Hsp-27 expression at diagnosis predicts poor clinical outcome in prostate cancer independent of ETS-gene rearrangement

British Journal of Cancer

Volumn 101, Issue 7, 2009, Pages 1137-1144

  Foster, C S ^a   Dodson, A R ^a   Ambroisine, L ^b   Fisher, G ^b   Moller H ^c   Clark, J ^d   Attard, G ^d   De Bono, J ^d   Scardino, P ^e   Reuter, V E ^e   Cooper, C S ^d   Berney, D M ^b   Cuzick, J ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Heat shock protein 27; Prognostic biomarker; Prostate cancer

Indexed keywords

HEAT SHOCK PROTEIN 27;

AGED; APOPTOSIS; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ETS GENE; GENE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; OUTCOME ASSESSMENT; PARAMETER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION;

AGED; GENE REARRANGEMENT; HSP27 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; PROGNOSIS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-ETS;

EID: 70349659461     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605227     Document Type: Article

References (75)

1. Adams DJ, Hajj H, Edwards DP, Bjercke RJ, McGuire WL (1983) Detection of a Mr 24,000 estrogen-regulated protein in human breast cancer by monoclonal antibodies. Cancer Res 43: 4297-4301
2. Adolfsson J, Steineck G, Hedlund P-O (1997) Deferred treatment of clinically localized low-grade prostate cancer: actual 10-year and projected 15-year follow-up of the Karolinska series. Urology 50: 722-726 (Pubitemid 27494993)
3. Albertsen P, Hanley JA, Fine J (2005) 20-year outcomes following conservative management of clinically localized prostate cancer. JAMA 293: 2095-2101 (Pubitemid 40617061)
4. Albertsen PC, Fryback DG, Storer BE, Kolon TF, Fine J (1995) Long-term survival among men with conservatively treated localized prostate cancer. JAMA 274: 626-631
5. Attard G, Clark J, Ambroisine L, Fisher G, Kovacs G, Flohr P, Berney D, Foster CS, Fletcher A, Gerald WL, Moller H, Reuter V, De Bono JS, Scardino P, Cuzick J, Cooper CS (2008a) Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene 27: 253-263
6. Attard G, Clark J, Ambroisine L, Mills IG, Fisher G, Flohr P, Reid A, Edwards S, Kovacs G, Berney D, Foster CS, Massie CE, Fletcher A, De Bono JS, Scardino P, Cuzick J, Cooper CS, Transatlantic Prostate Group (2008b) Heterogeneity and clinical significance of ETV1 translocations in human prostate cancer. Br J Cancer 99: 314-320
7. Berges RR, Vucanovic J, Epstein JI, Carmichel M, Cisek L, Johnson DE, Veltri RN, Walsh PC, Isaacs JT (1995) Implication of cell kinetic changes during progression of human prostatic cancer. Clin Cancer Res 1: 473-480
8. Berney DM, Fisher G, Kattan MW, Oliver RTD, Moller H, Fearn P, Eastham J, Scardino P, Cuzick J, Reuter VE, Foster CS (2007a) Major shifts in the treatment and prognosis of prostate cancer due to changes in pathological diagnosis and grading. BJU Int 100: 1240-1244 (Pubitemid 350043922)
9. Berney DM, Fisher G, Kattan MW, Oliver RTD, Moller H, Fearn P, Eastham J, Scardino P, Cuzick J, Reuter VE, Foster CS (2007b) Pitfalls in the diagnosis of prostate cancer: retrospective review of 1791 cases with clinical outcome. Histopathology 51: 452-457 (Pubitemid 47437843)
10. Berney DM, Gopalan A, Kudahetti S, Fisher G, Ambroisine L, Foster CS, Reuter V, Eastham J, Moller H, Kattan MW, Gerald W, Cooper C, Scardino P, Cuzick J, for the Trans-Atlantic Prostate Group (2009) Ki-67 and outcome in clinically localised prostate cancer: analysis of conservatively treated prostate cancer patients from the Trans-Atlantic Prostate Group study. Br J Cancer 100(6): 888-893
