The HSP70 family and cancer

Carcinogenesis

Volumn 34, Issue 6, 2013, Pages 1181-1188

  Murphy, Maureen E ^a  

^a WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ETHYL 2 [[3 ETHYL 5 (3 METHYLBENZOTHIAZOLIN 2 YLIDENE) 4 OXOTHIAZOLIDIN 2 YLIDENE]METHYL]PYRIDINIUM CHLORIDE; 15 DEOXYSPERGUALIN; ANTINEOPLASTIC AGENT; APOLATE SODIUM; DIHYDROPYRIMIDINE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; UNCLASSIFIED DRUG; VER 155008; VER 1555008;

APOPTOSIS; ARTICLE; AUTOPHAGY; B CELL LYMPHOMA; CANCER THERAPY; CELL AGING; DRUG MECHANISM; GENE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENOMIC INSTABILITY; HEAT SHOCK PROTEIN 70 GENE; HUMAN; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ANIMALS; APOPTOSIS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MICE; NEOPLASMS; PROGNOSIS; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; PROTEIN TRANSPORT; STRESS, PHYSIOLOGICAL;

EID: 84878964181     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt111     Document Type: Article

References (122)

1. Daugaard,M. et al. (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett., 581, 3702-3710.
2. Rérole,A.L. et al. (2011) Hsp70: anti-apoptotic and tumorigenic protein. Methods Mol. Biol., 787, 205-230.
3. Brodsky,J.L. et al. (2006) Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr. Top. Med. Chem., 6, 1215-1225.
4. Bonnycastle,L.L. et al. (1994) Cloning, sequencing, and mapping of the human chromosome 14 heat shock protein gene (HSPA2). Genomics, 23, 85-93.
5. Su,A.I. et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U. S. A., 101, 6062-6067.
6. Florin,L. et al. (2004) Nuclear translocation of papillomavirus minor capsid protein L2 requires Hsc70. J. Virol., 78, 5546-5553.
7. Bertelsen,E.B. et al. (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl. Acad. Sci. U. S. A., 106, 8471-8476.
8. Flaherty,K.M. et al. (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature, 346, 623-628.
9. Bork,P. et al. (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl. Acad. Sci. U. S. A., 89, 7290-7294.
10. Zhu,X. et al. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science, 272, 1606-1614.
11. Russell,R. et al. (1998) Kinetic characterization of the ATPase cycle of the DnaK molecular chaperone. Biochemistry, 37, 596-607.
12. Laufen,T. et al. (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. U. S. A., 96, 5452-5457.
13. Bukau,B. et al. (2006) Molecular chaperones and protein quality control. Cell, 125, 443-451.
14. Allan,R.K. et al. (2011) Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress Chaperones, 16, 353-367.
15. Mayer,M.P. et al. (2000) Multistep mechanism of substrate binding determines chaperone activity of Hsp70. Nat. Struct. Biol., 7, 586-593.
16. Zhuravleva,A. et al. (2012) An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell, 151, 1296-1307.
17. Zuiderweg,E.R. et al. (2013) Allostery in the Hsp70 chaperone proteins. Top. Curr. Chem., 328, 99-153.
18. Parsian,A.J. et al. (2000) The human Hsp70B gene at the HSPA7 locus of chromosome 1 is transcribed but non-functional. Biochim. Biophys. Acta, 1494, 201-205.
19. Wu,B.J. et al. (1986) Human HSP70 promoter contains at least two distinct regulatory domains. Proc. Natl. Acad. Sci. U. S. A., 83, 629-633.
20. Morgan,W.D. (1989) Transcription factor Sp1 binds to and activates a human hsp70 gene promoter. Mol. Cell. Biol., 9, 4099-4104.
21. Morgan,W.D. et al. (1987) Two transcriptional activators, CCAAT-boxbinding transcription factor and heat shock transcription factor, interact with a human hsp70 gene promoter. Mol. Cell. Biol., 7, 1129-1138.
22. Milarski,K.L. et al. (1986) Expression of human HSP70 during the synthetic phase of the cell cycle. Proc. Natl. Acad. Sci. U. S. A., 83, 9517-9521.
