Heat shock protein 27 as a prognostic and predictive biomarker in pancreatic ductal adenocarcinoma

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 8, 2012, Pages 1776-1791

  Schäfer, Claus ^a   Seeliger, Hendrik ^b   Bader, Dominik C ^c   Assmann, Gerald ^c   Buchner, Denise ^c   Guo, Yang ^c   Ziesch, Andreas ^c   Palagyi, Andreas ^c   Ochs, Stephanie ^c   Laubender, Rüdiger P ^c   Jung, Andreas ^c   De Toni, Enrico N ^c   Kirchner, Thomas ^c   Göke, Burkhard ^c   Bruns, Christiane ^b   Gallmeier, Eike ^c  

^a Klinikum Neumarkt   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Biomarker; Gemcitabine; HSP27; Pancreatic cancer; TMA

Indexed keywords

DEOXYCYTIDINE; DRUG DERIVATIVE; GEMCITABINE; HEAT SHOCK PROTEIN 27; HSPB1 PROTEIN, HUMAN; TUMOR MARKER;

ADENOCARCINOMA; ADULT; AGED; ARTICLE; DRUG EFFECT; DRUG SCREENING; FEMALE; HEAT SHOCK RESPONSE; HUMAN; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; MALE; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; PANCREAS; PANCREAS CARCINOMA; PATHOLOGY; PROGNOSIS; TISSUE MICROARRAY; TUMOR CELL LINE;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DEOXYCYTIDINE; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; HEAT-SHOCK RESPONSE; HSP27 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; PANCREAS; PROGNOSIS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84864389664     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01473.x     Document Type: Article

References (84)

