Heat-shock proteins in cancer vaccines: Agents of antigen cross-presentation

Expert Review of Vaccines

Volumn 7, Issue 7, 2008, Pages 1019-1030

  Murshid, Ayesha ^a   Gong, Jianlin ^b   Calderwood, Stuart K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Antigen cross presentation; Heat shock protein; Molecular chaperone; Scavenger receptor; Tumor vaccine

Indexed keywords

CALRETICULIN; CANCER VACCINE; CARCINOEMBRYONIC ANTIGEN; CELL SURFACE PROTEIN; CHAPERONE; ENDOSOMAL PROTEASE; GLYCOPROTEIN GP 100; GLYCOPROTEIN GP 170; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MELAN A; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PROTEIN FEEL 1; PROTEIN SREC 1; SARCOPLASMIC RETICULUM PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CANCER IMMUNOTHERAPY; CANCER REGRESSION; CROSS PRESENTATION; DRUG DOSE REGIMEN; ENDOPLASMIC RETICULUM; ENDOSOME; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; ANTIGENS; CANCER VACCINES; CROSS-PRIMING; HEAT-SHOCK PROTEINS; HUMANS; NEOPLASMS;

EID: 51549104719     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.7.7.1019     Document Type: Review

References (92)

1. Lindquist S, Craig EA. The heat shock proteins. Ann. Rev. Genet. 22, 631-637 (1988).
2. Wegele H, Muller L, Buchner J. Hsp70 and Hsp90 - a relay team for protein folding. Rev. Physiol. Biochem. Pharmacol. 151, 1-44 (2004).
3. Young JC, Agashe VR, Siegers K, Hartl FU. Pathways of chaperone-mediated protein folding in the cytosol. Nat. Rev. Mol. Cell. Biol. 5, 781-791 (2004).
4. Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440, 551-555 (2006).
5. Mayer MP, Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62, 670-684 (2005).
6. Spiess C, Meyer AS, Reissmann S, Frydman J. Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol. 14, 14598-14604 (2004).
7. Pockley AG, Muthana M, Calderwood SK. The dual immunoregulatory roles of stress proteins. Trends Biochem. Sci. 33, 71-79 (2008).
8. Calderwood SK, Theriault JR, Gong J. Message in a bottle: role of the 70-kDa heat shock protein family in anti-tumor immunity. Eur. J. Immunol. 35, 2518-2527 (2005).
9. Srivastava PK. Heat shock protein-based novel immunotherapies. Drug News Perspect 13, 517-522 (2000).
10. + T cells. Nat. Immunol. 6, 593-599 (2005).
11. Tang D, Khaleque MA, Jones EL et al. Expression of heat shock proteins and heat shock protein messenger ribonucleic acid in human prostate carcinoma in vitro and in tumors in vivo. Cell Stress Chaperones 10, 46-58 (2005).
12. Srivastava P. Hypothesis: controlled necrosis as a tool for immunotherapy of human cancer. Cancer Immun. 3, 4 (2003).
13. Asea A, Kraeft SK, Kurt-Jones EA 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 (2000).
14. Asea A, Rehli M, Kabingu E et al. Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR)2 and TLR4. J. Biol. Chem. 277, 15028-15034 (2002).
15. Vabulas RM, Ahmad-Nejad P, Ghose S et al. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277, 15107-15112 (2002).
16. Vabulas RM, Wagner H. Toll-like receptor-dependent activation of antigen presenting cells by Hsp60, Gp96 and Hsp70. In: Molecular Chaperones and Cell Signalling. B Henderson, AG Pockley (Eds). Cambridge University Press, Cambridge, UK 113-133 (2005).
17. Monaco JJ. A molecular model of MHC class-I-restricted antigen processing. Immunol. Today 13, 173-179 (1992).
18. Germain RN. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76, 287-299 (1994).
19. Udono H, Srivastava, PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J. Exp. Med. 178, 1391-1396 (1993).
20. 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, 395-425 (2002).