23. Taira,T. et al. (1997) A novel G1-specific enhancer identified in the human heat shock protein 70 gene. Nucleic Acids Res., 25, 1975-1983.
24. Akerfelt,M. et al. (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat. Rev. Mol. Cell Biol., 11, 545-555.
25. Mason,P.B. Jr et al. (1997) Cooperative and competitive protein interactions at the hsp70 promoter. J. Biol. Chem., 272, 33227-33233.
26. Cotto,J.J. et al. (1999) Stress-induced activation of the heat-shock response: cell and molecular biology of heat-shock factors. Biochem. Soc. Symp., 64, 105-118.
27. Hunt,C. et al. (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc. Natl. Acad. Sci. U. S. A., 82, 6455-6459.
28. Chou,S.D. et al. (2012) mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS One, 7, e39679.
29. Westerheide,S.D. et al. (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science, 323, 1063-1066.
30. Wu,G. et al. (2005) DeltaNp63alpha up-regulates the Hsp70 gene in human cancer. Cancer Res., 65, 758-766.
31. Hunt,C.R. et al. (2004) Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice. Mol. Cell. Biol., 24, 899-911.
32. Lee,S.H. et al. (2001) Targeted hsp70.1 disruption increases infarction volume after focal cerebral ischemia in mice. Stroke., 32, 2905-2912.
33. Van Molle,W. et al. (2002) HSP70 protects against TNF-induced lethal inflammatory shock. Immunity, 16, 685-695.
34. Shim,E.H. et al. (2002) Targeted disruption of hsp70.1 sensitizes to osmotic stress. EMBO Rep., 3, 857-861.
35. Hwang,J.H. et al. (2005) Spontaneous activation of pancreas trypsinogen in heat shock protein 70.1 knock-out mice. Pancreas, 31, 332-336.
36. Rattner,J.B. (1991) hsp70 is localized to the centrosome of dividing HeLa cells. Exp. Cell Res., 195, 110-113.
37. Oka,M. et al. (1998) Loss of Hsp70-Hsp40 chaperone activity causes abnormal nuclear distribution and aberrant microtubule formation in M-phase of Saccharomyces cerevisiae. J. Biol. Chem., 273, 29727-29737.
38. Sconzo,G. et al. (1999) Constitutive hsp70 is essential to mitosis during early cleavage of Paracentrotus lividus embryos: the blockage of constitutive hsp70 impairs mitosis. Biochem. Biophys. Res. Commun., 260, 143-149.
39. Agueli,C. et al. (2001) A constitutive 70 kDa heat-shock protein is localized on the fibres of spindles and asters at metaphase in an ATP-dependent manner: a new chaperone role is proposed. Biochem. J., 360, 413-419.
40. Jäättelä,M. (1995) Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int. J. Cancer, 60, 689-693.
41. Seo,J.S. et al. (1996) T cell lymphoma in transgenic mice expressing the human Hsp70 gene. Biochem. Biophys. Res. Commun., 218, 582-587.
42. Volloch,V.Z. et al. (1999) Oncogenic potential of Hsp72. Oncogene, 18, 3648-3651.
43. Meng,L. et al. (2011) Heat shock protein Hsp72 plays an essential role in Her2-induced mammary tumorigenesis. Oncogene, 30, 2836-2845.
44. Rohde,M. et al. (2005) Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev., 19, 570-582.
45. Ciocca,D.R. et al. (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones, 10, 86-103.
46. Calderwood,S.K. et al. (2006) Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci., 31, 164-172.
47. Chuma,M. et al. (2003) Expression profiling in multistage hepatocarcinogenesis: identification of HSP70 as a molecular marker of early hepatocellular carcinoma. Hepatology, 37, 198-207.
48. Abe,M. et al. (2004) Plasma levels of heat shock protein 70 in patients with prostate cancer: a potential biomarker for prostate cancer. Clin. Prostate Cancer, 3, 49-53.
49. Hwang,T.S. et al. (2003) Differential, stage-dependent expression of Hsp70, Hsp110 and Bcl-2 in colorectal cancer. J. Gastroenterol. Hepatol., 18, 690-700.
