Phosphorylation status of heat shock protein 27 plays a key role in gemcitabine-induced apoptosis of pancreatic cancer cells

Cancer Letters

Volumn 313, Issue 2, 2011, Pages 218-225

  Nakashima, Masanori ^a   Adachi, Seiji ^a   Yasuda, Ichiro ^a   Yamauchi, Takahiro ^a   Kawaguchi, Junji ^a   Itani, Masahiko ^a   Yoshioka, Takashi ^a   Matsushima Nishiwaki, Rie ^a   Hirose, Yoshinobu ^b   Kozawa, Osamu ^a   Moriwaki, Hisataka ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b GIFU UNIVERSITY HOSPITAL   (Japan)

Author keywords

Apoptosis; Gemcitabine; HSP27; Pancreatic cancer; Phosphorylation

Indexed keywords

GEMCITABINE; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG SENSITIVITY; ENZYME ACTIVATION; GENETIC TRANSFECTION; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; ENZYME INHIBITORS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PANCREATIC NEOPLASMS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN-SERINE-THREONINE KINASES; SERINE;

EID: 82655187445     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.09.008     Document Type: Article

References (35)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics, 2009. CA Cancer J. Clin. 2009, 59:225-249.
2. Cress R.D., Yin D., Clarke L., Bold R., Holly E.A. Survival among patients with adenocarcinoma of the pancreas: a population-based study (United States). Cancer Causes Control 2006, 17:403-409.
3. Burris H.A., Moore M.J., Andersen J., Green M.R., Rothenberg M.L., Modiano M.R., Cripps M.C., Portenoy R.K., Storniolo A.M., Tarassoff P., Nelson R., Dorr F.A., Stephens C.D., Von Hoff D.D. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 1997, 15:2403-2413.
4. Stathis A., Moore M.J. Advanced pancreatic carcinoma: current treatment and future challenges. Nat. Rev. Clin. Oncol. 2010, 7:163-172.
5. Plunkett W., Huang P., Searcy C.E., Gandhi V. Gemcitabine: preclinical pharmacology and mechanisms of action. Semin. Oncol. 1996, 23:3-15.
6. Habiro A., Tanno S., Koizumi K., Izawa T., Nakano Y., Osanai M., Mizukami Y., Okumura T., Kohgo Y. Involvement of p38 mitogen-activated protein kinase in gemcitabine-induced apoptosis in human pancreatic cancer cells. Biochem. Biophys. Res. Commun. 2004, 316:71-77.
7. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
8. Freeman B.C., Yamamoto K.R. Disassembly of transcriptional regulatory complexes by molecular chaperones. Science 2002, 296:2232-2235.
9. Garrido C., Brunet M., Didelot C., Zermati Y., Schmitt E., Kroemer G. Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 2006, 5:2592-2601.
10. Benjamin I.J., McMillan D.R. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ. Res. 1998, 83:117-132.
11. Lambert H., Charette S.J., Bernier A.F., Guimond A., Landry J. HSP27 multimerization mediated by phosphorylation-sensitive intermolecular interactions at the amino terminus. J. Biol. Chem. 1999, 274:9378-9385.
12. Landry J., Lambert H., Zhou M., Lavoie J.N., Hickey E., Weber L.A., Anderson C.W. Human HSP27 is phosphorylated at serines 78 and 82 by heat shock and mitogen-activated kinases that recognize the same amino acid motif as S6 kinase II. J. Biol. Chem. 1992, 267:794-803.
13. Rouse J., Cohen P., Trigon S., Morange M., Alonso-Llamazares A., Zamanillo D., Hunt T., Nebreda A.R. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 1994, 78:1027-1037.
14. Langdon S.P., Rabiasz G.J., Hirst G.L., King R.J., Hawkins R.A., Smyth J.F., Miller W.R. Expression of the heat shock protein HSP27 in human ovarian cancer. Clin. Cancer Res. 1995, 1:1603-1609.
15. Fortin A., Raybaud-Diogene H., Tetu B., Deschenes R., Huot J., Landry J. 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, 46:1259-1266.
16. Piura B., Rabinovich A., Yavelsky V., Wolfson M. Heat shock proteins and malignancies of the female genital tract. Harefuah 2002, 141:969-972. 1010, 1009.
17. Nakajima M., Kuwano H., Miyazaki T., Masuda N., Kato H. Significant correlation between expression of heat shock proteins 27, 70 and lymphocyte infiltration in esophageal squamous cell carcinoma. Cancer Lett. 2002, 178:99-106.
