Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms

Genes and Development

Volumn 19, Issue 5, 2005, Pages 570-582

  Rohde, Mikkel ^a   Daugaard, Mads ^a   Jensen, Mette Hartvig ^a   Helin, Kristian ^b,c   Nylandsted, Jesper ^a   Jäättelä, Marja ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Heat shock proteins 70; Macrophage inhibitory cytokine 1; Microarray; Neoplasms; RNA interference; Senescence

Indexed keywords

CASPASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN E; CYTOKINE; DNA BINDING PROTEIN; GENE PRODUCT; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; HEAT SHOCK PROTEIN 70; HISTONE H2B; LONG CHAIN FATTY ACID COENZYME A LIGASE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; MACROPHAGE INHIBITORY CYTOKINE 1; MITOGEN ACTIVATED PROTEIN KINASE; N ACETYLGLUCOSAMINYLTRANSFERASE; PLECTIN; PODOCALYXIN; PROSTAGLANDIN SYNTHASE; PROTEIN P53; RIBOSOME PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; SECRETOGRANIN II; TRANSGELIN; TROPOMYOSIN; UNCLASSIFIED DRUG; ZYXIN;

ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL CYCLE; CELL SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; GENETIC TRANSFECTION; HOUSEKEEPING GENE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

CELL DIVISION; CELL SURVIVAL; CYTOKINES; G1 PHASE; G2 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HSC70 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; NEOPLASMS; RNA, SMALL INTERFERING; SPERMATOGENESIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 14644435819     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.305405     Document Type: Article

References (52)

