Functions of heat shock proteins in pathways of the innate and adaptive immune system

Journal of Immunology

Volumn 193, Issue 12, 2014, Pages 5765-5771

  Binder, Robert Julian ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; PEPTIDE; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; PROTEIN BINDING;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL PROTECTION; HIGH TEMPERATURE; HUMAN; IMMUNOPATHOGENESIS; IMMUNOSURVEILLANCE; IMMUNOTHERAPY; INFECTION; INNATE IMMUNITY; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RHEUMATOID ARTHRITIS; SHORT SURVEY; TUMOR IMMUNITY; ANIMAL; EXTRACELLULAR SPACE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN PRESENTATION; EXTRACELLULAR SPACE; HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, INNATE; PEPTIDES; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84916919262     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401417     Document Type: Short Survey

References (105)

1. Ritossa, F. 1962. A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18: 571-573.
2. Lindquist, S., and E. A. Craig. 1988. The heat-shock proteins. Annu. Rev. Genet. 22: 631-677.
3. Zhu, X., X. Zhao, W. F. Burkholder, A. Gragerov, C. M. Ogata, M. E. Gottesman, and W. A. Hendrickson. 1996. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272: 1606-1614.
4. Peng, P., A. Ménoret, and P. K. Srivastava. 1997. Purification of immunogenic heat shock protein 70-peptide complexes by ADP-affinity chromatography. J. Immunol. Methods 204: 13-21.
5. Chouquet, A., H. Païdassi, W. L. Ling, P. Frachet, G. Houen, G. J. Arlaud, and C. Gaboriaud. 2011. X-ray structure of the human calreticulin globular domain reveals a peptide-binding area and suggests a multi-molecular mechanism. PLoS ONE 6: e17886.
6. Stirling, P. C., S. F. Bakhoum, A. B. Feigl, and M. R. Leroux. 2006. Convergent evolution of clamp-like binding sites in diverse chaperones. Nat. Struct. Mol. Biol. 13: 865-870.
7. Ostrovsky, O., C. A. Makarewich, E. L. Snapp, and Y. Argon. 2009. An essential role for ATP binding and hydrolysis in the chaperone activity of GRP94 in cells. Proc. Natl. Acad. Sci. USA 106: 11600-11605.
8. Grossmann, M. E., B. J. Madden, F. Gao, Y. P. Pang, J. E. Carpenter, D. McCormick, and C. Y. Young. 2004. Proteomics shows Hsp70 does not bind peptide sequences indiscriminately in vivo. Exp. Cell Res. 297: 108-117.
9. Demine, R., and P. Walden. 2005. Testing the role of gp96 as peptide chaperone in antigen processing. J. Biol. Chem. 280: 17573-17578.
10. Li, H. Z., C. W. Li, C. Y. Li, B. F. Zhang, L. T. Li, J. M. Li, J. N. Zheng, and J. W. Chang. 2013. Isolation and identification of renal cell carcinoma-derived peptides associated with GP96. Technol. Cancer Res. Treat. 12: 285-293.
11. Ménoret, A., P. Peng, and P. K. Srivastava. 1999. Association of peptides with heat shock protein gp96 occurs in vivo and not after cell lysis. Biochem. Biophys. Res. Commun. 262: 813-818.
12. Nieland, T. J., M. C. Tan, M. Monne-van Muijen, F. Koning, A. M. Kruisbeek, and G. M. van Bleek. 1996. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc. Natl. Acad. Sci. USA 93: 6135-6139.
13. Navaratnam, M., M. S. Deshpande, M. J. Hariharan, D. S. Zatechka, Jr., and S. Srikumaran. 2001. Heat shock protein-peptide complexes elicit cytotoxic T-lymphocyte and antibody responses specific for bovine herpesvirus 1. Vaccine 19: 1425-1434.
14. Meng, S. D., T. Gao, G. F. Gao, and P. Tien. 2001. HBV-specific peptide associated with heat-shock protein gp96. Lancet 357: 528-529.
15. Heikema, A., E. Agsteribbe, J. Wilschut, and A. Huckriede. 1997. Generation of heat shock protein-based vaccines by intracellular loading of gp96 with antigenic peptides. Immunol. Lett. 57: 69-74.