50. Lazaris,A.C.h. et al. (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.
51. Malusecka,E. et al. (2001) Expression of heat shock proteins HSP70 and HSP27 in primary non-small cell lung carcinomas. An immunohistochemical study. Anticancer Res., 21, 1015-1021.
52. Athanassiadou,P. et al. (1998) Expression of p53, bcl-2 and heat shock protein (hsp72) in malignant and benign ovarian tumours. Eur. J. Cancer Prev., 7, 225-231.
53. Ralhan,R. et al. (1995) Differential expression of Mr 70,000 heat shock protein in normal, premalignant, and malignant human uterine cervix. Clin. Cancer Res., 1, 1217-1222.
54. Lazaris,A.C. et al. (1995) Immunohistochemical expression of C-myc oncogene, heat shock protein 70 and HLA-DR molecules in malignant cutaneous melanoma. Virchows Arch., 426, 461-467.
55. Kaur,J. et al. (1998) Expression of 70-kDa heat shock protein in oral lesions: marker of biological stress or pathogenicity. Oral Oncol., 34, 496-501.
56. Syrigos,K.N. et al. (2003) Clinical significance of heat shock protein-70 expression in bladder cancer. Urology, 61, 677-680.
57. Ciocca,D.R. et al. (1993) Heat shock protein hsp70 in patients with axillary lymph node-negative breast cancer: prognostic implications. J. Natl. Cancer Inst., 85, 570-574.
58. Thanner,F. et al. (2003) Heat-shock protein 70 as a prognostic marker in node-negative breast cancer. Anticancer Res., 23, 1057-1062.
59. Nanbu,K. et al. (1998) Prognostic significance of heat shock proteins HSP70 and HSP90 in endometrial carcinomas. Cancer Detect. Prev., 22, 549-555.
60. Thomas,X. et al. (2005) Expression of heat-shock proteins is associated with major adverse prognostic factors in acute myeloid leukemia. Leuk. Res., 29, 1049-1058.
61. Ren,A. et al. (2008) Down-regulation of mammalian sterile 20-like kinase 1 by heat shock protein 70 mediates cisplatin resistance in prostate cancer cells. Cancer Res., 68, 2266-2274.
62. Pocaly,M. et al. (2007) Overexpression of the heat-shock protein 70 is associated to imatinib resistance in chronic myeloid leukemia. Leukemia, 21, 93-101.
63. Sliutz,G. et al. (1996) Drug resistance against gemcitabine and topotecan mediated by constitutive hsp70 overexpression in vitro: implication of quercetin as sensitiser in chemotherapy. Br. J. Cancer, 74, 172-177.
64. Jäättelä,M. et al. (1993) Heat-shock proteins protect cells from monocyte cytotoxicity: possible mechanism of self-protection. J. Exp. Med., 177, 231-236.
65. Chalmin,F. et al. (2010) Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest., 120, 457-471.
66. Nylandsted,J. et al. (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. U. S. A., 97, 7871-7876.
67. Kaur,J. et al. (2000) Induction of apoptosis by abrogation of HSP70 expression in human oral cancer cells. Int. J. Cancer, 85, 1-5.
68. Frese,S. et al. (2003) Cell death induced by down-regulation of heat shock protein 70 in lung cancer cell lines is p53-independent and does not require DNA cleavage. J. Thorac. Cardiovasc. Surg., 126, 748-754.
69. Nylandsted,J. et al. (2002) Eradication of glioblastoma, and breast and colon carcinoma xenografts by Hsp70 depletion. Cancer Res., 62, 7139-7142.
70. Powers,M.V. et al. (2008) Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell, 14, 250-262.
71. Gotoh,T. et al. (2004) hsp70-DnaJ chaperone pair prevents nitric oxideand CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ., 11, 390-402.
72. Stankiewicz,A.R. et al. (2005) Hsp70 inhibits heat-induced apoptosis upstream of mitochondria by preventing Bax translocation. J. Biol. Chem., 280, 38729-38739.