1. Jemal A, Siegel R, Ward E, et al Cancer statistics, 2008. CA Cancer J Clin. 2008; 58: 71-96.
2. Li D, Xie K, Wolff R, et al Pancreatic cancer. Lancet. 2004; 363: 1049-57.
3. Garcea G, Dennison AR, Pattenden CJ, et al Survival following curative resection for pancreatic ductal adenocarcinoma. A systematic review of the literature. JOP. 2008; 9: 99-132.
4. Camp RL, Neumeister V, Rimm DL. A decade of tissue microarrays: progress in the discovery and validation of cancer biomarkers. J Clin Oncol. 2008; 26: 5630-7.
5. Lindquist S, Craig EA. The heat-shock proteins. Annu Rev Genet. 1988; 22: 631-77.
6. Georgopoulos C, Welch WJ. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol. 1993; 9: 601-34.
7. Arrigo AP, Simon S, Gibert B, et al Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett. 2007; 581: 3665-74.
8. Garrido C, Brunet M, Didelot C, et al Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle. 2006; 5: 2592-601.
9. Theriault JR, Lambert H, Chavez-Zobel AT, et al Essential role of the NH2-terminal WD/EPF motif in the phosphorylation-activated protective function of mammalian Hsp27. J Biol Chem. 2004; 279: 23463-71.
10. Kostenko S, Moens U. Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci. 2009; 66: 3289-307.
11. Ciocca DR, Adams DJ, Edwards DP, et al Distribution of an estrogen-induced protein with a molecular weight of 24, 000 in normal and malignant human tissues and cells. Cancer Res. 1983; 43: 1204-10.
12. Soldes OS, Kuick RD, Thompson IA 2nd, et al Differential expression of Hsp27 in normal oesophagus, Barrett's metaplasia and oesophageal adenocarcinomas. Br J Cancer. 1999; 79: 595-603.
13. Ciocca DR, Calderwood SK. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones. 2005; 10: 86-103.
14. Schafer C, Williams JA. Stress kinases and heat shock proteins in the pancreas: possible roles in normal function and disease. J Gastroenterol. 2000; 35: 1-9.
15. Rakonczay Z Jr, Takacs T, Boros I, et al Heat shock proteins and the pancreas. J Cell Physiol. 2003; 195: 383-91.
16. Kubisch C, Dimagno MJ, Tietz AB, et al Overexpression of heat shock protein Hsp27 protects against cerulein-induced pancreatitis. Gastroenterology. 2004; 127: 275-86.
17. Lu Z, Hu L, Evers S, et al Differential expression profiling of human pancreatic adenocarcinoma and healthy pancreatic tissue. Proteomics. 2004; 4: 3975-88.
18. Melle C, Ernst G, Escher N, et al Protein profiling of microdissected pancreas carcinoma and identification of HSP27 as a potential serum marker. Clin Chem. 2007; 53: 629-35.
19. Liao WC, Wu MS, Wang HP, et al Serum heat shock protein 27 is increased in chronic pancreatitis and pancreatic carcinoma. Pancreas. 2009; 38: 422-6.
20. Mori-Iwamoto S, Kuramitsu Y, Ryozawa S, et al Proteomics finding heat shock protein 27 as a biomarker for resistance of pancreatic cancer cells to gemcitabine. Int J Oncol. 2007; 31: 1345-50.
21. Mori-Iwamoto S, Taba K, Kuramitsu Y, et al Interferon-gamma down-regulates heat shock protein 27 of pancreatic cancer cells and helps in the cytotoxic effect of gemcitabine. Pancreas. 2009; 38: 224-6.
22. Taba K, Kuramitsu Y, Ryozawa S, et al Heat-shock protein 27 is phosphorylated in gemcitabine-resistant pancreatic cancer cells. Anticancer Res. 2010; 30: 2539-43.
23. Kononen J, Bubendorf L, Kallioniemi A, et al Tissue microarrays for high-throughput molecular profiling of tumour specimens. Nat Med. 1998; 4: 844-7.
24. Neumann J, Zeindl-Eberhart E, Kirchner T, et al Frequency and type of KRAS mutations in routine diagnostic analysis of metastatic colorectal cancer. Pathol Res Pract. 2009; 205: 858-62.
25. Ogino S, Kawasaki T, Brahmandam M, et al Sensitive sequencing method for KRAS mutation detection by Pyrosequencing. J Mol Diagn. 2005; 7: 413-21.
26. Parmar M, Machin D. Survival analysis - a practical approach. New York : Wiley & Sons; 1996.
27. Schafer C, Clapp P, Welsh MJ, et al HSP27 expression regulates CCK-induced changes of the actin cytoskeleton in CHO-CCK-A cells. Am J Physiol. 1999; 277: C1032-43.
28. Mehlen P, Hickey E, Weber LA, et al Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFalpha in NIH-3T3-ras cells. Biochem Biophys Res Commun. 1997; 241: 187-92.
29. Katz MH, Hwang R, Fleming JB, et al Tumour-node-metastasis staging of pancreatic adenocarcinoma. CA Cancer J Clin. 2008; 58: 111-25.
30. Rozenblum E, Schutte M, Goggins M, et al Tumour-suppressive pathways in pancreatic carcinoma. Cancer Res. 1997; 57: 1731-4.
31. Redston MS, Caldas C, Seymour AB, et al p53 mutations in pancreatic carcinoma and evidence of common involvement of homocopolymer tracts in DNA microdeletions. Cancer Res. 1994; 54: 3025-33.
32. Almoguera C, Shibata D, Forrester K, et al Most human carcinomas of the exocrine pancreas contain mutant c-K-ras genes. Cell. 1988; 53: 549-54.