21. Srivastava PK. Therapeutic cancer vaccines. Curr. Opin. Immunol. 18, 201-205 (2006).
22. Binder RJ, Kelly JB 3rd, Vatner RE, Srivastava PK. Specific immunogenicity of heat shock protein Gp96 derives from chaperoned antigenic peptides and not from contaminating proteins. J. Immunol. 179, 7254-7261 (2007).
23. + T lymphocyte immune responses. J. Immunol. 177, 1017-1027 (2006).
24. Kunisawa J, Shastri N. Hsp90α chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 24, 523-534 (2006).
25. Enomoto Y, Bharti A, Khaleque AA et al. Enhanced immunogenicity of heat shock protein 70 peptide complexes from dendritic cell-tumor fusion cells. J. Immunol. 177, 5946-5955 (2006).
26. Noessner E, Gastpar R, Milani V et al. Tumor-derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. J. Immunol. 169, 5424-5432 (2002).
27. Berwin B, Hart JP, Rice S et al. Scavenger receptor-A mediates Gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J. 22, 6127-6136 (2003).
28. + T cell effector function. J. Immunol. 172, 6087-6092 (2004).
29. Singh-Jasuja H, Scherer HU, Hilf N et al. The heat shock protein Gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur. J. Immunol. 30, 2211-2215 (2000).
30. Facciponte JG, Wang XY, Subjeck JR. Hsp110 and Grp170, members of the Hsp70 superfamily, bind to scavenger receptor-A and scavenger receptor expressed by endothelial cells-I. Eur. J. Immunol. 37, 2268-2279 (2007).
31. Manjili MH, Park JE, Facciponte JG, Wang XY, Subjeck JR. Immunoadjuvant chaperone, GRP170, induces 'danger signals' upon interaction with dendritic cells. Immunol. Cell Biol. 84, 203-208 (2006).
32. Villadangos JA, Heath WR. Life cycle, migration and antigen presenting functions of spleen and lymph node dendritic cells: limitations of the Langerhans cells paradigm. Semin. Immunol. 17, 262-272 (2005).
33. Villadangos JA, Schnorrer P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7, 543-555 (2007).
34. Calderwood SK. Heat shock proteins in extracellular signaling. Methods 43, 167 (2007).
35. Basu S, Binder RJ, Ramalingam T, Srivastava PK. CD91 is a common receptor for heat shock proteins Gp96, Hsp90, Hsp70, and calreticulin. Immunity 14, 303-313 (2001).
36. Becker T, Hartl FU, Wieland F. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell. Biol. 158, 1277-1285 (2002).
37. Delneste Y, Magistrelli G, Gauchat J et al. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 17, 353-362 (2002).
38. Calderwood SK, Theriault J, Gray PJ, Gong J. Cell surface receptors for molecular chaperones. Methods 43, 199-206 (2007).
39. Theriault JR, Mambula SS, Sawamura T, Stevenson MA, Calderwood SK. Extracellular Hsp70 binding to surface receptors present on antigen presenting cells and endothelial/epithelial cells. FEBS Lett. 579, 1951-1960 (2005).
40. Theriault JR, Adachi H, Calderwood SK. Role of scavenger receptors in the binding and internalization of heat shock protein 70. J. Immunol. 177, 8604-8611 (2006).
41. Pluddemann A, Neyen C, Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods 43, 207-217 (2007).
42. + dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad. Sci. USA 103, 10729-10734 (2006).
43. Cheng CF, Fan J, Fedesco M et al. Transforming growth factor α (TGFα)-stimulated secretion of Hsp90α: using the receptor LRP-1/CD91 to promote human skin cell migration against a TGFβ-rich environment during wound healing. Mol. Cell. Biol. 28, 3344-3358 (2008).
44. Ramanayake T, Maniero GD, Morales H, Chida AS. Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. J. Immunol. 180, 3176-3182 (2008).
45. Millar DG, Garza KM Odermatt B et al. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat. Med. 9, 1469-1476 (2003).