73. Saleh,A. et al. (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol., 2, 476-483.
74. Guo,F. et al. (2005) Mechanistic role of heat shock protein 70 in Bcr-Ablmediated resistance to apoptosis in human acute leukemia cells. Blood, 105, 1246-1255.
75. Gabai,V.L. et al. (2002) Hsp72 and stress kinase c-jun N-terminal kinase regulate the bid-dependent pathway in tumor necrosis factor-induced apoptosis. Mol. Cell. Biol., 22, 3415-3424.
76. Park,H.S. et al. (2002) Heat shock protein hsp72 is a negative regulator of apoptosis signal-regulating kinase 1. Mol. Cell. Biol., 22, 7721-7730.
77. Park,H.S. et al. (2001) Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J., 20, 446-456.
78. Gabai,V.L. et al. (1997) Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J. Biol. Chem., 272, 18033-18037.
79. Ravagnan,L. et al. (2001) Heat-shock protein 70 antagonizes apoptosisinducing factor. Nat. Cell Biol., 3, 839-843.
80. Yaglom,J.A. et al. (2007) High levels of heat shock protein Hsp72 in cancer cells suppress default senescence pathways. Cancer Res., 67, 2373-2381.
81. Gabai,V.L. et al. (2009) Heat shock protein Hsp72 controls oncogeneinduced senescence pathways in cancer cells. Mol. Cell. Biol., 29, 559-569.
82. Nylandsted,J. et al. (2004) Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med., 200, 425-435.
83. Daugaard,M. et al. (2007) Lens epithelium-derived growth factor is an Hsp70-2 regulated guardian of lysosomal stability in human cancer. Cancer Res., 67, 2559-2567.
84. Kirkegaard,T. et al. (2010) Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature, 463, 549-553.
85. Leu,J.I. et al. (2009) A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell, 36, 15-27.
86. Amaravadi,R.K. et al. (2007) Autophagy inhibition enhances therapyinduced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest., 117, 326-336.
87. Carew,J.S. et al. (2007) Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Ablmediated drug resistance. Blood, 110, 313-322.
88. Balaburski,G.M. et al. (2013) A modified HSP70 inhibitor shows broad activity as an anticancer agent. Mol. Cancer Res., 11, 219-229.
89. Banerji,U. et al. (2005) Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J. Clin. Oncol., 23, 4152-4161.
90. Morishima,Y. et al. (2000) Stepwise assembly of a glucocorticoid receptor. hsp90 heterocomplex resolves two sequential ATP-dependent events involving first hsp70 and then hsp90 in opening of the steroid binding pocket. J. Biol. Chem., 275, 18054-18060.
91. Massey,A.J. et al. (2010) A novel, small molecule inhibitor of Hsc70/ Hsp70 potentiates Hsp90 inhibitor induced apoptosis in HCT116 colon carcinoma cells. Cancer Chemother. Pharmacol., 66, 535-545.
92. Leu,J.I. et al. (2011) HSP70 inhibition by the small-molecule 2-phenylethynesulfonamide impairs protein clearance pathways in tumor cells. Mol. Cancer Res., 9, 936-947.
93. Braunstein,M.J. et al. (2011) Antimyeloma effects of the heat shock protein 70 molecular chaperone inhibitor MAL3-101. J. Oncol., 2011, 232037.
94. Davenport,E.L. et al. (2010) Targeting heat shock protein 72 enhances Hsp90 inhibitor-induced apoptosis in myeloma. Leukemia, 24, 1804-1807.
95. Evans,C.G. et al. (2010) Heat shock protein 70 (hsp70) as an emerging drug target. J. Med. Chem., 53, 4585-4602.
96. Powers,M.V. et al. (2010) Targeting HSP70: the second potentially druggable heat shock protein and molecular chaperone? Cell Cycle, 9, 1542-1550.
97. Patury S. et al. (2009) Pharmacological targeting of the Hsp70 chaperone. Curr. Top. Med. Chem. 9, 1337-1351
98. Goloudina,A.R. et al. (2012) Inhibition of HSP70: a challenging anticancer strategy. Cancer Lett., 325, 117-124.
99. Plowman,J. et al. (1987) Preclinical antitumor activity and pharmacological properties of deoxyspergualin. Cancer Res., 47, 685-689.
