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

Journal of Immunology

Volumn 182, Issue 3, 2009, Pages 1449-1459

  Chen, Taoyong ^a   Guo, Jun ^a,b   Han, Chaofeng ^a   Yang, Mingjin ^a   Cao, Xuetao ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b CANCER HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; HEAT SHOCK PROTEIN 70; TOLL LIKE RECEPTOR 4; STCH PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HEAT STRESS; HYPERTHERMIA; LYMPHOCYTE FUNCTION; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR CELL; TUMOR IMMUNITY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOTOXIC T LYMPHOCYTE; GENETICS; HEAT; IMMUNOLOGY; LEWIS CARCINOMA; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECRETION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE;

ANIMALS; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; DENDRITIC CELLS; HOT TEMPERATURE; HSP70 HEAT-SHOCK PROTEINS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES, CYTOTOXIC; TOLL-LIKE RECEPTOR 4;

EID: 63149158731     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.3.1449     Document Type: Article

References (36)

1. Wallin, R. P., A. Lundqvist, S. H. More, A. von Bonin, R. Kiessling, and H. G. Ljunggren. 2002. Heat shock proteins as activators of the innate immune system. Trends Immunol. 23: 130-135.
2. Tsan, M. F., and B. Gao. 2004. Cytokine function of heat shock proteins. Am. J. Physiol. 286: C739-C744.
3. Johnson, J. D., and M. Fleshner. 2006. Releasing signals, secretory pathways, and immune function of endogenous extracellular heat shock protein 72. J. Leukocyte Biol. 79: 425-434.
4. Asea, A. 2006. Initiation of the immune response by extracellular Hsp72: chaperokine activity of Hsp72. Curr. Immunol. Rev. 2: 209-215.
5. Pockley, A. G. 2003. Heat shock proteins as regulators of the immune response. Lancet 362: 469-476.
6. Srivastava, P. 2002. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20: 395-425.
7. Baronzio, G., A. Gramaglia, and G. Fiorentini. 2006. Hyperthermia and immunity: a brief overview. In Vivo 20: 689-695.
8. Milani, V., and E. Noessner. 2006. Effects of thermal stress on tumor antigenicity and recognition by immune effector cells. Cancer Immunol. Immunother. 55: 312-319.
9. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752.
10. Chen, T., J. Guo, M. Yang, M. Zhang, W. Chen, Q. Liu, J. Wang, and X. Cao. 2004. Cyclosporin A impairs dendritic cell migration by regulating chemokine receptor expression and inhibiting cyclooxygenase-2 expression. Blood 103: 413-421.
11. Gao, B., and M. F. Tsan. 2003. Endotoxin contamination in recombinant human heat shock protein 70 (Hsp70) preparation is responsible for the induction of tumor necrosis factor α release by murine macrophages. J. Biol. Chem. 278: 174-179.
12. Wan, T., X. Zhou, G. Chen, H. An, T. Chen, W. Zhang, S. Liu, Y. Jiang, F. Yang, Y. Wu, and X. Cao. 2004. Novel heat shock protein Hsp70L1 activates dendritic cells and acts as a Th1 polarizing adjuvant. Blood 103: 1747-1754.
13. Guo, J., J. Zhu, X. Sheng, X. Wang, L. Qu, Y. Han, Y. Liu, H. Zhang, L. Huo, S. Zhang, et al. 2007. Intratumoral injection of dendritic cells in combination with local hyperthermia induces systemic antitumor effect in patients with advanced melanoma. Int. J. Cancer 120: 2418-2425.
14. Guo, J., M. Zhang, B. Wang, Z. Yuan, Z. Guo, T. Chen, Y. Yu, Z. Qin, and X. Cao. 2003. Fractalkine transgene induces T cell-dependent antitumor immunity through chemoattraction and activation of dendritic cells. Int. J. Cancer 103: 212-220.
15. Wang, Y., T. Chen, C. Han, D. He, H. Liu, H. An, Z. Cai, and X. Cao. 2007. Lysosome-associated small Rab GTPase Rab7b negatively regulates TLR4 signaling in macrophages by promoting lysosomal degradation of TLR4. Blood 110: 962-971.