11. Bill-Axelson A, Holmberg L, Ruutu M, Haggman M, Anderson SO, Bratell S, Spangberg A, Busch C, Nordling S, Garmo H, Palmgren J, Adami HO, Norlen BJ, Johansson JE, Scandinavian Prostate Cancer Group Study No.4 (2005) Radical prostatectomy versus watchful waiting in early prostate cancer. N Engl J Med 352: 1977-1984
12. Carver BS, Tran J, Chen Z, Carracedo-Perez A, Alimonti A, Nardella C, Gopalan A, Scardino PT, Cordon-Cardo C, Gerald W, Pandolfi PP (2009) ETS rearrangements and prostate cancer inhibition. Nature 457: 7231
13. Cerveira N, Ribeiro FR, Peixoto A, Costa V, Henrique R, Jeronimo C, Teixeira MR (2006) TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia 8: 826-832 (Pubitemid 44564838)
14. Charette SJ, Lambert H, Landry J (2001) A kinase-independent function of Ask1 in caspase-independent cell death. J Biol Chem 276: 36071-36074 (Pubitemid 37390811)
15. Charette SJ, Lavoie JN, Lambert H, Landry J (2000) Inhibition of Daxx-mediated apoptosis by heat shock protein 27. Mol Cell Biol 20: 7602-7612 (Pubitemid 30736884)
16. Chen HF, Xie LD, Xu CS (2009) Role of heat shock protein 27 phosphorylation in migration of vascular smooth muscle cells. Mol Cell Biochem 327(1-2): 1-6
17. Chodak GW, Kranc DM, Puy LA, Takeda H, Johnson K, Chang C (1992) Nuclear localization of androgen receptor in heterogeneous samples of normal, hyperplastic and neoplastic human prostate. J Urol 147: 798-803
18. Clark J, Attard G, Jhavar S, Flohr P, Reid A, De-Bono J, Eeles R, Scardino P, Cuzick J, Fisher G, Parker MD, Foster CS, Berney D, Kovacs G, Cooper CS (2008) Complex patterns of ETS gene alteration arise during cancer development in the human prostate. Oncogene 27: 1993-2003
19. Clark J, Merson S, Flohr P, Edwards S, Foster CS, Eeles R, Martin FL, Phillips DH, Crundwell M, Christmas T, Thompson A, Fisher C, Kovacs G, Cooper CS (2007) Diversity of TMPRSS2-ERG fusion transcripts in the human prostate. Oncogene 26: 2667-2673 (Pubitemid 46632014)
20. Cornford PA, Dodson AR, Parsons KF, Fordham M, Desmond AD, Woolfenden A, Neoptolemos JP, Foster CS (2000) Heat shock protein (HSP) expression independently predicts clinical outcome in prostate cancer. Cancer Res 60: 7099-7105 (Pubitemid 32059190)
21. Cox DR, Oakes D (1984) Analysis of Survival Data. Chapman and Hall: London, New York
22. Cuzick J, Fisher G, Kattan MW, Berney D, Oliver T, Foster CS, Moller H, Reuter V, Fearn P, Eastham J, Scardino P, Transatlantic Prostate Group (2006) Long-term outcome among men with conservatively treated localised prostate cancer. Br J Cancer 95: 1186-1194 (Pubitemid 44658482)
23. Deshmukh N, Foster CS (1997) Grading prostate cancer. In Pathology of the Prostate Foster CS, Bostwick DG (eds) Vol.34, Chapter 11, pp 191-227. WB Saunders: Philadelphia
24. Doshi BM, Hightower LE, Lee J (2009) The role of Hsp27 and actin in the regulation of movement in human cancer cells responding to heat shock. Cell Stress Chaperones 14: 445-457
25. Eastham MA, Kattan MW, Fearn P, Fisher G, Berney DM, Oliver T, Foster CS, Moller H, Reuter V, Cuzick J, Scardino P (2008) Local progression among men with conservatively treated localized prostate cancer: results from the Transatlantic Prostate Group. Eur Urol 53: 347-354
26. Foster CS (2000) Pathology of benign prostatic hyperplasia. Prostate 9: 4-14