18. Mori-Iwamoto S., Kuramitsu Y., Ryozawa S., Mikuria K., Fujimoto M., Maehara S., Maehara Y., Okita K., Nakamura K., Sakaida I. Proteomics finding heat shock protein 27 as a biomarker for resistance of pancreatic cancer cells to gemcitabine. Int. J. Oncol. 2007, 31:1345-1350.
19. Taba K., Kuramitsu Y., Ryozawa S., Yoshida K., Tanaka T., Maehara S., Maehara Y., Sakaida I., Nakamura K. Heat-shock protein 27 is phosphorylated in gemcitabine-resistant pancreatic cancer cells. Anticancer Res. 2010, 30:2539-2543.
20. Matsushima-Nishiwaki R., Takai S., Adachi S., Minamitani C., Yasuda E., Noda T., Kato K., Toyoda H., Kaneoka Y., Yamaguchi A., Kumada T., Kozawa O. Phosphorylated heat shock protein 27 represses growth of hepatocellular carcinoma via inhibition of extracellular signal-regulated kinase. J. Biol. Chem. 2008, 283:18852-18860.
21. Adachi S., Nagao T., Ingolfsson H.I., Maxfield F.R., Andersen O.S., Kopelovich L., Weinstein I.B. The inhibitory effect of (-)-epigallocatechin gallate on activation of the epidermal growth factor receptor is associated with altered lipid order in HT29 colon cancer cells. Cancer Res. 2007, 67:6493-6501.
22. Oliver F.J., de la Rubia G., Rolli V., Ruiz-Ruiz M.C., de Murcia G., Murcia J.M. Importance of poly (ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J. Biol. Chem. 1998, 273:33533-33539.
23. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M.A., Lassota P., Traganos F. Features of apoptotic cells measured by flow cytometry. Cytometry 1992, 13:795-808.
24. Kato K., Ito H., Iwamoto I., Lida K., Inaguma Y. Protein kinase inhibitors can suppress stress-induced dissociation of Hsp27. Cell Stress Chaperon. 2001, 6:16-20.
25. Cuenda A., Rouse J., Doza Y.N., Meier R., Cohen P., Gallagher T.F., Young P.R., Lee J.C. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 1995, 364:229-233.
26. Bain J., Plater L., Elliott M., Shpiro N., Hastie C.J., McLauchlan H., Klevernic I., Arthur J.S., Alessi D.R., Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 2007, 408:297-315.
27. Melle C., Ernst G., Escher N., Hartmann D., Schimmel B., Bleul A., Thieme H., Kaufmann R., Felix K., Friess H.M., Settmacher U., Hommann M., Richter K.K., Daffner W., Taubig H., Manger T., Claussen U., von Eggeling F. Protein profiling of microdissected pancreas carcinoma and identification of HSP27 as a potential serum marker. Clin. Chem. 2007, 53:629-635.
28. Adachi S., Shimizu M., Shirakami Y., Yamauchi J., Natsume H., Matsushima-Nishiwaki R., To S., Weinstein I.B., Moriwaki H., Kozawa O. (-)-Epigallocatechin gallate downregulates EGF receptor via phosphorylation at Ser1046/1047 by p38 MAPK in colon cancer cells. Carcinogenesis 2009, 30:1544-1552.
29. Adachi S., Natsume H., Yamauchi J., Matsushima-Nishiwaki R., Joe A.K., Moriwaki H., Kozawa O. P38 MAP kinase controls EGF receptor downregulation via phosphorylation at Ser1046/1047. Cancer Lett. 2009, 277:108-113.
30. Adachi S., Yasuda I., Nakashima M., Yamauchi T., Yamauchi J., Natsume H., Moriwaki H., Kozawa O. HSP90 inhibitors induce desensitization of EGF receptor via p38 MAPK-mediated phosphorylation at Ser1046/1047 in human pancreatic cancer cells. Oncol. Rep. 2010, 23:1709-1714.
31. Winograd-Katz S.E., Levitzki A. Cisplatin induces PKB/Akt activation and p38(MAPK) phosphorylation of the EGF receptor. Oncogene 2006, 25:7381-7390.
32. Koizumi K., Tanno S., Nakano Y., Habiro A., Izawa T., Mizukami Y., Okumura T., Kohgo Y. Activation of p38 mitogen-activated protein kinase is necessary for gemcitabine-induced cytotoxicity in human pancreatic cancer cells. Anticancer Res. 2005, 25:3347-3353.
33. Feng F.Y., Varambally S., Tomlins S.A., Chun P.Y., Lopez C.A., Li X., Davis M.A., Chinnaiyan A.M., Lawrence T.S., Nyati M.K. Role of epidermal growth factor receptor degradation in gemcitabine-mediated cytotoxicity. Oncogene 2007, 26:3431-3439.
34. Concannon C.G., Gorman A.M., Samali A. On the role of Hsp27 in regulating apoptosis. Apoptosis 2003, 8:61-70.
35. Yasuda E., Kumada T., Takai S., Ishisaki A., Noda T., Matsushima-Nishiwaki R., Yoshimi N., Kato K., Toyoda H., Kaneoka Y., Yamaguchi A., Kozawa O. Attenuated phosphorylation of heat shock protein 27 correlates with tumor progression in patients with hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 2005, 337:337-3342.