46. Vabulas RM, Ahmad-Nejad P, da Costa C et al. 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 (2001).
47. Habich C, Kempe K, van der Zee R et al. Heat shock protein 60: specific binding of lipopolysaccharide. J. Immunol. 174, 1298-1305 (2005).
48. + T cells and dendritic cells. J. Immunol. 178, 1671-1679 (2007).
49. Wang Y, Kelly CG, Karttunen JT et al. CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15, 971-983 (2001).
50. Wang XY, Facciponte J, Chen X, Subjeck JR, Repasky EA. Scavenger receptor-A negatively regulates antitumor immunity. Cancer Res. 67, 4996-5002 (2007).
51. Kurotaki T, Tamura Y, Ueda G et al. Efficient cross-presentation by heat shock protein 90-peptide complex-loaded dendritic cells via an endosomal pathway. J. Immunol. 179, 1803-1813 (2007).
52. Burgdorf S, Kurts C. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20, 89-95 (2008).
53. Burgdorf S, Scholz C, Kautz A, Tampe R, Kurts C. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9, 558-566 (2008).
54. Bendz H, Ruhland SC, Pandya MJ et al. 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 (2007).
55. Tamura Y, Kutomi G, Oura J, Torigoe T, Sato N. Piloting of exogenous antigen into cross-presentation pathway. In: Heat Shock Proteins in Cancer. Calderwood SK, Sherman MY, Ciocca DR (Eds). Springer, Dordrecht, ND, USA 383-396 (2007).
56. Kunisawa J, Shastri N. The group II chaperonin TRiC protects proteolytic intermediates from degradation in the MHC class I antigen processing pathway. Mol. Cell 12, 565-576 (2003).
57. Castellino F, Boucher PE, Eichelberg K et al. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J. Exp. Med. 191, 1957-1964 (2000).
58. + memory T cells. Eur. J. Immunol. 35, 3163-3172 (2005).
59. SenGupta D, Norris PJ, Suscovich TJ et al. Heat shock protein-mediated cross-presentation of exogenous HIV antigen on HLA class I and class II. J. Immunol. 173, 1987-1993 (2004).
60. Asea A. Heat shock proteins and Toll-like receptors. Handb. Exp. Pharmacol. 111-127 (2008).
61. Ohashi PS, DeFranco AL. Making and breaking tolerance. Curr. Opin. Immunol. 14, 744-759 (2002).
62. Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol. Rev. 199, 227-250 (2004).
63. Ouaaz F, Arron J, Zheng Y, Choi Y, Beg AA. Dendritic cell development and survival require distinct NF-κB subunits. Immunity 16, 257-270 (2002).
64. Cominacini L, Pasini AF, Garbin U et al. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-κB through an increased production of intracellular reactive oxygen species. J. Biol. Chem. 275, 12633-12638 (2000).
65. Pan PY, Gu P, Li Q et al. Regulation of dendritic cell function by NK cells: mechanisms underlying the synergism in the combination therapy of IL-12 and 4-1BB activation. J. Immunol. 172, 4779-4789 (2004).
66. Gross C, Koelch W, DeMaio A, Arispe N, Multhoff G. Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J. Biol. Chem. 278(42), 41173-41181 (2003).
67. Elsner L, Muppala V, Gehrmann M et al. The heat shock protein Hsp70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J. Immunol. 179, 5523-5533 (2007).
68. 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 (2003).
69. Massa C, Melani C, Colombo MP. Chaperon and adjuvant activity of Hsp70: different natural killer requirement for cross-priming of chaperoned and bystander antigens. Cancer Res. 65, 7942-7949 (2005).
70. Belli F, Testori A, Rivoltini L et al. Vaccination of metastatic melanoma patients with autologous tumor-derived heat shock protein Gp96-peptide complexes: clinical and immunologic findings. J. Clin. Oncol. 20, 4169-4180 (2002).