27. Foster CS, Bostwick DG, Bonkoff H, Damber J-E, Van der Kwast T, Montironi R, Sakr W (2000) Cellular and molecular pathology of prostate cancer precursors. Scand J Urol Nephrol 34(Suppl 205): 19-43 (Pubitemid 32056463)
28. Foster CS, Dodson A, Karavana V, Smith PH, Ke Y (2002) Prostatic stem cells. J Pathol 197: 551-565
29. Foster CS, Falconer A, Dodson AR, Norman AR, Dennis A, Fletcher A, Southgate C, Dowe A, Dearnaley D, Jhavar S, Eeles R, Feber A, Cooper CS (2004) Transcription factor E2F3 overexpressed in prostate cancer independently predicts clinical outcome. Oncogene 23: 5871-5879 (Pubitemid 39093531)
30. Gibbons NB, Watson RWG, Coffey RNT, Brady HP, Fitzpatrick JM (2000) Heat-shock proteins inhibit induction of prostate cancer cell apoptosis. Prostate 45: 58-65 (Pubitemid 30679645)
31. Glaessgen A, Jonmarker S, Lindberg A, Nilsson B, Lewensohn R, Ekman P, Valdman A, Egevad L (2008) Heat shock proteins 27, 60 and 70 as prognostic markers of prostate cancer. APMIS 116: 888-895
32. Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J (1997) Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 110: 357-368 (Pubitemid 27095655)
33. Hirano S, Shelden EA, Gilmont RR (2004) HSP27 regulates fibroblast adhesion, motility and matrix contraction. Cell Stress Chaperones 9: 29-37 (Pubitemid 38429073)
34. Holmberg L, Bill-Axelson A, Helgesen F, Salo JO, Folmerz P, Haggman M, Andersson SO, Spangberg A, Busch C, Nordling S, Palmgren J, Adami HO, Johansson JE, Norlen BJ (2002) A randomized trial comparing radical prostatectomy with watchful waiting in early prostate cancer. N Engl J Med 347: 781-789 (Pubitemid 34988336)
35. http://info.cancerresearchuk.org/cancerstats/types/prostate/
36. Huot J, Lambert H, Lavoie JN, Guimond A, Houle F, Landry J (1995) Characterization of 45-kDa/54-kDa HSP27 kinase, a stress sensitive kinase which may activate the phosphorylation-dependent protective function of mammalian 27-kDa heat shock protein HSP27. Eur J Biochem 227: 416-427
37. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ (2008) Cancer statistics 2008. CA Cancer J Clin 58: 71-96
38. Johansson JE, Andren O, Andersson SO, Dickman PW, Holmberg L, Magnuson A, Adami HO (2004) Natural history of early, localized prostate cancer. JAMA 291: 2713-2719 (Pubitemid 38725420)
39. Jolly C, Morimoto RI (2000) Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst 92: 1564-1572 (Pubitemid 30770506)
40. Kostenko S, Johannessen M, Moens U (2009) PKA-induced F-actin rearrangement requires phosphorylation of Hsp27 by the MAPKAP kinase MK5. Cell Signal 21(5): 712-718
41. Landry J, Huot J (1999) Regulation of actin dynamics by stress-activated protein kinase 2 (SAPK2)-dependent phosphorylation of heat-shock protein of 27 kDa (Hsp27). Biochem Soc Symp 64: 79-89
42. Landry J, Lambert H, Zhou M, Lavoie JM, Hickey E, Weber LA, Anderson CW (1992) Human HSP27 is phosphorylated as serines 78 and serines 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J Biol Chem 267: 794-803
43. McLoughlin J, Foster CS, Price P, WIlliams G, Abel PD (1993) Evaluation of Ki-67 monoclonal antibody as prognostic indicator for prostatic carcinoma. Br J Urol 72: 92-97 (Pubitemid 23227442)
44. Miyake H, Muramaki M, Kurahashi T, Takenaka A, Fujisawa M (2008) Expression of potential molecular markers in prostate cancer: correlation with clinicopathological outcomes in patients undergoing radical prostatectomy. Urol Oncol (Epub ahead of print), doi:10.1016/j.urolonc.2008.08.001 (Pubitemid 46054000)