33. Maitra A, Adsay NV, Argani P, et al Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol. 2003; 16: 902-12.
34. Gao C, Zou Z, Xu L, et al p53-dependent induction of heat shock protein 27 (HSP27) expression. Int J Cancer. 2000; 88: 191-4.
35. Evans JR, Bosman JD, Brown-Endres L, et al Induction of the small heat shock protein alphaB-crystallin by genotoxic stress is mediated by p53 and p73. Breast Cancer Res Treat. 2010; 122: 159-68.
36. Kanagasabai R, Krishnamurthy K, Druhan LJ, et al Forced expression of Hsp27 reverses P-glycoprotein (ABCB1) mediated drug efflux and MDR1 gene expression in adriamycin resistant human breast cancer cells. J Biol Chem. 2011.
37. O'Callaghan-Sunol C, Gabai VL, Sherman MY. Hsp27 modulates p53 signaling and suppresses cellular senescence. Cancer Res. 2007; 67: 11779-88.
38. Garcea G, Neal CP, Pattenden CJ, et al Molecular prognostic markers in pancreatic cancer: a systematic review. Eur J Cancer. 2005; 41: 2213-36.
39. Uozaki H, Ishida T, Kakiuchi C, et al Expression of heat shock proteins in osteosarcoma and its relationship to prognosis. Pathol Res Pract. 2000; 196: 665-73.
40. King KL, Li AF, Chau GY, et al Prognostic significance of heat shock protein-27 expression in hepatocellular carcinoma and its relation to histologic grading and survival. Cancer. 2000; 88: 2464-70.
41. Cornford PA, Dodson AR, Parsons KF, et al Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res. 2000; 60: 7099-105.
42. Foster CS, Dodson AR, Ambroisine L, 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.
43. Geisler JP, Geisler HE, Tammela J, et al A study of heat shock protein 27 in endometrial carcinoma. Gynecol Oncol. 1999; 72: 347-50.
44. Kawanishi K, Shiozaki H, Doki Y, et al Prognostic significance of heat shock proteins 27 and 70 in patients with squamous cell carcinoma of the esophagus. Cancer. 1999; 85: 1649-57.
45. Tetu B, Lacasse B, Bouchard HL, et al Prognostic influence of HSP-27 expression in malignant fibrous histiocytoma: a clinicopathological and immunohistochemical study. Cancer Res. 1992; 52: 2325-8.
46. Gandour-Edwards R, Trock BJ, Gumerlock P, et al Heat shock protein and p53 expression in head and neck squamous cell carcinoma. Otolaryngol Head Neck Surg. 1998; 118: 610-5.
47. Storm FK, Mahvi DM, Gilchrist KW. Hsp-27 has no diagnostic or prognostic significance in prostate or bladder cancers. Urology. 1993; 42: 379-82.
48. Erkizan O, Kirkali G, Yorukoglu K, et al Significance of heat shock protein-27 expression in patients with renal cell carcinoma. Urology. 2004; 64: 474-8.
49. Ito T, Kawabe R, Kurasono Y, et al Expression of heat shock proteins in squamous cell carcinoma of the tongue: an immunohistochemical study. J Oral Pathol Med. 1998; 27: 18-22.
50. Mese H, Sasaki A, Nakayama S, et al Prognostic significance of heat shock protein 27 (HSP27) in patients with oral squamous cell carcinoma. Oncol Rep. 2002; 9: 341-4.
51. Wang A, Liu X, Sheng S, et al Dysregulation of heat shock protein 27 expression in oral tongue squamous cell carcinoma. BMC Cancer. 2009; 9: 167.
52. Lo Muzio L, Campisi G, Farina A, et al Prognostic value of HSP27 in head and neck squamous cell carcinoma: a retrospective analysis of 57 tumours. Anticancer Res. 2006; 26: 1343-9.
53. Kapranos N, Kominea A, Konstantinopoulos PA, et al Expression of the 27-kDa heat shock protein (HSP27) in gastric carcinomas and adjacent normal, metaplastic, and dysplastic gastric mucosa, and its prognostic significance. J Cancer Res Clin Oncol. 2002; 128: 426-32.
54. Takeno S, Noguchi T, Kikuchi R, et al Analysis of the survival period in resectable stage IV gastric cancer. Ann Surg Oncol. 2001; 8: 215-21.
55. Giaginis C, Daskalopoulou SS, Vgenopoulou S, et al Heat Shock Protein-27, -60 and -90 expression in gastric cancer: association with clinicopathological variables and patient survival. BMC Gastroenterol. 2009; 9: 14.
56. Langdon SP, Rabiasz GJ, Hirst GL, et al Expression of the heat shock protein HSP27 in human ovarian cancer. Clin Cancer Res. 1995; 1: 1603-9.
57. Geisler JP, Geisler HE, Tammela J, et al Heat shock protein 27: an independent prognostic indicator of survival in patients with epithelial ovarian carcinoma. Gynecol Oncol. 1998; 69: 14-6.
58. Schneider J, Jimenez E, Marenbach K, et al Co-expression of the MDR1 gene and HSP27 in human ovarian cancer. Anticancer Res. 1998; 18: 2967-71.
59. Arts HJ, Hollema H, Lemstra W, 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.
60. Elpek GO, Karaveli S, Simsek T, et al Expression of heat-shock proteins hsp27, hsp70 and hsp90 in malignant epithelial tumour of the ovaries. APMIS. 2003; 111: 523-30.