16. Strbo, N., M. Vaccari, S. Pahwa, M. A. Kolber, M. N. Doster, E. Fisher, L. Gonzalez, D. Stablein, G. Franchini, and E. R. Podack. 2013. Cutting edge: novel vaccination modality provides significant protection against mucosal infection by highly pathogenic simian immunodeficiency virus. J. Immunol. 190: 2495-2499.
17. Basta, S., R. Stoessel, M. Basler, M. van den Broek, and M. Groettrup. 2005. Cross-presentation of the long-lived lymphocytic choriomeningitis virus nucleoprotein does not require neosynthesis and is enhanced via heat shock proteins. J. Immunol. 175: 796-805.
18. Zügel, U., A. M. Sponaas, J. Neckermann, B. Schoel, and S. H. Kaufmann. 2001. gp96-peptide vaccination of mice against intracellular bacteria. Infect. Immun. 69: 4164-4167.
19. Rapp, U. K., and S. H. Kaufmann. 2004. DNA vaccination with gp96-peptide fusion proteins induces protection against an intracellular bacterial pathogen. Int. Immunol. 16: 597-605.
20. Castelli, C., A. M. Ciupitu, F. Rini, L. Rivoltini, A. Mazzocchi, R. Kiessling, and G. Parmiani. 2001. Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res. 61: 222-227.
21. Ishii, T., H. Udono, T. Yamano, H. Ohta, A. Uenaka, T. Ono, A. Hizuta, N. Tanaka, P. K. Srivastava, and E. Nakayama. 1999. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J. Immunol. 162: 1303-1309.
22. Qian, J., S. Wang, J. Yang, J. Xie, P. Lin, M. E. Freeman, III, and Q. Yi. 2005. Targeting heat shock proteins for immunotherapy in multiple myeloma: generation of myeloma-specific CTLs using dendritic cells pulsed with tumor-derived gp96. Clin. Cancer Res. 11: 8808-8815.
23. Breloer, M., T. Marti, B. Fleischer, and A. von Bonin. 1998. Isolation of processed, H-2Kb-binding ovalbumin-derived peptides associated with the stress proteins HSP70 and gp96. Eur. J. Immunol. 28: 1016-1021.
24. Arnold, D., C. Wahl, S. Faath, H.-G. Rammensee, and H. Schild. 1997. Influences of transporter associated with antigen processing (TAP) on the repertoire of peptides associated with the endoplasmic reticulum-resident stress protein gp96. J. Exp. Med. 186: 461-466.
25. Binder, R. J., J. B. Kelly, III, R. E. Vatner, and P. K. Srivastava. 2007. Specific immunogenicity of heat shock protein gp96 derives from chaperoned antigenic peptides and not from contaminating proteins. J. Immunol. 179: 7254-7261.
26. Dai, J., B. Liu, M. M. Caudill, H. Zheng, Y. Qiao, E. R. Podack, and Z. Li. 2003. Cell surface expression of heat shock protein gp96 enhances cross-presentation of cellular antigens and the generation of tumor-specific T cell memory. Cancer Immun. 3: 1.
27. Nair, S., P. A. Wearsch, D. A. Mitchell, J. J. Wassenberg, E. Gilboa, and C. V. Nicchitta. 1999. Calreticulin displays in vivo peptide-binding activity and can elicit CTL responses against bound peptides. J. Immunol. 162: 6426-6432.
28. Arnold, D., S. Faath, H. Rammensee, and H. Schild. 1995. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J. Exp. Med. 182: 885-889.
29. Lammert, E., D. Arnold, H. G. Rammensee, and H. Schild. 1996. Expression levels of stress protein gp96 are not limiting for major histocompatibility complex class I-restricted antigen presentation. Eur. J. Immunol. 26: 875-879.
30. Robert, J., T. Ramanayake, G. D. Maniero, H. Morales, and A. S. Chida. 2008. Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. J. Immunol. 180: 3176-3182.
31. Yedavelli, S. P., L. Guo, M. E. Daou, P. K. Srivastava, A. Mittelman, and R. K. Tiwari. 1999. Preventive and therapeutic effect of tumor derived heat shock protein, gp96, in an experimental prostate cancer model. Int. J. Mol. Med. 4: 243-248.
32. Yewdell, J. W., and C. V. Nicchitta. 2006. The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol. 27: 368-373.
33. Rock, K. L., D. J. Farfán-Arribas, J. D. Colbert, and A. L. Goldberg. 2014. Reexamining class-I presentation and the DRiP hypothesis. Trends Immunol. 35: 144-152.