45. Morino M, Tsuzuki T, Ishikawa Y, Shirakami T, Yoshimura M, Kiyosuke Y, Matsunaga K, Yoshikumi C, Saijo N (1997) Specific expression of HSP27 in human tumour cell lines in vitro. In Vivo 11: 179-184 (Pubitemid 27219890)
46. Mosquera JM, Perner S, Genega EM, Sanda M, Hofer MD, Mertz KD, Paris PL, Simko J, Bismar TA, Ayala G, Shah RB, Loda M, Rubin MA (2008) Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications. Clin Cancer Res 14: 3380-3385
47. Nagy S, Ricca BL, Norstrom MF, Courson DS, Brawley CM, Smithback PA, Rock RS (2008) A myosin motor that selects bundles actin for motility. Proc Natl Acad Sci USA 105: 9616-9620 (Pubitemid 352031349)
48. O'Neill PAO, Shaaban AM, West CR, Dodson A, Jarvis C, Moore P, Davies MPA, Sibson DR, Foster CS (2003) Increased risk of malignant progression in benign proliferating breast lesions defined by expression of heat shock protein 27. Br J Cancer 90: 182-188 (Pubitemid 38174959)
49. Ono A, Kumai T, Koizumi H, Nishikawa H, Kobayashi S, Tadokoro M (2009) Overexpression of heat shock protein 27 in squamous cell carcinoma of the uterine cervix: a proteomic analysis using archival formalin-fixed, paraffin-embedded tissues. Hum Pathol 40: 41-49
50. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global science statistics. CA Cancer J Clin 55: 74-108
51. Perner S, Mosquera JM, Demichelis F, Hofer MD, Paris PL, Simko J, Collins C, Bismar TA, Chinnaiyan AM, De Marzo AM, Rubin MA (2007) TMPRSS2-ERG fusion prostate cancer: an early molecular event associated with invasion. Am J Surg Pathol 31: 882-888 (Pubitemid 47165141)
52. Pichon S, Bryckaert M, Berrou E (2004) Control of actin dynamics by p38 MAP kinase - Hsp27 distribution in the lamellipodium of smooth muscle cells. J Cell Sci 117: 2569-2577 (Pubitemid 38877852)
53. Rocchi P, Beraldi E, Ettinger S, Fazli L, Vessella RL, Nelson C, Gleave M (2005) Increased Hsp27 after androgen ablation facilities androgen-independent progression in prostate cancer via signal transducers and activators of transcription 3-mediated suppression of apoptosis. Cancer Res 65: 11083-11093 (Pubitemid 41713379)
54. Rocchi P, So A, Kojima S, Signaevsky M, Beraldi E, Fazli L, Hurtado-Coll A, Yamanaka K, Gleave M (2004) Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res 64: 6595-6602 (Pubitemid 39297919)
55. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, Hunt T, Nebreda AR (1994) A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 78: 1027-1037 (Pubitemid 24292330)
56. Samali A, Cotter TG (1996) Heat shock proteins increase resistance to apoptosis. Exp Cell Res 223: 163-170 (Pubitemid 26063934)
57. Schlapbach A, Feifel R, Hawtin S, Heng R, Koch G, Moebitz H, Revesz L, Scheufler C, Velcicky J, Waelchli R, Huppertz C (2008) Pyrrolopyrimidones: a novel class of MK2 inhibitors with potent cellular activity. Bioorg Med Chem Lett 18: 6142-6146
58. Shi P, Wang MM, Jiang LY, Liu HT, Sun JZ (2008) Paclitaxel-doxorubicin sequence is more effective in breast cancer cells with heat shock protein 27 overexpression. Chin Med J (Engl) 121: 1975-1979
59. Shin KD, Lee MY, Shin DS, Lee S, Son KH, Koh S, Paik YK, Kwon BM, Han DC (2005) Blocking tumor cell migration and invasion with biphenyl isoxazole derivative KRIBB3, a synthetic molecule that inhibits Hsp27 phorphorylation. J Biol Chem 280: 41439-41448 (Pubitemid 41832203)