16. Bouchier-Hayes, L., H. Conroy, H. Egan, C. Adrain, E. M. Creagh, M. MacFarlane, and S. J. Martin. 2001. CARDINAL, a novel caspase recruitment domain protein, is an inhibitor of multiple NF-κB activation pathways. J. Biol. Chem. 276: 44069-44077.
17. Shinobu, N., T. Iwamura, M. Yoneyama, K. Yamaguchi, W. Suhara, Y. Fukuhara, F. Amano, and T. Fujita. 2002. Involvement of TIRAP/MAL in signaling for the activation of interferon regulatory factor 3 by lipopolysaccharide. FEBS Lett. 517: 251-256.
18. Dai, S., T. Wan, B. Wang, X. Zhou, F. Xiu, T. Chen, Y. Wu, and X. Cao. 2005. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin. Cancer Res. 11: 7554-7563.
19. + CTL response by exosomes derived from IL-18 gene-modified CEA-positive tumor cells. J. Mol. Med. 84: 1067-1076.
20. b-low affinity, high affinity, and covalently-bound peptides in antitumor vaccination. Immunol. Lett. 70: 21-28.
21. El-Shami, K. M., B. Tirosh, D. Popovic, L. Carmon, E. Tzehoval, E. Vadai, M. Feldman, and L. Eisenbach. 2000. Induction of antitumor immunity by proteasome-inhibited syngeneic fibroblasts pulsed with a modified TAA peptide. Int. J. Cancer. 85: 236-242.
22. Luster, A. D. 2002. The role of chemokines in linking innate and adaptive immunity. Curr. Opin. Immunol. 14: 129-135.
23. Balkwill, F. 2003. Chemokine biology in cancer. Semin. Immunol. 15: 49-55.
24. Moser, B., M. Wolf, A. Walz, and P. Loetscher. 2004. Chemokines: multiple levels of leukocyte migration control. Trends Immunol. 25: 75-84.
25. Asea, A., S. K. Kraeft, E. A. Kurt-Jones, M. A. Stevenson, L. B. Chen, R. W. Finberg, G. C. Koo, and S. K. Calderwood. 2000. Hsp70 stimulates cytokine production through a CD-14-dependent pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6: 435-442.
26. Asea, A., M. Rehli, E. Kabingu, J. A. Boch, O. Bare, P. E. Auron, M. A. Stevenson, and S. K. Calderwood. 2002. Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277: 15028-15034.
27. Kol, A., A. H. Lichtman, R. W. Finberg, P. Libby, and E. A. Kurt-Jones. 2000. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response - CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164: 13-17.
28. Vabulas, R. M., P. Ahmad-Nejad, C. da Costa, T. Miethke, C. J. Kirschning, H. Hacker, and H. Wagner. 2001. Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276: 31332-31339.
29. Vabulas, R. M., P. Ahmad-Nejad, S. Ghose, C. J. Kirschning, R. D. Issels, and H. Wagner. 2002. Hsp70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277: 15107-15112.
30. Vabulas, R. M., S. Braedel, N. Hilf, H. Singh-Jasuja, S. Herter, P. Ahmad-Nejad, C. J. Kirschning, C. Da Costa, H. G. Rammensee, H. Wagner, and H. Schild. 2002. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J. Biol. Chem. 277: 20847-20853.
31. Dybdahl, B., A. Wahba, E. Lien, T. H. Flo, A. Waage, N. Qureshi, O. F. Sellevold, T. Espevik, and A. Sundan. 2002. Inflammatory response after open heart surgery: release of heat shock protein 70 and signaling through Tolllike receptor-4. Circulation 105: 685-690.
32. Becker, T., F. U. Hartl, and F. Wieland. 2002. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell Biol. 158: 1277-1285.
33. Binder, R. J., D. K. Han, and P. K. Srivastava. 2000. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1: 151-155.
34. Basu, S., R. J. Binder, T. Ramalingam, and P. K. Srivastava. 2001. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14: 303-313.
35. Bethke, K., F. Staib, M. Distler, U. Schmitt, H. Jonuleit, A. H. Enk, P. R. Galle, and M. Heike. 2002. Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: superiority of HSP60. J. Immunol. 169: 6141-6148.
36. Re, F., and J. L. Strominger. 2001. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem. 276: 37692-37699.