34. Blum, J. S., P. A. Wearsch, and P. Cresswell. 2013. Pathways of antigen processing. Annu. Rev. Immunol. 31: 443-473.
35. Dick, T. P., T. Ruppert, M. Groettrup, P. M. Kloetzel, L. Kuehn, U. H. Koszinowski, S. Stevanović, H. Schild, and H. G. Rammensee. 1996. Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell 86: 253-262.
36. Villanueva, M. S., P. Fischer, K. Feen, and E. G. Pamer. 1994. Efficiency of MHC class I antigen processing: a quantitative analysis. Immunity 1: 479-489.
37. Yewdell, J. W., E. Reits, and J. Neefjes. 2003. Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3: 952-961.
38. Srivastava, P. K., H. Udono, N. E. Blachere, and Z. Li. 1994. Heat shock proteins transfer peptides during antigen processing and CTL priming. Immunogenetics 39: 93-98.
39. Binder, R. J., N. E. Blachere, and P. K. Srivastava. 2001. Heat shock proteinchaperoned peptides but not free peptides introduced into the cytosol are presented efficiently by major histocompatibility complex I molecules. J. Biol. Chem. 276: 17163-17171.
40. Callahan, M. K., M. Garg, and P. K. Srivastava. 2008. Heat-shock protein 90 associates with N-terminal extended peptides and is required for direct and indirect antigen presentation. Proc. Natl. Acad. Sci. USA 105: 1662-1667.
41. Kunisawa, J., and N. Shastri. 2006. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 24: 523-534.
42. Kropp, L. E., M. Garg, and R. J. Binder. 2010. Ovalbumin-derived precursor peptides are transferred sequentially from gp96 and calreticulin to MHC class I in the endoplasmic reticulum. J. Immunol. 184: 5619-5627.
43. Spee, P., and J. Neefjes. 1997. TAP-translocated peptides specifically bind proteins in the endoplasmic reticulum, including gp96, protein disulfide isomerase and calreticulin. Eur. J. Immunol. 27: 2441-2449.
44. Anderson, S. L., T. Shen, J. Lou, L. Xing, N. E. Blachere, P. K. Srivastava, and B. Y. Rubin. 1994. The endoplasmic reticular heat shock protein gp96 is transcriptionally upregulated in interferon-treated cells. J. Exp. Med. 180: 1565-1569.
45. Wang, S., M. Zhou, F. Lin, D. Liu, W. Hong, L. Lu, Y. Zhu, and A. Xu. 2014. Interferon-γ induces senescence in normal human melanocytes. PLoS ONE 9: e93232.
46. Yamano, T., S. Mizukami, S. Murata, T. Chiba, K. Tanaka, and H. Udono. 2008. Hsp90-mediated assembly of the 26 S proteasome is involved in major histocompatibility complex class I antigen processing. J. Biol. Chem. 283: 28060-28065.
47. Yamano, T., S. Murata, N. Shimbara, N. Tanaka, T. Chiba, K. Tanaka, K. Yui, and H. Udono. 2002. Two distinct pathways mediated by PA28 and hsp90 in major histocompatibility complex class I antigen processing. J. Exp. Med. 196: 185-196.
48. French, J. B., H. Zhao, S. An, S. Niessen, Y. Deng, B. F. Cravatt, and S. J. Benkovic. 2013. Hsp70/Hsp90 chaperone machinery is involved in the assembly of the purinosome. Proc. Natl. Acad. Sci. USA 110: 2528-2533.
49. Chen, D., and M. J. Androlewicz. 2001. Heat shock protein 70 moderately enhances peptide binding and transport by the transporter associated with antigen processing. Immunol. Lett. 75: 143-148.
50. Jutras, I., and M. Desjardins. 2005. Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell Dev. Biol. 21: 511-527.
51. Ichiyanagi, T., T. Imai, C. Kajiwara, S. Mizukami, A. Nakai, T. Nakayama, and H. Udono. 2010. Essential role of endogenous heat shock protein 90 of dendritic cells in antigen cross-presentation. J. Immunol. 185: 2693-2700.