1. Albertoni, M., Shaw, P.H., Nozaki, M., Godard, S., Tenan, M., Hamou, M.F., Fairlie, D.W., Breit, S.N., Paralkar, V.M., de Tribolet, N., et al. 2002. Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene 21: 4212-4219.
2. Baek, S.J., Kim, K.S., Nixon, J.B., Wilson, L.C., and Eling, T.E. 2001. Cyclooxygenase inhibitors regulate the expression of a TGF-β superfamily member that has proapoptotic and antitumorigenic activities. Mol. Pharmacol. 59: 901-908.
3. Bootcov, M.R., Bauskin, A.R., Valenzuela, S.M., Moore, A.G., Bansal, M., He, X.Y., Zhang, H.P., Donnellan, M., Mahler, S., Pryor, K., et al. 1997. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-β superfamily. Proc. Natl. Acad. Sci. 94: 11514-11519.
4. Bottner, M., Suter-Crazzolara, C., Schober, A., and Unsicker, K. 1999. Expression of a novel member of the TGF-β superfamily, growth/ differentiation factor-15/macrophage-inhibiting cytokine-1 (GDF-15/MIC-1) in adult rat tissues. Cell Tissue Res. 297: 103-110.
5. Buckhaults, P., Rago, C., St Croix, B., Romans, K.E., Saha, S., Zhang, L., Vogelstein, B., and Kinzler, K.W. 2001. Secreted and cell surface genes expressed in benign and malignant colorectal tumors. Cancer Res. 61: 6996-7001.
6. Bukau, B. and Horwich, A.L. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92: 351-366.
7. Buzzard, K.A., Giaccia, A.J., Killender, M., and Anderson, R.L. 1998. Heat shock protein 72 modulates pathways of stress-induced apoptosis. J. Biol. Chem. 273: 17147-17153.
8. Ciocca, D.R., Clark, G.M., Tandon, A.K., Fuqua, S.A., Welch, W.J., and McGuire, W.L. 1993. Hcat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: Prognostic implications. J. Natl. Cancer Inst. 85: 570-574.
9. Dix, D.J., Allen, J.W., Collins, B.W., Mori, C., Nakamura, N., Poorman-Allen, P., Goulding, E.H., and Eddy, E.M. 1996. Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc. Natl. Acad. Sci. 93: 3264-3268.
10. Foghsgaard, L., Wissing, D., Mauch, D., Lademann, U., Bastholm, L., Boes, M., Elling, F., Leist, M., and Jäättelä, M. 2001. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J. Cell Biol. 153: 999-1009.
11. Fourie, A.M., Peterson, P.A., and Yang, Y. 2001. Characterization and regulation of the major histocompatibility complex-encoded proteins Hsp70-Hom and Hsp70-1/2. Cell Stress Chaperones 6: 282-295.
12. Gurbuxani, S., Bruey, J.M., Fromentin, A., Larmonier, N., Parcellier, A., Jäättelä, M., Martin, F., Solary, E., and Garrido, C. 2001. Selective depletion of inducible HSP70 enhances immunogenicity of rat colon cancer cells. Oncogene 20: 7478-7485.
13. Hanahan, D. and Weinberg, R.A. 2000. The hallmarks of cancer. Cell 100: 57-70.
14. Hromas, R., Hufford, M., Sutton, J., Xu, D., Li, Y., and Lu, L. 1997. PLAB, a novel placental bone morphogenetic protein. Biochim. Biophys. Acta 1354: 40-44.
15. Hsiao, E.C., Koniaris, L.G., Zimmers-Koniaris, T., Sebald, S.M., Huynh, T.V., and Lee, S.J. 2000. Characterization of growth-differentiation factor 15, a transforming growth factor β superfamily member induced following liver injury. Mol. Cell Biol. 20: 3742-3751.
16. Huber, O. 2003. Structure and function of desmosomal proteins and their role in development and disease. Cell Mol. Life Sci. 60: 1872-1890.
17. Hunt, C. and Morimoto, R.I. 1985. Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc. Natl. Acad. Sci. 82: 6455-6459.
18. Jäättelä, M. 1995. Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Intl. J. Cancer 60: 689-693.
19. -. 1999. Heat shock proteins as cellular lifeguards. Ann. Med. 31: 261-271.
20. Jäättelä, M. and Wissing, D. 1993. Heat-shock proteins protect cells from monocyte cytotoxicity: Possible mechanism of self-protection. J. Exp. Med. 177: 231-236.
21. Jäättelä, M., Wissing, D., Bauer, P.A., and Li, G.C. 1992. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J. 11: 3507-3512.
22. Jäättelä, M., Wissing, D., Kokholm, K., Kallunki, T., and Egeblad, M. 1998. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 17: 6124-6134.
23. Kaur, J. and Ralhan, R. 2000. Induction of apoptosis by abrogation of HSP70 expression in human oral cancer cells. Intl. J. Cancer 85: 1-5.
24. Kiyono, T., Foster, S.A., Koop, J.I., McDougall, J.K., Galloway, D.A., and Klingelhutz, A.J. 1998. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396: 84-88.
25. Lawton, L.N., Bonaldo, M.F., Jelene, P.C., Qiu, L., Baumes, S.A., Marcelino, R.A., de Jesus, G.M., Wellington, S., Knowles, J.A., Warburton, D., et al. 1997. Identification of a novel member of the TGF-β superfamily highly expressed in human placenta. Gene 203: 17-26.
26. Lazaris, A., Chatzigianni, E.B., Panoussopoulos, D., Tzimas, G.N., Davaris, P.S., and Golematis, B. 1997. Proliferating cell nuclear antigen and heat shock protein 70 immunolocalization in invasive ductal breast cancer not otherwise specified. Breast Cancer Res. Treat. 43: 43-51.
27. Lee, D.H., Yang, Y., Lee, S.J., Kim, K.Y., Koo, T.H., Shin, S.M., Song, K.S., Lee, Y.H., Kim, Y.J., Lee, J.J., et al. 2003. Macrophage inhibitory cytokine-1 induces the invasiveness of gastric cancer cells by up-regulating the urokinase-type plasminogen activator system. Cancer Res. 63: 4648-4655.