60. Shin KD, Yoon YJ, Kang YR, Son KH, Kim HM, Kwon BM, Han DC (2008) KRIBB3, a novel microtubule inhibitor, induces mitotic arrest and apoptosis in human cancer cells. Biochem Pharmacol 75: 383-394 (Pubitemid 350298462)
61. Song H, Ethier SP, Dziubinski ML, Lin J (2004) Stat3 modulates heat shock 27 kDa protein expression in breast epithelial cells. Biochem Biophys Res Commun 314: 143-150 (Pubitemid 38058381)
62. Tak H, Jang E, Kim SB, Park J, Suk J, Yoon YS, Ahn JK, Lee JH, Joe CO (2007) 14-3-3epsilon inhibits MK5-mediated cell migration by disrupting F-actin polymerization. Cell Signal 19: 2379-2387 (Pubitemid 47361692)
63. Tenniswood MP, Guenette RS, Lakins J, Mooibroek M, Wong P, Welsh JE (1992) Active cell death in hormone-dependent tissues. Cancer Metastasis Rev 11: 197-220
64. Tetu B, Brisson J, Landry J, Huot J (1995) Prognostic significance of heat-shock protein-27 in node-positive breast carcinoma: an immunohistochemical study. Breast Cancer Res Treat 36: 93-97 (Pubitemid 23300594)
65. Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, Helgeson BE, Cao Q, Prensner JR, Rubin MA, Shah RB, Mehra R, Chinnaiyan AM (2008) Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 10: 177-188 (Pubitemid 351240884)
66. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun X-W, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM (2005) Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310: 644-648 (Pubitemid 41528150)
67. Tsuruta M, Nishibori H, Hasegawa H, Ishil Y, Endo T, Kubota T, Kitajima M, Kitagawa Y (2008) Heat shock protein 27, a novel regulator of 5-fluorouracil resistance in colon cancer. Oncol Rep 20: 1165-1172
68. van Diest PJ, van Dam P, Henzen-Logmans SC, Berns E, van der Burg MEL, Green J, Vergote I (1997) A scoring system for immunohistochemical staining: consensus report of the task force for basic research of the EORTC-GCCG. J Clin Pathol 50: 801-804 (Pubitemid 27475783)
69. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkinas T, Borisy GG (2006) Role of fascin in filopodial protrusion. J Cell Biol 174: 863-875
70. Wang J, Cai Y, Yu W, Ren C, Spencer DM, Ittmann M (2008) Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res 68: 8516-8524
71. Wissing D, Jaattela M (1996) HSP27 and HSP70 increase the survival of WEHI-S cells exposed to hyperthermia. Int J Hyperthermia 12: 125-138 (Pubitemid 26096971)
72. Wu R, Kausar H, Johnson P, Montoya-Durango DE, Merchant M, Rane MJ (2007) Hsp27 regulates Akt activation and polymorphonuclear leukocyte apoptosis by scaffolding MK2 to Akt signal complex. J Biol Chem 282: 21598-21608 (Pubitemid 47195774)
73. Xu L, Bergan RC (2006) Genistein inhibits matrix metalloproteinase type 2 activation and prostate cancer cell invasion by blocking the transforming growth factor beta-mediated activation of mitogen-activated protein kinase-activated protein kinase 2-27-kDa heat shock protein pathway. Mol Pharmacol 70: 869-877 (Pubitemid 44268444)
74. Yang YX, Sun XF, Cheng AL, Zhang GY, Yi H, Sun Y, Hu HD, Hu P, Ye F, Chen ZC, Xiao ZQ (2009) Increased expression of HSP27 linked to vincristine resistance in human gastric cancer cell line. J Cancer Res Clin Oncol 135: 181-189
75. Zoubeidi A, Zardan A, Beraldi E, Fazli L, Sowery R, Rennie P, Nelson C, Gleave M (2007) Cooperative interactions between androgen receptor (AR) and heat shock protein 27 facilitate AR transcriptional activity. Cancer Res 67: 10455-10465 (Pubitemid 350070821)