71. Mazzaferro V, Coppa J, Carrabba MG et al. Vaccination with autologous tumor-derived heat-shock protein Gp96 after liver resection for metastatic colorectal cancer. Clin. Cancer Res. 9, 3235-3245 (2003).
72. Parmiani G, De Filippo A, Novellino L, Castelli C. Unique human tumor antigens: immunobiology and use in clinical trials. J. Immunol. 178, 1975-1979 (2007).
73. Tamura Y, Peng P, Liu K, Daou M, Srivastava PK. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 278, 117-120 (1997).
74. Yedavelli SP, Guo L, Daou ME et al. Preventive and therapeutic effect of tumor derived heat shock protein, Gp96, in an experimental prostate cancer model. Int. J. Mol. Med. 4, 243-248 (1999).
75. Testori A, Richards J, Whitman E et al. Phase III comparison of Vitespen, an autologous tumor-derived heat shock protein Gp96 peptide complex vaccine, with physician's choice of treatment for stage IV melanoma: the C-100-21 study group. J. Clin. Oncol. 26, 955-962 (2008).
76. Melief CJ, van der Burg SH. Immunotherapy of established (pre) malignant disease by synthetic long peptide vaccines. Nat. Rev. Cancer 8, 351-360 (2008).
77. Zeng Y, Graner MW, Katsanis E. Chaperone-rich cell lysates, immune activation and tumor vaccination. Cancer Immunol. Immunother. 55, 329-338 (2006).
78. Rivoltini L, Castelli C, Carrabba M et al. Human tumor-derived heat shock protein 96 mediates in vitro activation and in vivo expansion of melanoma- and colon carcinoma-specific T cells. J. Immunol. 171, 3467-3474 (2003).
79. Wang XY, Chen X, Manjili MH et al. Targeted immunotherapy using reconstituted chaperone complexes of heat shock protein 110 and melanoma-associated antigen Gp100. Cancer Res. 63, 2553-2560 (2003).
80. Suzue K, Young RA. Adjuvant-free Hsp70 fusion protein system elicits humoral and cellular immune responses to HIV-1 p24. J. Immunol. 156, 873-879 (1996).
81. Liu B, Ye D, Song X et al. A novel therapeutic fusion protein vaccine by two different families of heat shock proteins linked with HPV16 E7 generates potent antitumor immunity and antiangiogenesis. Vaccine 26, 1387-1396 (2008).
82. Susumu S, Nagata Y, Ito S et al. Cross-presentation of NY-ESO-1 cytotoxic T lymphocyte epitope fused to human heat shock cognate protein 70 by dendritic cells. Cancer Sci. 99, 107-112 (2008).
83. + T cell epitopes fused to heat shock cognate protein 70 (hsc70) can function to eradicate tumors. Cancer Sci. 99, 1008-1015 (2008).
84. Calderwood SK. Chaperones and slow death - a recipe for tumor immunotherapy. Trends Biotechnol 23, 57-59 (2005).
85. Daniels GA, Sanchez-Perez L, Diaz RM et al. A simple method to cure established tumors by inflammatory killing of normal cells. Nat. Biotechnol. 22, 1125-1132 (2004).
86. Melcher A, Murphy S, Vile R. Heat shock protein expression in target cells infected with low levels of replication-competent virus contributes to the immunogenicity of adenoviral vectors. Hum. Gene Ther. 10, 1431-1442 (1999).
87. Kottke T, Sanchez-Perez L, Diaz RM et al. Induction of Hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer. Cancer Res. 67, 11970-11979 (2007).
88. Multhoff G. Activation of natural killer cells by heat shock protein 70. Int. J. Hyperthermia 18, 576-585 (2002).
89. Multhoff G, Hightower LE. Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaperones 1, 167-176 (1996).
90. Krause SW, Gastpar R, Andreesen R et al. Treatment of colon and lung cancer patients with ex vivo heat shock protein 70-peptide- activated, autologous natural killer cells: a clinical Phase I trial. Clin. Cancer Res. 10, 3699-3707 (2004).
91. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Naure Medicine 10, 909-915 (2004).
92. Rosenberg SA. Shedding light on tumor immunotherapy of cancer. NEJM 350, 1461-1463 (2004).