ISO: A critical evaluation of the role of peptides in heat shock/chaperone protein-mediated tumor rejection

Current Opinion in Immunology

Volumn 15, Issue 1, 2003, Pages 89-94

  Baker LePain, Julie C ^a   Reed, Robyn C ^a   Nicchitta, Christopher V ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; PEPTIDE; SARCOMA GLYCOPROTEIN GP96 REJECTION ANTIGENS; TUMOR ANTIGEN;

IMMUNITY; IMMUNOGENICITY; MOLECULAR DYNAMICS; PROTEIN FUNCTION; REVIEW; TUMOR REJECTION; ANIMAL; ANTIGEN PRESENTATION; CELLULAR IMMUNITY; GRAFT REJECTION; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; NEOPLASM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; GRAFT REJECTION; HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; MOLECULAR CHAPERONES; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 0037290769     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952791502000067     Document Type: Review

References (55)

1. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20:2002;395-425 A very comprehensive and personal account of the identification and analysis of gp96 function as a tumor-specific transplantation antigen. Contains a thorough summary of the data supporting a peptide-basis for gp96 immunogenicity.
2. Basu S., Binder R.J., Suto R., Anderson K.M., Srivastava P.K. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int. Immunol. 12:2000;1539-1546.
3. Berwin B., Reed R.C., Nicchitta C.V. Virally induced lytic cell death elicits the release of immunogenic GRP94/gp96. J. Biol. Chem. 276:2001;21083-21088.
4. Singh-Jasuja H., Toes R.E., Spee P., Munz C., Hilf N., Schoenberger S.P., Ricciardi-Castagnoli P., Neefjes J., Rammensee H.G., Arnold-Schild D.et al. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. J. Exp. Med. 191:2000;1965-1974.
5. Binder R.J., Han D.K., Srivastava P.K. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1:2000;151-155.
6. Wassenberg J.J., Dezfulian C., Nicchitta C.V. Receptor mediated and fluid phase pathways for internalization of the ER Hsp90 chaperone GRP94 in murine macrophages. J. Cell Sci. 112:1999;2167-2175.
7. Vabulas R.M., Braedel S., Hilf N., Singh-Jasuja H., Herter S., Ahmad-Nejad P., Kirschning C.J., Da Costa C., Rammensee H.G., Wagner H.et al. The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J. Biol. Chem. 277:2002;20847-20853 In extending insights into the role of gp96 in innate immunity, this report provides evidence indicating that gp96 binding to TLRs 2/4 elicits DC activation.
8. Berwin B., Rosser M.F., Brinker K.G., Nicchitta C.V. Transfer of GRP94(Gp96)-associated peptides onto endosomal MHC class I molecules. Traffic. 3:2002;358-366 The first report to identify a potential subcellular trafficking pathway for re-presentation of gp96-bound peptides. The authors provide evidence that gp96-bound peptides can be transferred onto structurally mature MHC class I molecules.
9. Srivastava P.K., DeLeo A.B., Old L.J. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc. Natl. Acad. Sci. U.S.A. 83:1986;3407-3411.
10. Srivastava P.K., Heike M. Tumor-specific immunogenicity of stress-induced proteins: convergence of two evolutionary pathways of antigen presentation? Semin. Immunol. 3:1991;57-64.
11. Flynn G.C., Chappell T.G., Rothman J.E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science. 245:1989;385-390.
12. Blachere N.E., Li Z., Chandawarkar R.Y., Suto R., Jaikaria N.S., Basu S., Udono H., Srivastava P.K. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J. Exp. Med. 186:1997;1315-1322.
13. Wearsch P.A., Nicchitta C.V. Interaction of endoplasmic reticulum chaperone GRP94 with peptide substrates is adenine nucleotide-independent. J. Biol. Chem. 272:1997;5152-5156.
14. Lefkovitz I (Ed): Immunology Methods Manual. Orlando, FL, USA: Academic Press; 1997.
15. Flynn G.C., Pohl J., Flocco M.T., Rothman J.E. Peptide-binding specificity of the molecular chaperone BiP. Nature. 353:1991;726-730.
16. Blond-Elguindi S., Cwirla S.E., Dower W.J., Lipshutz R.J., Sprang S.R., Sambrook J.F., Gething M.J. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell. 75:1993;717-728.
17. Spee P., Neefjes J. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur. J. Immunol. 27:1997;2441-2449.
18. Suto R., Srivastava P.K. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science. 269:1995;1585-1588.
19. Kornberg A. Why purify enzymes? Methods Enzymol. 182:1990;1-5.
20. Singh-Jasuja H., Scherer H.U., Hilf N., Arnold-Schild D., Rammensee H.G., Toes R.E., Schild H. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur. J. Immunol. 30:2000;2211-2215.
21. Panjwani N.N., Popova L., Srivastava P.K. Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J. Immunol. 168:2002;2997-3003 The authors report that gp96 and Hsp70 activate nitric oxide production in APCs. These data provide further evidence of a potentially important role for gp96 and Hsp70 in innate immunity.
22. Reed R.C., Zheng T., Nicchitta C.V. GRP94-associated enzymatic activities. Resolution by chromatographic fractionation. J. Biol. Chem. 277:2002;25082-25089.
23. Li M., Davey G.M., Sutherland R.M., Kurts C., Lew A.M., Hirst C., Carbone F.R., Heath W.R. Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J. Immunol. 166:2001;6099-6103.
24. Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat. Rev. Immunol. 2:2002;185-194.
25. Paz P., Brouwenstijn N., Perry R., Shastri N. Discrete proteolytic intermediates in the MHC class I antigen processing pathway and MHC I-dependent peptide trimming in the ER. Immunity. 11:1999;241-251.
26. Fourie A.M., Sambrook J.F., Gething M.J. Common and divergent peptide binding specificities of hsp70 molecular chaperones. J. Biol. Chem. 269:1994;30470-30478.
27. Nicchitta C.V., Reed R. The immunological properties of endoplasmic reticulum chaperones: a conflict of interest? Essays Biochem. 36:2000;15-25.
28. Thulasiraman V., Yun B.G., Uma S., Gu Y., Scroggins B.T., Matts R.L. Differential inhibition of Hsc70 activities by two Hsc70-binding peptides. Biochemistry. 41:2002;3742-3753.
29. Young J.C., Moarefi I., Hartl F.U. Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 154:2001;267-273.
30. Gallouzi I.E., Steitz J.A. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science. 294:2001;1895-1901.
31. Derossi D., Chassaing G., Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 8:1998;84-87.
32. Asea A., Kraeft S.K., Kurt-Jones E.A., Stevenson M.A., Chen L.B., Finberg R.W., Koo G.C., Calderwood S.K. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6:2000;435-442.
33. Kol A., Lichtman A.H., Finberg R.W., Libby P., Kurt-Jones E.A. 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. 164:2000;13-17.
34. Binder R.J., Anderson K.M., Basu S., Srivastava P.K. Cutting edge: heat shock protein gp96 induces maturation and migration of CD11c+ cells in vivo. J. Immunol. 165:2000;6029-6035.
35. Asea A., Kabingu E., Stevenson M.A., Calderwood S.K. HSP70 peptide bearing and peptide-negative preparations act as chaperokines. Cell Stress Chaperones. 5:2000;425-431.
36. Matzinger P. An innate sense of danger. Semin. Immunol. 10:1998;399-415.
37. Gallucci S., Lolkema M., Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 5:1999;1249-1255.
38. Berwin B., Hart J.P., Pizzo S.V., Nicchitta C.V. Cutting edge: CD91-independent cross-presentation of GRP94(gp96)-associated peptides. J. Immunol. 168:2002;4282-4286 This article provides data demonstrating that gp96 uptake into APCs can occur via a CD91-independent pathway and that this pathway for receptor-mediated uptake of gp96 can yield peptide re-presentation.
39. Panjwani N.N., Popova L., Febbraio M., Srivastava P.K. The CD36 scavenger receptor as a receptor for gp96. Cell Stress Chaperones. 5:2000;391.
40. Vabulas R.M., Ahmad-Nejad P., da Costa C., Miethke T., Kirschning C.J., Hacker H., Wagner H. 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. 276:2001;31332-31339.
41. Ohashi K., Burkart V., Flohe S., Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164:2000;558-561.
42. Janeway C.A. Jr., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 20:2002;197-216.
43. Tamura Y., Peng P., Liu K., Daou M., Srivastava P.K. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science. 278:1997;117-120.
44. Blachere N.E., Udono H., Janetzki S., Li Z., Heike M., Srivastava P.K. Heat shock protein vaccines against cancer. J. Immunother. 14:1993;352-356.
45. + T cell responses against minor histocompatability antigens. Of particular interest, they also provide data indicating that, in Xenopus, gp96-elicited tumor rejection can occur independently of bound peptides.
46. Nseyo U.O., Lamm D.L. Immunotherapy of bladder cancer. Semin. Surg. Oncol. 13:1997;342-349.
47. Ratliff T.L., Shapiro A., Catalona W.J. Inhibition of murine bladder tumor growth by bacille Calmette-Guerin: lack of a role of natural killer cells. Clin. Immunol. Immunopathol. 41:1986;108-115.
48. Trinchieri G. Biology of natural killer cells. Adv. Immunol. 47:1989;187-376.
49. Talmadge J.E., Meyers K.M., Prieur D.J., Starkey J.R. Role of natural killer cells in tumor growth and metastasis: C57BL/6 normal and beige mice. J. Natl. Cancer Inst. 65:1980;929-935.
50. Crowe N.Y., Smyth M.J., Godfrey D.I. A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. J. Exp. Med. 196:2002;119-127 This report identifies an innate immunity pathway in the immunosurveillance of methylcholanthrene-induced sarcomas, the tumor model used in the original identification of gp96 tumor-specific transplantation antigen activity.
51. Bendelac A., Medzhitov R. Adjuvants of immunity: harnessing innate immunity to promote adaptive immunity. J. Exp. Med. 195:2002;F19-F23.
52. Fernandez N.C., Lozier A., Flament C., Ricciardi-Castagnoli P., Bellet D., Suter M., Perricaudet M., Tursz T., Maraskovsky E., Zitvogel L. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat. Med. 5:1999;405-411.
53. Zitvogel L. Dendritic and natural killer cells cooperate in the control/switch of innate immunity. J. Exp. Med. 195:2002;F9-F14.
54. Wallin R.P., Lundqvist A., More S.H., von Bonin A., Kiessling R., Ljunggren H.G. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23:2002;130-135.
55. Vogen S., Gidalevitz T., Biswas C., Simen B.B., Stein E., Gulmen F., Argon Y. Radicicol-sensitive peptide binding to the N-terminal portion of GRP94. J. Biol. Chem. 277:2002;40742-40750 The binding of radiolabeled peptides to the amino-terminal domain of GRP94 is demonstrated, and differences between GRP94 and BiP in preferred peptide substrates are reported.