61. Elstrand MB, Kleinberg L, Kohn EC, et al Expression and clinical role of antiapoptotic proteins of the bag, heat shock, and Bcl-2 families in effusions, primary tumours, and solid metastases in ovarian carcinoma. Int J Gynecol Pathol. 2009; 28: 211-21.
62. Kassem H, Sangar V, Cowan R, et al A potential role of heat shock proteins and nicotinamide N-methyl transferase in predicting response to radiation in bladder cancer. Int J Cancer. 2002; 101: 454-60.
63. Seymour L, Bezwoda WR, Meyer K, et al Detection of P24 protein in human breast cancer: influence of receptor status and oestrogen exposure. Br J Cancer. 1990; 61: 886-90.
64. Vargas-Roig LM, Gago FE, Tello O, et al Heat shock protein expression and drug resistance in breast cancer patients treated with induction chemotherapy. Int J Cancer. 1998; 79: 468-75.
65. Takeno S, Noguchi T, Takahashi Y, et al Immunohistochemical and clinicopathologic analysis of response to neoadjuvant therapy for esophageal squamous cell carcinoma. Dis Esophagus. 2001; 14: 149-54.
66. Langer R, Ott K, Specht K, et al Protein expression profiling in esophageal adenocarcinoma patients indicates association of heat-shock protein 27 expression and chemotherapy response. Clin Cancer Res. 2008; 14: 8279-87.
67. Bubendorf L, Kolmer M, Kononen J, et al Hormone therapy failure in human prostate cancer: analysis by complementary DNA and tissue microarrays. J Natl Cancer Inst. 1999; 91: 1758-64.
68. Damstrup L, Andersen J, Kufe DW, et al Immunocytochemical determination of the estrogen-regulated proteins Mr 24, 000, Mr 52, 000 and DF3 breast cancer associated antigen: clinical value in advanced breast cancer and correlation with estrogen receptor. Ann Oncol. 1992; 3: 71-7.
69. Ciocca DR, Green S, Elledge RM, et al Heat shock proteins hsp27 and hsp70: lack of correlation with response to tamoxifen and clinical course of disease in estrogen receptor-positive metastatic breast cancer (a Southwest Oncology Group Study). Clin Cancer Res. 1998; 4: 1263-6.
70. Germain I, Tetu B, Brisson J, et al Markers of chemoresistance in ovarian carcinomas: an immunohistochemical study of 86 cases. Int J Gynecol Pathol. 1996; 15: 54-62.
71. Vargas Roig LM, Lotfi H, Olcese JE, et al Effects of short-term tamoxifen administration in patients with invasive cervical carcinoma. Anticancer Res. 1993; 13: 2457-63.
72. Fortin A, Raybaud-Diogene H, Tetu B, et al Overexpression of the 27 KDa heat shock protein is associated with thermoresistance and chemoresistance but not with radioresistance. Int J Radiat Oncol Biol Phys. 2000; 46: 1259-66.
73. Rau B, Gaestel M, Wust P, et al Preoperative treatment of rectal cancer with radiation, chemotherapy and hyperthermia: analysis of treatment efficacy and heat-shock response. Radiat Res. 1999; 151: 479-88.
74. Adachi S, Kokura S, Okayama T, et al Effect of hyperthermia combined with gemcitabine on apoptotic cell death in cultured human pancreatic cancer cell lines. Int J Hyperthermia. 2009; 25: 210-9.
75. Ohguri T, Imada H, Yahara K, et al Concurrent chemoradiotherapy with gemcitabine plus regional hyperthermia for locally advanced pancreatic carcinoma: initial experience. Radiat Med. 2008; 26: 587-96.
76. Tschoep KE, Boeck S, Berger F, et al Regional hyperthermia (RHT) combined with gemcitabine (GEM) + cisplatin (CIS) in patients with GEM-refractory advanced pancreatic cancer: results of the ESHO phase II trial. J Clin Oncol (Meeting Abstracts). 2008; 26: 4635.
77. Calderwood SK, Khaleque MA, Sawyer DB, et al Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci. 2006; 31: 164-72.
78. Stammler G, Volm M. Expression of heat shock proteins, glutathione peroxidase and catalase in childhood acute lymphoblastic leukemia and nephroblastoma. Cancer Lett. 1996; 99: 35-42.
79. Aghdassi A, Phillips P, Dudeja V, et al Heat shock protein 70 increases tumorigenicity and inhibits apoptosis in pancreatic adenocarcinoma. Cancer Res. 2007; 67: 616-25.
80. Gress TM, Muller-Pillasch F, Weber C, et al Differential expression of heat shock proteins in pancreatic carcinoma. Cancer Res. 1994; 54: 547-51.
81. Sagol O, Tuna B, Coker A, et al Immunohistochemical detection of pS2 protein and heat shock protein-70 in pancreatic adenocarcinomas. Relationship with disease extent and patient survival. Pathol Res Pract. 2002; 198: 77-84.
82. Saluja A, Dudeja V. Heat shock proteins in pancreatic diseases. J Gastroenterol Hepatol. 2008; 23 Suppl 1: S42-5.
83. Phillips PA, Dudeja V, McCarroll JA, et al Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res. 2007; 67: 9407-16.
84. Dudeja V, Mujumdar N, Phillips P, et al Heat shock protein 70 inhibits apoptosis in cancer cells through simultaneous and independent mechanisms. Gastroenterology. 2009; 136: 1772-82.