Hsp27 regulates epithelial mesenchymal transition, metastasis, and circulating tumor cells in prostate cancer

Cancer Research

Volumn 73, Issue 10, 2013, Pages 3109-3119

  Shiota, Masaki ^a   Bishop, Jennifer L ^a   Nip, Ka Mun ^a   Zardan, Anousheh ^a   Takeuchi, Ario ^a   Cordonnier, Thomas ^a   Beraldi, Eliana ^a   Bazov, Jenny ^a   Fazli, Ladan ^a   Chi, Kim ^a   Gleave, Martin ^a,b   Zoubeidi, Amina ^a,b  

^a VANCOUVER PROSTATE CENTRE   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; HEAT SHOCK PROTEIN 27; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; OGX 427; STAT3 PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER GRADING; CANCER INHIBITION; CELL TRANSPORT; CIRCULATING TUMOR CELL; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG RESPONSE; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; MALE; METASTASIS; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HSP27 HEAT-SHOCK PROTEINS; HUMANS; INTERLEUKIN-6; MALE; MICE; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; PROMOTER REGIONS, GENETIC; PROSTATIC NEOPLASMS; STAT3 TRANSCRIPTION FACTOR; TWIST TRANSCRIPTION FACTOR;

EID: 84877855030     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3979     Document Type: Article

References (43)