28. Leung, T.K., Rajendran, M.Y., Monfries, C., Hall, C., and Lim, L. 1990. The human heat-shock protein family. Expression of a novel heat-inducible HSP70 (HSP70B') and isolation of its cDNA and genomic DNA. Biochem. J. 267: 125-132.
29. Li, P.X., Wong, J., Ayed, A., Ngo, D., Brade, A.M., Arrowsmith, C., Austin, R.C., and Klamut, H.J. 2000. Placental transforming growth factor-β is a downstream mediator of the growth arrest and apoptotic response of tumor cells to DNA damage and p53 overexpression. J. Biol. Chem. 275: 20127-20135.
30. Lindquist, S. and Craig, E.A. 1988. The heat shock proteins. Ann. Rev. Genet. 22: 631-677.
31. McKay, D.B. 1993. Structure and mechanism of 70-kDa heat-shock-related proteins. Adv. Prot. Chem. 44: 67-97.
32. Mosser, D.D., Caron, A.W., Bourget, L., Denis-Larose, C., and Massie, B. 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17: 5317-5327.
33. Nollen, E.A., Brunsting, J.F., Roelofsen, H., Weber, L.A., and Kampinga, H.H. 1999. In vivo chaperone activity of heat shock protein 70 and thermotolerance. Mol. Cell. Biol. 19: 2069-2079.
34. Nylandsted, J., Rohde, M., Brand, K., Bastholm, L., Elling, F., and Jäättelä, M. 2000. Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc. Natl. Acad. Sci. 97: 7871-7876.
35. Nylandsted, J., Wick, W., Hirt, U.A., Brand, K., Rohde, M., Leist, M., Weller, M., and Jäättelä, M. 2002. Eradication of glioblastoma, and breast and colon carcinoma xenografts by Hsp70 depletion. Cancer Res. 62: 7139-7142.
36. Nylandsted, J., Gyrd-Hansen, M., Danielewich, A., Fehrenbacher, N., Lademann, U., Hoyer-Hansen, M., Weber, E., Multhoff, G., Rohde, M., and Jäättelä, M. 2004. Hsp70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med. 200:425-435.
37. Paralkar, V.M., Vail, A.L., Grasser, W.A., Brown, T.A., Xu, H., Vukicevic, S., Ke, H.Z., Qi, H., Owen, T.A., and Thompson, D.D. 1998. Cloning and characterization of a novel member of the transforming growth factor-β/bone morphogenetic protein family. J. Biol. Chem. 273: 13760-13767.
38. Pelham, H.R.B. 1984. Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO J. 3: 3095-3100.
39. Seo, J.S., Park, Y.M., Kim, J.I., Shim, E.H., Kim, C.W., Jang, J.J., Kim, S.H., and Lee, W.H. 1996. T cell lymphoma in transgenic mice expressing the human Hsp70 gene. Biochem. Biophys. Res. Commun. 218: 582-587.
40. Simon, M.M., Krone, C., Schwarz, A., Luger, T.A., Jäättelä , M., and Schwarz, T. 1995. Heat shock protein 70 overexpression affects the response to ultraviolet light in murine fibroblasts. Evidence for increased cell viability and suppression of cytokine release. J. Clin. Invest. 95: 926-933.
41. Son, W.Y., Hwang, S.H., Han, C.T., Lee, J.H., Kim, S., and Kim, Y.C. 1999. Specific expression of heat shock protein HspA2 in human male germ cells. Mol. Hum. Reprod. 5: 1122-1126.
42. Son, W.Y., Han, C.T., Hwang, S.H., Lee, J.H., Kim, S., and Kim, Y.C. 2000. Repression of hspA2 messenger RNA in human testes with abnormal spermatogenesis. Fertil. Steril. 73: 1138-1144.
43. Tan, M., Wang, Y., Guan, K., and Sun, Y. 2000. PTGF-β, a type β transforming growth factor (TGF-β) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-β signaling pathway. Proc. Natl. Acad. Sci. 97: 109-114.
44. Tavaria, M., Gabriele, T., Kola, I., and Anderson, R.L. 1996. A hitchhiker's guide to the human Hsp70 family. Cell Stress Chaperones 1: 23-28.
45. Vargas-Roig, L.M., Fanelli, M.A., Lopez, L.A., Gago, F.E., Tello, O., Aznar, J.C., and Ciocca, D.R. 1997. Heat shock proteins and cell proliferation in human breast cancer biopsy samples. Cancer Detect. Prev. 21: 441-451.
46. Vargas-Roig, L.M., Gago, F.E., Tello, O., Aznar, J.C., and Ciocca, D.R. 1998. Heat shock protein expression and drug resistance in breast cancer patients treated with induction chemotherapy. Intl. J. Cancer 79: 468-475.
47. Vayssier, M., Banzet, N., Francois, D., Bellmann, K., and Polla, B.S. 1998. Tobacco smoke induces both apoptosis and necrosis in mammalian cells: Differential effects of HSP70. Am. J. Physiol. 275: L771-L779.
48. Volloch, V.Z. and Sherman, M.Y. 1999. Oncogenic potential of Hsp72. Oncogene 18: 3648-3651.
49. Wei, Y., Zhao, X., Kariya, Y., Teshigawara, K., and Uchida, A. 1995. Inhibition of proliferation and induction of apoptosis by abrogation of heat-shock protein (HSP) expression in tumor cells. Cancer Immunol. Immunother. 40: 73-78.
50. Wilson, L.C., Baek, S.J., Call, A., and Eling, T.E. 2003. Nonsteroidal anti-inflammatory drug-activated gene (NAG-1) is induced by genistein through the expression of p53 in colorectal cancer cells. Intl. J. Cancer 105: 747-753.
51. Xanthoudakis, S. and Nicholson, D.W. 2000. Heat-shock proteins as death determinants. Nat. Cell Biol. 2: E163-E165.
52. Zhu, D., Dix, D.J., and Eddy, E.M. 1997. HSP70-2 is required for CDC2 kinase activity in meiosis 1 of mouse spermatocytes. Development 124: 3007-3014.