–2605
   PubMed Web of Science ®Google Scholar
• Howard EW, Leung SC, Yuen HF, Chua CW, Lee DT, Chan KW, Wang X, Wong YC. Decreased adhesiveness, resistance to anoikis and suppression of GRP94 are integral to the survival of circulating tumor cells in prostate cancer. Clin Exp Metastasis 2008; 25: 497–508
   PubMed Web of Science ®Google Scholar
• Elmore LW, Forsythe R, Forsythe H, Bright AT, Nasim S, Endo K, Holt SE. Overexpression of telomerase-associated chaperone proteins in prostatic intraepithelial neoplasia and carcinomas. Oncol Rep 2008; 20: 613–617
   PubMed Web of Science ®Google Scholar
• Cardillo MR, Ippoliti F. IL-6, IL-10 and HSP-90 expression in tissue microarrays from human prostate cancer assessed by computer-assisted image analysis. Anticancer Res 2006; 26: 3409–3416
   PubMed Web of Science ®Google Scholar
• Mori R, Wang Q, Danenberg KD, Pinski JK, Danenberg PV. Both beta-actin and GAPDH are useful reference genes for normalization of quantitative RT-PCR in human FFPE tissue samples of prostate cancer. Prostate 2008; 68: 1555–1560
   PubMed Web of Science ®Google Scholar
• Sfar S, Saad H, Mosbah F, Chouchane L. Association of HSP70-hom genetic variant with prostate cancer risk. Mol Biol Rep 2008; 35: 459–464
   PubMed Web of Science ®Google Scholar
• Lexander H, Palmberg C, Auer G, Hellström M, Franzén B, Jörnvall H, Egevad L. Proteomic analysis of protein expression in prostate cancer. Anal Quant Cytol Histol 2005; 27: 263–272
   PubMedGoogle Scholar
• Cappello F, Ribbene A, Campanella C, Czarnecka AM, Anzalone R, Bucchieri F, Palma A, Zummo G. The value of immunohistochemical research on PCNA, p53 and heat shock proteins in prostate cancer management: A review. Eur J Histochem 2006; 50: 25–34
   PubMed Web of Science ®Google Scholar
• Zhen B, Shen Y, Zhang YM, Zhu CH, Liu ZL. Analysis of the differences in the expression of HSP27 and c-kit between benign prostatic hyperplasia and prostatic cancer tissues. Zhonghua Nan Ke Xue 2006; 12: 416–420
   PubMedGoogle Scholar
• Buchanan G, Ricciardelli C, Harris JM, Prescott J, Yu ZC, Jia L, Butler LM, Marshall VR, Scher HI, Gerald WL, et al. Control of androgen receptor signaling in prostate cancer by the cochaperone small glutamine rich tetratricopeptide repeat containing protein alpha. Cancer Res 2007; 67: 10087–10096
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Calderwood SK. Heat shock proteins in cancer: Diagnostic, prognostic, predictive and treatment implications. Cell Stress Chaperones 2005; 10: 86–103
   PubMed Web of Science ®Google Scholar
• Miyake H, Muramaki M, Kurahashi T, Yamanaka K, Hara I, Fijisawa M. Enhanced expression of heat shock protein 27 following neoadjuvant hormonal therapy is associated with poor clinical outcome in patients undergoing radical prostatectomy for prostate cancer. Anticancer Res 2006; 26: 1583–1587
   PubMed Web of Science ®Google Scholar
• Kurahashi T, Miyake H, Hara I, Fijisawa M. Expression of major heat shock proteins in prostate cancer: Correlation with clinicopathological outcomes in patients with radical prostatectomy. J Urol 2007; 177: 757–761
   PubMed Web of Science ®Google Scholar
• Glaessgen A, Jonmarker S, Lindberg A, Nilsson B, Lewensohn R, Ekman P, Valdman A, Egevad L. Heat shock proteins 27, 60 and 70 as prognostic markers of prostate cancer. Acta Pathol Microbiol Immunol Scand 2008; 116: 888–895
   PubMed Web of Science ®Google Scholar
• Pootrakul L, Datar RH, Shi SR, Cai J, Hawes D, Groshen SG, Lee AS, Cote RJ. Expression of stress response protein Grp78 is associated with the development of castration-resistance prostate cancer. Clin Cancer Res 2006; 12: 5987–5993
   PubMed Web of Science ®Google Scholar
• Daneshmand S, Quek ML, Lin E, Cote RJ, Hawes D, Cai J, Groshen S, Lieskovsky G, Skinner DG, Lee AS, Pinski J. Glucose-regulated protein GRP78 is up-regulated in prostate cancer and correlates with recurrence and survival. Human Pathol 2007;38:1547–1552.
   Google Scholar
• Miyake H, Muramaki M, Kurahashi T, Takenaka A, Fujisawa M. Expression of potential molecular markers in prostate cancer: correlation with clinicopathological outcomes in patients undergoing radical prostatectomy. Urol Oncol 2010;28:145–151.