52. Imai, T., Y. Kato, C. Kajiwara, S. Mizukami, I. Ishige, T. Ichiyanagi, M. Hikida, J. Y. Wang, and H. Udono. 2011. Heat shock protein 90 (HSP90) contributes to cytosolic translocation of extracellular antigen for cross-presentation by dendritic cells. Proc. Natl. Acad. Sci. USA 108: 16363-16368.
53. Liu, B., Y. Yang, Z. Qiu, M. Staron, F. Hong, Y. Li, S. Wu, Y. Li, B. Hao, R. Bona, et al. 2010. Folding of Toll-like receptors by the HSP90 paralogue gp96 requires a substrate-specific cochaperone. Nat. Commun. 1: 79.
54. Wu, S., F. Hong, D. Gewirth, B. Guo, B. Liu, and Z. Li. 2012. The molecular chaperone gp96/GRP94 interacts with Toll-like receptors and integrins via its Cterminal hydrophobic domain. J. Biol. Chem. 287: 6735-6742.
55. Staron, M., Y. Yang, B. Liu, J. Li, Y. Shen, J. C. Zúñiga-Pflücker, H. L. Aguila, I. Goldschneider, and Z. Li. 2010. gp96, an endoplasmic reticulum master chaperone for integrins and Toll-like receptors, selectively regulates early T and B lymphopoiesis. Blood 115: 2380-2390.
56. Miyake, Y., and S. Yamasaki. 2012. Sensing necrotic cells. Adv. Exp. Med. Biol. 738: 144-152.
57. Hunter, M. C., K. L. O'Hagan, A. Kenyon, K. C. Dhanani, E. Prinsloo, and A. L. Edkins. 2014. Hsp90 binds directly to fibronectin (FN) and inhibition reduces the extracellular fibronectin matrix in breast cancer cells. PLoS ONE 9: e86842.
58. Altmeyer, A., R. G. Maki, A. M. Feldweg, M. Heike, V. P. Protopopov, S. K. Masur, and P. K. Srivastava. 1996. Tumor-specific cell surface expression of the-KDEL containing, endoplasmic reticular heat shock protein gp96. Int. J. Cancer 69: 340-349.
59. Becker, B., G. Multhoff, B. Farkas, P. J. Wild, M. Landthaler, W. Stolz, and T. Vogt. 2004. Induction of Hsp90 protein expression in malignant melanomas and melanoma metastases. Exp. Dermatol. 13: 27-32.
60. Binder, R. J., D. K. Han, and P. K. Srivastava. 2000. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1: 151-155.
61. 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.
62. Binder, R. J., and P. K. Srivastava. 2004. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc. Natl. Acad. Sci. USA 101: 6128-6133.
63. Binder, R. J. 2009. Hsp receptors: the cases of identity and mistaken identity. Curr. Opin. Mol. Ther. 11: 62-71.
64. Schreiber, R. D., L. J. Old, and M. J. Smyth. 2011. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331: 1565-1570.
65. North, R. J., and D. P. Kirstein. 1977. T-cell-mediated concomitant immunity to syngeneic tumors. I. Activated macrophages as the expressors of nonspecific immunity to unrelated tumors and bacterial parasites. J. Exp. Med. 145: 275-292.
66. den Haan, J. M., and M. J. Bevan. 2001. Antigen presentation to CD8+ T cells: cross-priming in infectious diseases. Curr. Opin. Immunol. 13: 437-441.
67. Blanchard, T., P. K. Srivastava, and F. Duan. 2013. Vaccines against advanced melanoma. Clin. Dermatol. 31: 179-190.
68. Ma, Y., L. Aymeric, C. Locher, G. Kroemer, and L. Zitvogel. 2011. The dendritic cell-tumor cross-talk in cancer. Curr. Opin. Immunol. 23: 146-152.
69. Binder, R. J., and P. K. Srivastava. 2005. Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8+ T cells. Nat. Immunol. 6: 593-599.
70. Li, M., G. M. Davey, R. M. Sutherland, C. Kurts, A. M. Lew, C. Hirst, F. R. Carbone, and W. R. Heath. 2001. Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo. J. Immunol. 166: 6099-6103.
71. Kovacsovics-Bankowski, M., and K. L. Rock. 1995. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267: 243-246.
72. Messmer, M. N., J. Pasmowitz, L. E. Kropp, S. C. Watkins, and R. J. Binder. 2013. Identification of the cellular sentinels for native immunogenic heat shock proteins in vivo. J. Immunol. 191: 4456-4465.
