Inducible heat shock protein 70 reduces T cell responses and stimulatory capacity of monocyte-derived dendritic cells

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 12387-12394

  Stocki, Pawel ^a   Wang, Xiao N ^a   Dickinson, Anne M ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL CONDITIONS; DENDRITIC CELLS; HEAT SHOCK PROTEIN 70; INFLAMMATORY REACTION; PROINFLAMMATORY; T CELLS; T-CELL RESPONSE; UP-REGULATION;

BODY FLUIDS; CYTOLOGY; RECOMBINANT PROTEINS;

CELLS;

ENDOTOXIN; HEAT SHOCK PROTEIN 70; INTERLEUKIN 2; PHYTOHEMAGGLUTININ;

ARTICLE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; INCUBATION TIME; LYMPHOCYTE PROLIFERATION; MONOCYTE; MONOCYTE DERIVED DENDRITIC CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ADJUVANTS, IMMUNOLOGIC; CELL DIFFERENTIATION; CELL SHAPE; CELLS, CULTURED; DENDRITIC CELLS; ENDOTOXINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; PHYTOHEMAGGLUTININS; T-LYMPHOCYTES;

EID: 84859489665     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.307579     Document Type: Article

References (33)

1. Udono, H., and Srivastava, P. K. (1993) Heat shock protein 70-associated peptides elicit specific cancer immunity. J. Exp. Med. 178, 1391-1396 (Pubitemid 23277370)
2. Li, Z., and Srivastava, P. K. (1993) Tumor rejection antigen gp96/grp94 is an ATPase: implications for protein folding and antigen presentation. EMBO J. 12, 3143-3151 (Pubitemid 23232745)
3. Stocki, P., Morris, N. J., Preisinger, C., Wang, X. N., Kolch, W., Multhoff, G., and Dickinson, A. M. (2010) Identification of potential HLA class I and class II epitope precursors associated with heat shock protein 70 (HSPA). Cell Stress Chaperones 15, 729-741
4. Stocki, P., Wang, X. N., Morris, N. J., and Dickinson, A. M. (2011) HSP70 natively and specifically associates with an N-terminal dermcidin-derived peptide that contains an HLA-A*03 antigenic epitope. J. Biol. Chem. 286, 12803-12811
5. Srivastava, P. (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2, 185-194
6. Binder, R. J., Harris, M. L., Ménoret, A., and Srivastava, P. K. (2000) Saturation, competition, and specificity in interaction of heat shock proteins (Hsp) gp96, Hsp90, and Hsp70 with CD11b+ cells. J. Immunol. 165, 2582-2587 (Pubitemid 30660704)
7. Delneste, Y., Magistrelli, G., Gauchat, J., Haeuw, J., Aubry, J., Nakamura, K., Kawakami-Honda, N., Goetsch, L., Sawamura, T., Bonnefoy, J., and Jeannin, P. (2002) Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 17, 353-362 (Pubitemid 35279555)
8. Thériault, J. R., Mambula, S. S., Sawamura, T., Stevenson, M. A., and Calderwood, S. K. (2005) Extracellular HSP70 binding to surface receptors present on antigen presenting cells and endothelial/epithelial cells. FEBS Lett. 579, 1951-1960 (Pubitemid 40404037)
9. Asea, A., Kraeft, S. K., Kurt-Jones, E. A., Stevenson, M. A., Chen, L. B., Finberg, R. W., Koo, G. C., and Calderwood, S. K. (2000) HSP70 stimulates cytokine production through a CD14-dependent pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6, 435-442 (Pubitemid 30208161)
10. Vabulas, R. M., Ahmad-Nejad, P., Ghose, S., Kirschning, C. J., Issels, R. D., and Wagner, H. (2002) HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277, 15107-15112 (Pubitemid 34952589)
11. Asea, A., Rehli, M., Kabingu, E., Boch, J. A., Bare, O., Auron, P. E., Stevenson, M. A., and Calderwood, S. K. (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277, 15028-15034 (Pubitemid 34952579)
12. Gao, B., and Tsan, M. F. (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 (Pubitemid 36043559)
13. Bausinger, H., Lipsker, D., Ziylan, U., Manié, S., Briand, J. P., Cazenave, J. P., Muller, S., Haeuw, J. F., Ravanat, C., de la Salle, H., and Hanau, D. (2002) Endotoxin-free heat-shock protein 70 fails to induce APC activation. Eur. J. Immunol. 32, 3708-3713 (Pubitemid 36032655)
14. Ye, Z., and Gan, Y. H. (2007) Flagellin contamination of recombinant heat shock protein 70 is responsible for its activity on T cells. J. Biol. Chem. 282, 4479-4484 (Pubitemid 47100931)
15. Motta, A., Schmitz, C., Rodrigues, L., Ribeiro, F., Teixeira, C., Detanico, T., Bonan, C., Zwickey, H., and Bonorino, C. (2007) Mycobacterium tuberculosis heat-shock protein 70 impairs maturation of dendritic cells from bone marrow precursors, induces interleukin-10 production, and inhibits T-cell proliferation in vitro. Immunology 121, 462-472 (Pubitemid 47030084)