1. Gleave ME, Goldenberg SL, Chin JL, Warner J, Saad F, Klotz LH, et al. Randomized comparative study of 3 versus 8-month neoadjuvant hormonal therapy before radical prostatectomy: Biochemical and pathological effects. J Urol 2001;166:500-6. (Pubitemid 32652231)
2. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
3. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 2011;9:1658-67.
4. Yao Z, Fenoglio S, Gao DC, Camiolo M, Stiles B, Lindsted T, et al. TGFbeta IL-6 axis mediates selective and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc Natl Acad Sci U S A 2010;107:15535-40.
5. Sullivan NJ, Sasser AK, Axel AE, Vesuna F, Raman V, Ramirez N, et al. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells. Oncogene 2009;28:2940-7.
6. Drachenberg DE, Elgamal AA, RowbothamR, Peterson M, Murphy GP. Circulating levels of interleukin-6 in patients with hormone refractory prostate cancer. Prostate 1999;41:127-33. (Pubitemid 29446967)
7. Rocchi P, Beraldi E, Ettinger S, Fazli L, Vessella RL, Nelson C, et al. 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;65:11083-93. (Pubitemid 41713379)
8. Tenniswood MP, Guenette RS, Lakins J, Mooibroek M, Wong P, Welsh JE. Active cell death in hormone-dependent tissues. Cancer Metastasis Rev 1992;11:197-220.
9. Paul C, Manero F, Gonin S, Kretz-Remy C, Virot S, Arrigo AP. Hsp27 as a negative regulator of cytochrome C release. Mol Cell Biol 2002;22:816-34. (Pubitemid 34053061)
10. Zoubeidi A, Gleave M. Small heat shock proteins in cancer therapy and prognosis. Int J Biochem Cell Biol 2012;44:1646-56.
11. Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J 1999;13:2061-70. (Pubitemid 29517636)
12. Zoubeidi A, Zardan A, Wiedmann RM, Locke J, Beraldi E, Fazli L, et al. Hsp27 promotes insulin-like growth factor-I survival signaling in prostate cancer via p90Rsk-dependent phosphorylation and inactivation of BAD. Cancer Res 2010;70:2307-17.
13. Bausero MA, Bharti A, Page DT, Perez KD, Eng JW, Ordonez SL, et al. Silencing the hsp25 gene eliminates migration capability of the highly metastatic murine 4T1 breast adenocarcinoma cell. Tumour Biol 2006;27:17-26. (Pubitemid 41832700)
14. Mizutani H,Okano T,Minegishi Y,MatsudaK, Sudoh J,KitamuraK, et al. HSP27 modulates epithelial to mesenchymal transition of lung cancer cells in a Smad-independent manner. Oncol Lett 2010;1:1011-6.
15. Vidyasagar A, Reese S, Acun Z, Hullett D, Djamali A. HSP27 is involved in the pathogenesis of kidney tubulointerstitial fibrosis. Am J Physiol Renal Physiol 2008;295:F707-16.
16. Song H, Ethier SP, Dziubinski ML, Lin J. Stat3 modulates heat shock 27kDa protein expression in breast epithelial cells. Biochem Biophys Res Commun 2004;314:143-50. (Pubitemid 38058381)
17. Zhau HE, Odero-Marah V, Lue HW, Nomura T, Wang R, Chu G, et al. Epithelial to mesenchymal transition (EMT) in human prostate cancer: Lessons learned from ARCaP model. Clin Exp Metastasis 2008;25: 601-10.
18. Xu J, Wang R, Xie ZH, Odero-Marah V, Pathak S, Multani A, et al. Prostate cancer metastasis: Role of the host microenvironment in promoting epithelial to mesenchymal transition and increased bone and adrenal gland metastasis. Prostate 2006;66:1664-73. (Pubitemid 44646357)
19. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, et al. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 2008;283:14665-73.
20. Bruey JM, Paul C, Fromentin A, Hilpert S, Arrigo AP, Solary E, et al. Differential regulation of HSP27 oligomerization in tumor cells grown in vitro and in vivo. Oncogene 2000;19:4855-63.
21. Conroy SE, Sasieni PD, Amin V, Wang DY, Smith P, Fentiman IS, et al. Antibodies to heat-shock protein 27 are associated with improved survival in patients with breast cancer. Br J Cancer 1998;77:1875-9. (Pubitemid 28254627)
22. Foster CS, Dodson AR, Ambroisine L, Fisher G, Moller H, Clark J, et al. Hsp-27 expression at diagnosis predicts poor clinical outcome in prostate cancer independent of ETS-gene rearrangement. Br J Cancer 2009;101:1137-44.
23. Garrido C, Fromentin A, Bonnotte B, Favre N, Moutet M, Arrigo AP, et al. Heat shock protein 27 enhances the tumorigenicity of immunogenic rat colon carcinoma cell clones. Cancer Res 1998;58: 5495-9. (Pubitemid 28551136)
24. Rocchi P, So A, Kojima S, Signaevsky M, Beraldi E, Fazli L, et al. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res 2004;64:6595-602. (Pubitemid 39297919)
25. Lee JW, Kwak HJ, Lee JJ, Kim YN, Park MJ, Jung SE, et al. HSP27 regulates cell adhesion and invasion via modulation of focal adhesion kinase and MMP-2 expression. Eur J Cell Biol 2008;87:377-87.
26. Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, Tighiouart M, et al. Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 2008;68:2479-88. (Pubitemid 351521824)
27. Kostenko S, Johannessen M, Moens U. PKA-induced F-actin rearrangement requires phosphorylation of Hsp27 by the MAPKAP kinase MK5. Cell Signal 2009;21:712-8.
28. Chen P, Parks WC. Role of matrix metalloproteinases in epithelial migration. J Cell Biochem 2009;108:1233-43.
29. Adler HL, McCurdy MA, Kattan MW, Timme TL, Scardino PT, Thompson TC. Elevated levels of circulating interleukin-6 and transforming growth factor-beta1 in patients with metastatic prostatic carcinoma. J Urol 1999;161:182-7. (Pubitemid 29422316)
30. Scher HI, Jia X, de Bono JS, Fleisher M, Pienta KJ, Raghavan D, et al. Circulating tumour cells as prognostic markers in progressive, castration-resistant prostate cancer: A reanalysis of IMMC38 trial data. Lancet Oncol 2009;10:233-9.
31. Arts HJ, Hollema H, Lemstra W, Willemse PH, De Vries EG, Kampinga HH, et al. Heat-shock-protein-27 (hsp27) expression in ovarian carcinoma: Relation in response to chemotherapy and prognosis. Int J Cancer 1999;84:234-8. (Pubitemid 29256747)
32. Zhang R, Tremblay TL, McDermid A, Thibault P, Stanimirovic D. Identification of differentially expressed proteins in human glioblastoma cell lines and tumors. Glia 2003;42:194-208. (Pubitemid 36565123)
33. Bubendorf L, Kolmer M, Kononen J, Koivisto P, Mousses S, Chen Y, et al. Hormone therapy failure in human prostate cancer: Analysis by complementary DNA and tissue microarrays. J Natl Cancer Inst 1999;91:1758-64. (Pubitemid 29518772)
34. Cornford PA, Dodson AR, Parsons KF, Desmond AD, Woolfenden A, FordhamM, et al. Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res 2000;60:7099-105. (Pubitemid 32059190)
35. Wei L, Liu TT, Wang HH, Hong HM, Yu AL, Feng HP, et al. Hsp27 participates in the maintenance of breast cancer stem cells through regulation of epithelial-mesenchymal transition and nuclear factorkappaB. Breast Cancer Res 2011;13:R101.
36. Nakashima J, Tachibana M, Horiguchi Y, Oya M, Ohigashi T, Asakura H, et al. Serum interleukin 6 as a prognostic factor in patients with prostate cancer. Clin Cancer Res 2000;6:2702-6. (Pubitemid 30482107)
37. Rojas A, Liu G, Coleman I, Nelson PS, Zhang M, Dash R, et al. IL-6 promotes prostate tumorigenesis and progression through autocrine cross-activation of IGF-IR. Oncogene 2011;30:2345-55.
38. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 2007;67:9066-76. (Pubitemid 47535891)
39. Mathews LA, Hurt EM, Zhang X, Farrar WL. Epigenetic regulation of CpG promoter methylation in invasive prostate cancer cells. Mol Cancer 2010;9:267.
40. Xu L, Chen S, Bergan RC. MAPKAPK2 and HSP27 are downstream effectors of p38MAPkinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene 2006;25:2987-98. (Pubitemid 43780463)
41. Di K, Wong YC, Wang X. Id-1 promotes TGF-beta1-induced cell motility through HSP27 activation and disassembly of adherens junction in prostate epithelial cells. Exp Cell Res 2007;313:3983-99. (Pubitemid 47632543)
42. Parra E, Ferreira J, Saenz L. Inhibition of Egr-1 by siRNA in prostate carcinoma cell lines is associated with decreased expression of AP-1 and NF-kappaB. Int J Mol Med 2011;28:847-53.
43. Vetter G, Le Bechec A, Muller J, Muller A, Moes M, Yatskou M, et al. Time-resolved analysis of transcriptional events during SNAI1-triggered epithelial to mesenchymal transition. Biochem Biophys Res Commun 2009;385:485-91.