73. Suto, R., and P. K. Srivastava. 1995. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 269: 1585-1588.
74. Blachere, N. E., Z. Li, R. Y. Chandawarkar, R. Suto, N. S. Jaikaria, S. Basu, H. Udono, and P. K. Srivastava. 1997. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J. Exp. Med. 186: 1315-1322.
75. Zhou, Y. J., M. N. Messmer, and R. J. Binder. 2014. Establishment of tumor-associated immunity requires interaction of heat shock proteins with CD91. Cancer Immunol. Res 2: 217-228.
76. Norbury, C. C., S. Basta, K. B. Donohue, D. C. Tscharke, M. F. Princiotta, P. Berglund, J. Gibbs, J. R. Bennink, and J. W. Yewdell. 2004. CD8+ T cell cross-priming via transfer of proteasome substrates. Science 304: 1318-1321.
77. Basu, S., R. J. Binder, R. Suto, K. M. Anderson, and P. K. Srivastava. 2000. 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: 1539-1546.
78. Pawaria, S., and R. J. Binder. 2011. CD91-dependent programming of T-helper cell responses following heat shock protein immunization. Nat. Commun. 2: 521.
79. Gallo, P. M., and S. Gallucci. 2013. The dendritic cell response to classic, emerging, and homeostatic danger signals. Implications for autoimmunity. Front. Immunol. 4: 138.
80. Li, W., D. Mu, F. Tian, Y. Hu, T. Jiang, Y. Han, J. Chen, G. Han, and X. Li. 2013. Exosomes derived from Rab27a-overexpressing tumor cells elicit efficient induction of antitumor immunity. Mol. Med. Rep. 8: 1876-1882.
81. Martin, C. A., S. E. Carsons, R. Kowalewski, D. Bernstein, M. Valentino, and F. Santiago-Schwarz. 2003. Aberrant extracellular and dendritic cell (DC) surface expression of heat shock protein (hsp)70 in the rheumatoid joint: possible mechanisms of hsp/DC-mediated cross-priming. J. Immunol. 171: 5736-5742.
82. Sedlackova, L., T. T. Nguyen, D. Zlacka, A. Sosna, and I. Hromadnikova. 2009. Cell surface and relative mRNA expression of heat shock protein 70 in human synovial cells. Autoimmunity 42: 17-24.
83. Huang, Q. Q., R. Sobkoviak, A. R. Jockheck-Clark, B. Shi, A. M. Mandelin, II, P. P. Tak, G. K. Haines, III, C. V. Nicchitta, and R. M. Pope. 2009. Heat shock protein 96 is elevated in rheumatoid arthritis and activates macrophages primarily via TLR2 signaling. J. Immunol. 182: 4965-4973.
84. Auger, I., J. M. Escola, J. P. Gorvel, and J. Roudier. 1996. HLA-DR4 and HLA-DR10 motifs that carry susceptibility to rheumatoid arthritis bind 70-kD heat shock proteins. Nat. Med. 2: 306-310.
85. van Herwijnen, M. J., L. Wieten, R. van der Zee, P. J. van Kooten, J. P. Wagenaar-Hilbers, A. Hoek, I. den Braber, S. M. Anderton, M. Singh, H. D. Meiring, et al. 2012. Regulatory T cells that recognize a ubiquitous stress-inducible self-antigen are long-lived suppressors of autoimmune arthritis. Proc. Natl. Acad. Sci. USA 109: 14134-14139.
86. Massa, M., M. Passalia, S. M. Manzoni, R. Campanelli, L. Ciardelli, G. P. Yung, S. Kamphuis, A. Pistorio, V. Meli, A. Sette, et al. 2007. Differential recognition of heat-shock protein dnaJ-derived epitopes by effector and Treg cells leads to modulation of inflammation in juvenile idiopathic arthritis. Arthritis Rheum. 56: 1648-1657.
87. Aalberse, J. A., B. J. Prakken, and B. Kapitein. 2012. HSP: Bystander Antigen in Atopic Diseases? Front. Immunol. 3: 139-144.
88. Liu, B., J. Dai, H. Zheng, D. Stoilova, S. Sun, and Z. Li. 2003. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc. Natl. Acad. Sci. USA 100: 15824-15829.
