Tumor-derived inducible heat-shock protein 70 (HSP70) is an essential component of anti-tumor immunity

Oncogene

Volumn 34, Issue 10, 2015, Pages 1312-1322

  Dodd, K ^a   Nance, S ^a   Quezada, M ^a   Janke, L ^a   Morrison, J B ^a   Williams, R T ^a,b   Beere, H M ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b Puma Biotechnology Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; HEAT SHOCK PROTEIN 70;

ANIMAL; CELL LINE; CELL TRANSFORMATION; DISEASE MODEL; GENE EXPRESSION; GENE SILENCING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MOUSE; NEOPLASM; ONCOGENE; ONCOGENE MYC; PATHOLOGY; TUMOR VOLUME;

ANIMALS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; GENES, MYC; HSP70 HEAT-SHOCK PROTEINS; MICE; MICE, KNOCKOUT; NEOPLASMS; ONCOGENES; TUMOR BURDEN;

EID: 84896416745     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.63     Document Type: Article

References (39)

1. Ciocca DR, Arrigo AP, Calderwood SK. Heat shock proteins and heat shock factor 1 in carcinogenesis and tumor development: an update. Arch Toxicol 2013; 87: 19-48.
2. Min JN, Huang L, Zimonjic DB, Moskophidis D, Mivechi NF. Selective suppression of lymphomas by functional loss of Hsf1 in a p53-deficient mouse model for spontaneous tumors. Oncogene 2007; 26: 5086-5097.
3. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modi fier of carcinogenesis. Cell 2007; 130: 1005-1018.
4. Rohde M, Daugaard M, Jensen MH, Helin K, Nylandsted J, Jaattela M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev 2005; 19: 570-582.
5. Binder RJ, Srivastava PK. Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8+ T cells. Nat Immunol 2005; 6: 593-599.
6. Li Z, Menoret A, Srivastava P. Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr Opin Immnunol 2002; 14: 45-51.
7. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu Rev Immunol 2002; 20: 395-425.
8. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2002; 2: 185-194.
9. Elsner L, Muppala V, Gehrmann M, Lozano J, Malzahn D, Bickeboller H et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol 2007; 179: 5523-5533.
10. Gross C, Hansch D, Gastpar R, Multhoff G. Interaction of heat shock protein 70 peptide with NK cells involves the NK receptor CD94. Biol Chem 384: 267-279.
11. Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP et al. 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.
12. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6: 435-442.
13. Chen T, Guo J, Han C, Yang M, Cao X. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol 2009; 182: 1449-1459.
14. Mambula SS, Calderwood SK. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 2006; 177: 7849-7857.
15. Vega VL, Rodriguez-Silva M, Frey T, Gehrmann M, Diaz JC, Steinem C et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol 180: 4299-4307.
16. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994; 12: 991-1045.
17. Borges TJ, Wieten L, van Herwijnen MJ, Broere F, van der Zee R, Bonorino C et al. The anti-inflammatory mechanisms of Hsp70. Front Immunol 2012; 3: 95.
18. van Eden W, Spiering R, Broere F, van der Zee R. A case of mistaken identity: HSPs are no DAMPs but DAMPERs. Cell Stress Chaperones 2012; 17: 281-292.
19. Millar DG, Garza KM, Odermatt B, Elford AR, Ono N, Li Z et al. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat Med 2003; 9: 1469-1476.
20. Kottke T, Pulido J, Thompson J, Sanchez-Perez L, Chong H, Calderwood SK et al. Antitumor immunity can be uncoupled from autoimmunity following heat shock protein 70-mediated inflammatory killing of normal pancreas. Cancer Res 2009; 69: 7767-7774.
21. Stocki P, Dickinson AM. The immunosuppressive activity of heat shock protein 70 . Autoimmune Dis 2012; 2012: 617213.
22. Blachere NE, Li Z, Chandawarkar RY, Suto R, Jaikaria NS, Basu S et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-speci fic cytotoxic T lymphocyte response and tumor immunity. J Exp Med 1997; 186: 1315-1322.
23. Udono H, Srivastava PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med 1993; 178: 1391-1396.
24. Hunt CR, Dix DJ, Sharma GG, Pandita RK, Gupta A, Funk M et al. Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice. Mol Cell Biol 2004; 24: 899-911.
25. Williams RT, Roussel MF, Sherr CJ. Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia. Proc Natl Acad Sci USA 2006; 103: 6688-6693.
26. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S et al. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 1985; 318: 533-538.
27. Leu JI, Pimkina J, Frank A, Murphy ME, George DL. A small molecule inhibitor of inducible heat shock protein 70. Mol Cell 2009; 36: 15-27.
28. Nylandsted J, Rohde M, Brand K, Bastholm L, Elling F, Jaattela M. 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 USA 2000; 97: 7871-7876.
29. van Herwijnen MJ, Wieten L, van der Zee R, van Kooten PJ, Wagenaar-Hilbers JP, Hoek A et al. Regulatory T cells that recognize a ubiquitous stress-inducible selfantigen are long-lived suppressors of autoimmune arthritis. Proc Natl Acad Sci USA 2012; 109: 14134-14139.
30. Wachstein J, Tischer S, Figueiredo C, Limbourg A, Falk C, Immenschuh S et al. HSP70 enhances immunosuppressive function of CD4(+)CD25(+)FoxP3(+) T regulatory cells and cytotoxicity in CD4(+)CD25(-) T cells. PLoS One 2012; 7: e51747.
31. Multhoff G. Activation of natural killer cells by heat shock protein 70. Int J Hyperthermia 18: 576-585.
32. Stocki P, Wang XN, Dickinson AM. Inducible heat shock protein 70 reduces T cell responses and stimulatory capacity of monocyte-derived dendritic cells. J Biol Chem 287: 12387-12394.
33. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol. Annu Rev Immunol 2004; 22: 329-360.
34. DuPage M, Mazumdar C, Schmidt LM, Cheung AF, Jacks T. Expression of tumourspecific antigens underlies cancer immunoediting. Nature 482: 405-409.
35. Effendi K, Sakamoto M. Molecular pathology in early hepatocarcinogenesis. Oncology 2010; 78: 157-160.
36. Malusecka E, Krzyzowska-Gruca S, Gawrychowski J, Fiszer-Kierzkowska A, Kolosza Z, Krawczyk Z. Stress proteins HSP27 and HSP70i predict survival in non-small cell lung carcinoma. Anticancer Res 2008; 28: 501-506.
37. Torronteguy C, Frasson A, Zerwes F, Winnikov E, da Silva VD, Menoret A et al. Inducible heat shock protein 70 expression as a potential predictive marker of metastasis in breast tumors. Cell Stress Chaperones 2006; 11: 34-43.
38. Zietara N, Lyszkiewicz M, Gekara N, Puchalka J, Dos Santos VA, Hunt CR et al. Absence of IFN-beta impairs antigen presentation capacity of splenic dendritic cells via down-regulation of heat shock protein 70. J Immunol 2009; 183: 1099-1109.
39. Mignot G, Chalmin F, Ladoire S, Rebe C, Ghiringhelli F. Tumor exosome-mediated MDSC activation. Am J Pathol 2011; 178: 1403-1404, author reply 4-5.