16. Bendz, H., Marincek, B. C., Momburg, F., Ellwart, J. W., Issels, R. D., Nelson, P. J., and Noessner, E. (2008) Calcium signaling in dendritic cells by human or mycobacterial Hsp70 is caused by contamination and is not required for Hsp70-mediated enhancement of cross-presentation. J. Biol. Chem. 283, 26477-26483
17. Bendz, H., Ruhland, S. C., Pandya, M. J., Hainzl, O., Riegelsberger, S., Braüchle, C., Mayer, M. P., Buchner, J., Issels, R. D., and Noessner, E. (2007) Human heat shock protein 70 enhances tumor antigen presentation through complex formation and intracellular antigen delivery without innate immune signaling. J. Biol. Chem. 282, 31688-31702 (Pubitemid 350044903)
18. Triantafilou, K., Triantafilou, M., and Dedrick, R. L. (2001) A CD14-independent LPS receptor cluster. Nat. Immunol. 2, 338-345 (Pubitemid 33706345)
19. Triantafilou, M., and Triantafilou, K. (2004) Heat-shock protein 70 and heat-shock protein 90 associate with Toll-like receptor 4 in response to bacterial lipopolysaccharide. Biochem. Soc. Trans. 32, 636-639 (Pubitemid 39120403)
20. Basu, S., Binder, R. J., Suto, R., Anderson, K. M., and Srivastava, P. K. (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int. Immunol. 12, 1539-1546
21. Panjwani, N. N., Popova, L., and Srivastava, P. K. (2002) Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J. Immunol. 168, 2997-3003 (Pubitemid 34211681)
22. Zheng, H., Nagaraja, G. M., Kaur, P., Asea, E. E., and Asea, A. (20109) Chaperokine function of recombinant Hsp72 produced in insect cells using a baculovirus expression system is retained. J. Biol. Chem. 285, 349-356
23. Figueiredo, C., Wittmann, M., Wang, D., Dressel, R., Seltsam, A., Blasczyk, R., and Eiz-Vesper, B. (2009) Heat shock protein 70 (HSP70) induces cytotoxicity of T-helper cells. Blood 113, 3008-3016
24. Sallusto, F., and Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and down-regulated by tumor necrosis factor α. J. Exp. Med. 179, 1109-1118
25. Henderson, B., Calderwood, S. K., Coates, A. R., Cohen, I., van Eden, W., Lehner, T., and Pockley, A. G. (2010) Caught with their PAMPs down? The extracellular signalling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 15, 123-141
26. Jarvis, M., Marzolini, M., Wang, X. N., Jackson, G., Sviland, L., and Dickinson, A. M. (2003) Heat shock protein 70: correlation of expression with degree of graft-versus-host response and clinical graft-versus-host disease. Transplantation 76, 849-853 (Pubitemid 37140231)
27. Baba, H. A., Schmid, C., Wilhelm, M. J., Blasius, S., Scheld, H. H., Böcker, W., and Dockhorn-Dworniczak, B. (1997) Inducible heat shock protein 70 in rat cardiac allograft and its immunohistochemical localization in cardiac myocytes. Transplantation 64, 1035-1040 (Pubitemid 27446770)
28. Ludwig, D., Stahl, M., Ibrahim, E. T., Wenzel, B. E., Drabicki, D., Wecke, A., Fellermann, K., and Stange, E. F. (1999) Enhanced intestinal expression of heat shock protein 70 in patients with inflammatory bowel diseases. Dig. Dis. Sci. 44, 1440-1447
29. Njemini, R., Lambert, M., Demanet, C., and Mets, T. (2003) Elevated serum heat-shock protein 70 levels in patients with acute infection: use of an optimized enzyme-linked immunosorbent assay. Scand J. Immunol. 58, 664-669 (Pubitemid 37521942)
30. Multhoff, G., Botzler, C., Wiesnet, M., Müller, E., Meier, T., Wilmanns, W., and Issels, R. D. (1995) A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int. J. Cancer 61, 272-279
31. Mambula, S. S., and Calderwood, S. K. (2006) Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J. Immunol. 177, 7849-7857 (Pubitemid 44848243)
32. Hantschel, M., Pfister, K., Jordan, A., Scholz, R., Andreesen, R., Schmitz, G., Schmetzer, H., Hiddemann, W., and Multhoff, G. (2000) Hsp70 plasma membrane expression on primary tumor biopsy material and bone marrow of leukemic patients. Cell Stress Chaperones 5, 438-442 (Pubitemid 32057495)
33. Pfister, K., Radons, J., Busch, R., Tidball, J. G., Pfeifer, M., Freitag, L., Feldmann, H. J., Milani, V., Issels, R., and Multhoff, G. (2007) Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer 110, 926-935 (Pubitemid 47257673)