89. Strbo, N., K. Yamazaki, K. Lee, D. Rukavina, and E. R. Podack. 2002. Heat shock fusion protein gp96-Ig mediates strong CD8 CTL expansion in vivo. Am. J. Reprod. Immunol. 48: 220-225.
90. Srivastava, P. K., A. B. DeLeo, and L. J. Old. 1986. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc. Natl. Acad. Sci. USA 83: 3407-3411.
91. Udono, H., and P. K. Srivastava. 1994. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J. Immunol. 152: 5398-5403.
92. Udono, H., and P. K. Srivastava. 1993. Heat shock protein 70-associated peptides elicit specific cancer immunity. J. Exp. Med. 178: 1391-1396.
93. Basu, S., and P. K. Srivastava. 1999. Calreticulin, a peptide-binding chaperone of the endoplasmic reticulum, elicits tumor- and peptide-specific immunity. J. Exp. Med. 189: 797-802.
94. Wang, X. Y., L. Kazim, E. A. Repasky, and J. R. Subjeck. 2001. Characterization of heat shock protein 110 and glucose-regulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine activity. J. Immunol. 166: 490-497.
95. Eldor, R., S. Kassem, and I. Raz. 2009. Immune modulation in type 1 diabetes mellitus using DiaPep277: a short review and update of recent clinical trial results. Diabetes Metab. Res. Rev. 25: 316-320.
96. Birk, O. S., D. C. Douek, D. Elias, K. Takacs, H. Dewchand, S. L. Gur, M. D. Walker, R. van der Zee, I. R. Cohen, and D. M. Altmann. 1996. A role of Hsp60 in autoimmune diabetes: analysis in a transgenic model. Proc. Natl. Acad. Sci. USA 93: 1032-1037.
97. Chandawarkar, R. Y., M. S. Wagh, and P. K. Srivastava. 1999. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J. Exp. Med. 189: 1437-1442.
98. Chandawarkar, R. Y., M. S. Wagh, J. T. Kovalchin, and P. Srivastava. 2004. Immune modulation with high-dose heat-shock protein gp96: therapy of murine autoimmune diabetes and encephalomyelitis. Int. Immunol. 16: 615-624.
99. Kovalchin, J. T., C. Mendonca, M. S. Wagh, R. Wang, and R. Y. Chandawarkar. 2006. In vivo treatment of mice with heat shock protein, gp 96, improves survival of skin grafts with minor and major antigenic disparity. Transpl. Immunol. 15: 179-185.
100. Tamura, Y., P. Peng, K. Liu, M. Daou, and P. K. Srivastava. 1997. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 278: 117-120.
101. Mo, A., C. Musselli, H. Chen, J. Pappas, K. Leclair, A. Liu, R. M. Chicz, A. Truneh, S. Monks, D. L. Levey, and P. K. Srivastava. 2011. A heat shock protein based polyvalent vaccine targeting HSV-2: CD4(+) and CD8(+) cellular immunity and protective efficacy. Vaccine 29: 8530-8541.
102. di Pietro, A., G. Tosti, P. F. Ferrucci, and A. Testori. 2011. The immunological era in melanoma treatment: new challenges for heat shock protein-based vaccine in the advanced disease. Expert Opin. Biol. Ther. 11: 1395-1407.
103. Raz, I., A. G. Ziegler, T. Linn, G. Schernthaner, F. Bonnici, L. A. Distiller, C. Giordano, F. Giorgino, L. de Vries, D. Mauricio, et al; DIA-AID 1 Writing Group. 2014. Treatment of recent-onset type 1 diabetic patients with DiaPep277: results of a double-blind, placebo-controlled, randomized phase 3 trial. Diabetes Care 37: 1392-1400.
104. Wald, A., D. M. Koelle, K. Fife, T. Warren, K. Leclair, R. M. Chicz, S. Monks, D. L. Levey, C. Musselli, and P. K. Srivastava. 2011. Safety and immunogenicity of long HSV-2 peptides complexed with rhHsc70 in HSV-2 seropositive persons. Vaccine 29: 8520-8529.
105. Liu, Z., X. Li, L. Qiu, X. Zhang, L. Chen, S. Cao, F. Wang, and S. Meng. 2009. Treg suppress CTL responses upon immunization with HSP gp96. Eur. J. Immunol. 39: 3110-3120.