   Google Scholar
• So A, Hadaschik B, Sowery R, Gleave M. The role of stress proteins in prostate cancer. Current Genomics 2007; 8: 252–261
   PubMed Web of Science ®Google Scholar
• Vargas-Roig LM, Gago FE, Tello O, Aznar JC, Ciocca DR. Heat shock protein expression and drug resistance in breast cancer patients treated with induction chemotherapy. Int J Cancer (Pred Oncol) 1998; 79: 468–475
   PubMed Web of Science ®Google Scholar
• Nadin S, Ciocca DR. Participation of heat shock proteins in DNA repair mechanisms in cancer. In: Thomas AE, editor, DNA Repair: Damage, Repair Mechanisms and Aging. New York: Nova Science Publishers; 2010, (in press).
   Google Scholar
• Lattouf JB, Srinivasan R, Pinto PA, Linehan WM, Neckers L. Mechanisms of disease: The role of heat-shock protein 90 in genitourinary malignancy. Nat Clin Pract Urol 2006; 3: 590–601
   PubMedGoogle Scholar
• Powers MV, Workman P. Targeting of multiple signaling pathways by heat shock protein 90 molecular chaperone inhibitors. Endocr Relat Cancer 2006; 13: S125–135
   PubMed Web of Science ®Google Scholar
• Kang BH, Altieri DC. Compartmentalized cancer drug discovery targeting mitochondrial Hsp90 chaperones. Oncogene 2009; 28: 3681–3688
   PubMed Web of Science ®Google Scholar
• Taplin ME. Androgen receptor: Role and novel prospects in prostate cancer. Expert Rev Anticancer Ther 2008; 8: 1495–1508
   PubMed Web of Science ®Google Scholar
• Chen Y, Sawyers CL, Scher HI. Targeting the androgen receptor pathway in prostate cancer. Curr Opin Pharmacol 2008; 8: 440–448
   PubMed Web of Science ®Google Scholar
• Banerji U. Heat shock protein 90 as a drug target: Some like it hot. Clin Cancer Res 2009; 15: 9–14
   PubMed Web of Science ®Google Scholar
• Rocchi P, Beraldi E, Ettinger S, Fazli L, Vessella RL, Nelson C, Gleave M. Increased Hsp27 after androgen ablation facilitates androgen-independent progression in prostate cancer via signal transducers and activators of transcription 3-mediated suppression of apoptosis. Cancer Res 2005; 65: 11083–11093
   PubMed Web of Science ®Google Scholar
• Kang SH, Kang KW, Kim K-H, Kwon B, Kim S-K, Lee H-Y, Kong S-Y, Lee ES, Jang S-G, Yoo BC. Upregulated HSP27 in human breast cancer cells reduces Herceptin susceptibility by increasing Her2 protein stability. Br Med Council Cancer 2008; 8: 286–296
   Google Scholar
• Ronquist KG, Carlsson L, Ronquist G, Nilsson S, Larsson A. Prostasome-derived proteins capable of eliciting an immune response in prostate cancer patients. Int J Cancer 2006; 119: 847–853
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Frayssinet P, Cuello-Carrion FD. A pilot study with a therapeutic vaccine based on hydroxyapatite ceramic particles and self-antigens in cancer patients. Cell Stress Chaperones 2007; 12: 33–43
   PubMed Web of Science ®Google Scholar
• Kottke T, Sanchez-Perez L, Diaz RM, Thompson J, Chong H, Harrington K, Calderwood SK, Pulido J, Georgopoulos N, Selby P, et al. Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer. Cancer Res 2007; 67: 11970–11979
   PubMed Web of Science ®Google Scholar
• Gao P, Sun X, Chen X, Subjeck J, Wang X-Y. Secretion of stress protein grp170 promotes immune-mediated inhibition of murine prostate tumor. Cancer Immunol Immunother 2009; 58: 1319–1328
   PubMed Web of Science ®Google Scholar
• Brusa D, Migliore E, Garetto S, Simone M, Matera L. Immunogenicity of 56°C and UVC-treated prostate cancer is associated with release of HSP70 and HMGB1 from necrotic cells. Prostate 2009; 69: 1343–1352
   PubMed Web of Science ®Google Scholar
• Srivastava PK, Callahan MK, Mauri MM. Treating human cancers with heat shock protein-peptide complexes: The road ahead. Expert Opin Biol Ther 2009; 9: 179–186
   PubMed Web of Science ®Google Scholar
• Rylander MN, Feng Y, Bass J, Diller KR. Heat shock protein expression and injury optimization for laser therapy designs. Lasers Surg Med 2007; 39: 731–746
   PubMed Web of Science ®Google Scholar
• Liu S, Yamauchi H. Etoposide induces growth arrest and disrupts androgen receptor signaling in prostate cancer cells. Oncol Rep 2010; 23: 165–170
   PubMed Web of Science ®Google Scholar