100. Dhingra,K. et al. (1994) Phase II study of deoxyspergualin in metastatic breast cancer. Invest. New Drugs, 12, 235-241.
101. Fewell,S.W. et al. (2001) Identification of an inhibitor of hsc70-mediated protein translocation and ATP hydrolysis. J. Biol. Chem., 276, 910-914.
102. Rodina,A. et al. (2007) Selective compounds define Hsp90 as a major inhibitor of apoptosis in small-cell lung cancer. Nat. Chem. Biol., 3, 498-507.
103. Koya,K. et al. (1996) MKT-077, a novel rhodacyanine dye in clinical trials, exhibits anticarcinoma activity in preclinical studies based on selective mitochondrial accumulation. Cancer Res., 56, 538-543.
104. Chiba,Y. et al. (1998) MKT-077, localized lipophilic cation: antitumor activity against human tumor xenografts serially transplanted into nude mice. Anticancer Res., 18, 1047-1052.
105. Wadhwa,R. et al. (2000) Selective toxicity of MKT-077 to cancer cells is mediated by its binding to the hsp70 family protein mot-2 and reactivation of p53 function. Cancer Res., 60, 6818-6821.
106. Rousaki,A. et al. (2011) Allosteric drugs: the interaction of antitumor compound MKT-077 with human Hsp70 chaperones. J. Mol. Biol., 411, 614-632.
107. Propper,D.J. et al. (1999) Phase I trial of the selective mitochondrial toxin MKT077 in chemo-resistant solid tumours. Ann. Oncol., 10, 923-927.
108. Koren,J. III et al. (2012) Rhodacyanine derivative selectively targets cancer cells and overcomes tamoxifen resistance. PLoS One, 7, e35566.
109. Schmitt,E. et al. (2003) Chemosensitization by a non-apoptogenic heat shock protein 70-binding apoptosis-inducing factor mutant. Cancer Res., 63, 8233-8240.
110. Schmitt,E. et al. (2006) Heat shock protein 70 neutralization exerts potent antitumor effects in animal models of colon cancer and melanoma. Cancer Res., 66, 4191-4197.
111. Rérole,A.L. et al. (2011) Peptides and aptamers targeting HSP70: a novel approach for anticancer chemotherapy. Cancer Res., 71, 484-495.
112. Williamson,D.S. et al. (2009) Novel adenosine-derived inhibitors of 70 kDa heat shock protein, discovered through structure-based design. J. Med. Chem., 52, 1510-1513.
113. Strom,E. et al. (2006) Small-molecule inhibitor of p53 binding to mitochondria protects mice from gamma radiation. Nat. Chem. Biol., 2, 474-479.
114. Steele,A.J. et al. (2009) 2-Phenylacetylenesulfonamide (PAS) induces p53-independent apoptotic killing of B-chronic lymphocytic leukemia (CLL) cells. Blood, 114, 1217-1225.
115. Kaiser,M. et al. (2011) Antileukemic activity of the HSP70 inhibitor pifithrin-μ in acute leukemia. Blood Cancer J., 1, e28.
116. French,J.B. et al. (2013) Hsp70/Hsp90 chaperone machinery is involved in the assembly of the purinosome. Proc. Natl. Acad. Sci. U. S. A., 110, 2528-2533.
117. Liu,B. et al. (2013) Cotranslational response to proteotoxic stress by elongation pausing of ribosomes. Mol. Cell, 49, 453-463.
118. Multhoff,G. et al. (1996) Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones, 1, 167-176.
119. Multhoff,G. et al. (2011) Distinguishing integral and receptor-bound heat shock protein 70 (Hsp70) on the cell surface by Hsp70-specific antibodies. Cell Stress Chaperones, 16, 251-255.
120. Pfister,K. et al. (2007) Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer, 110, 926-935.
121. Stangl,S. et al. (2011) Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc. Natl. Acad. Sci. U. S. A., 108, 733-738.
122. Miyata,Y. et al. (2012) Cysteine reactivity distinguishes redox sensing by the heat-inducible and constitutive forms of heat shock protein 70. Chem. Biol., 19, 1391-1399.