High molecular weight stress proteins: Identification, cloning and utilisation in cancer immunotherapy

References

• Easton DP, Kaneko Y, Subjeck JR. The hsp110 and Grp1 70 stress proteins: Newly recognized relatives of the Hsp70s. Cell Stress Chaperones 2000;5:276–290
   PubMed Web of Science ®Google Scholar
• Subjeck JR, Shyy TT. Stress protein systems of mammalian cells. Am J Physiol 1986;250:C1–17
   PubMed Web of Science ®Google Scholar
• Lee AS. Mammalian stress response: Induction of the glucose-regulated protein family. Curr Opin Cell Biol 1992;4:267–273
   PubMedGoogle Scholar
• Shiu RP, Pouyssegur J, Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci USA 1977;74:3840–3844
   PubMed Web of Science ®Google Scholar
• Pouyssegur J, Shiu RP, Pastan I. Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell 1977;11:941–947
   PubMed Web of Science ®Google Scholar
• Sciandra JJ, Subjeck JR. The effects of glucose on protein synthesis and thermosensitivity in Chinese hamster ovary cells. J Biol Chem 1983;258:12091–12093
   PubMed Web of Science ®Google Scholar
• Sciandra JJ, Subjeck JR, Hughes CS. Induction of glucose-regulated proteins during anaerobic exposure and of heat-shock proteins after reoxygenation. Proc Natl Acad Sci USA 1984;81:4843–4847
   PubMed Web of Science ®Google Scholar
• Lin HY, Masso-Welch P, Di YP, Cai JW, Shen JW, Subjeck JR. The 170-kDa glucose-regulated stress protein is an endoplasmic reticulum protein that binds immunoglobulin. Mol Biol Cell 1993;4:1109–1119
   PubMed Web of Science ®Google Scholar
• Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999;13:1211–1233
   PubMed Web of Science ®Google Scholar
• Gething MJ, Sambrook J. Protein folding in the cell. Nature 1992;355:635533–635545
   Web of Science ®Google Scholar
• Craig EA, Gambill BD, Nelson RJ. Heat shock proteins: Molecular chaperones of protein biogenesis. Microbiol Rev 1993;57:402–414
   PubMedGoogle Scholar
• Hartl FU. Molecular chaperones in cellular protein folding. Nature 1996;381:6583571–6583579
   Web of Science ®Google Scholar
• Levinson W, Oppermann H, Jackson J. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim Biophys Acta 1980;606:170–180
   PubMed Web of Science ®Google Scholar
• Hightower LE. Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J Cell Physiol 1980;102:407–427
   PubMed Web of Science ®Google Scholar
• Subjeck JR, Sciandra JJ, Johnson RJ. Heat shock proteins and thermotolerance: A comparison of induction kinetics. Br J Radiol 1982;55: 579–584
   PubMed Web of Science ®Google Scholar
• Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N. Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 1982;42:2457–2461
   PubMed Web of Science ®Google Scholar
• Subjeck JR, Sciandra JJ, Chao CF, Johnson RJ. Heat shock proteins and biological response to hyperthermia. Br J Cancer 1982;45, Suppl 5:127–131
   Google Scholar
• Tomasovic SP, Steck PA, Heitzman D. Heat-stress proteins and thermal resistance in rat mammary tumor cells. Radiat Res 1983;95:399–413
   PubMed Web of Science ®Google Scholar
• Lee-Yoon D, Easton D, Murawski M, Burd R, Subjeck JR. Identification of a major subfamily of large hsp70-like proteins through the cloning of the mammalian 110-kDa heat shock protein. J Biol Chem 1995;270:15725–5733
   PubMed Web of Science ®Google Scholar
• Chen X, Easton D, Oh HJ, Lee-Yoon DS, Liu X, Subjeck J. The 170 kDa glucose regulated stress protein is a large Hsp70-, Hsp110-like protein of the endoplasmic reticulum. FEBS Lett 1996;380:68–72
   PubMed Web of Science ®Google Scholar
• Hylander BL, Chen X, Graf PC, Subjeck JR. The distribution and localization of hsp110 in brain. Brain Res 2000;869:49–55
   PubMed Web of Science ®Google Scholar
• Oh HJ, Chen X, Subjeck JR. Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 1997;272:31636–31640
   PubMed Web of Science ®Google Scholar
• Whelan SA, Hightower LE. Differential induction of glucose-regulated and heat shock proteins: Effects of pH and sulfhydryl-reducing agents on chicken embryo cells. J Cell Physiol 1985;125:251–258
   PubMed Web of Science ®Google Scholar
• Cai JW, Henderson BW, Shen JW, Subjeck JR. Induction of glucose regulated proteins during growth of a murine tumor. J Cell Physiol 1993;154:229–237
   PubMed Web of Science ®Google Scholar
• Kuwabara K, Matsumoto M, Ikeda J, Hori O, Ogawa S, Maeda Y, et al. Purification and characterization of a novel stress protein, the 150-kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J Biol Chem 1996;271:5025–5032
   PubMed Web of Science ®Google Scholar
• Shen J, Hughes C, Chao C, Cai J, Bartels C, Gessner T, et al. Coinduction of glucose-regulated proteins and doxorubicin resistance in Chinese hamster cells. Proc Natl Acad Sci USA 1987;84:3278–3282
   PubMed Web of Science ®Google Scholar
• Craven RA, Tyson JR, Stirling CJ. A novel subfamily of Hsp70s in the endoplasmic reticulum. Trends Cell Biol 1997;7:277–282
   PubMed Web of Science ®Google Scholar
• Koong AC, Chen EY, Lee AS, Brown JM, Giaccia AJ. Increased cytotoxicity of chronic hypoxic cells by molecular inhibition of GRP78 induction. Int J Radiat Oncol Biol Phys 1994;28:661–666
   PubMed Web of Science ®Google Scholar
• Tamatani M, Matsuyama T, Yamaguchi A, Mitsuda N, Tsukamoto Y, Taniguchi M, et al. ORP150 protects against hypoxia/ischemia-induced neuronal death. Nat Med 2001;7:317–323
   PubMed Web of Science ®Google Scholar
• Wang Y, Wu Z, Li D, Wang D, Wang X, Feng X, et al. Involvement of oxygen-regulated protein 150 in AMP-activated protein kinase-mediated alleviation of lipid-induced endoplasmic reticulum stress. J Biol Chem 2011;286:11119–111131
   PubMed Web of Science ®Google Scholar
• Hughes CS, Shen JW, Subjeck JR. Resistance to etoposide induced by three glucose-regulated stresses in Chinese hamster ovary cells. Cancer Res 1989;49:4452–4454
   PubMed Web of Science ®Google Scholar
• Mann MJ, Pereira ER, Liao N, Hendershot LM. UPR-induced resistance to etoposide is downstream of PERK and independent of changes in topoisomerase IIalpha levels. PLoS One 2012;7:e47931
   PubMed Web of Science ®Google Scholar
• Ye Z, Wang N, Xia P, Wang E, Liao J, Guo Q. Parecoxib suppresses CHOP and Foxo1 nuclear translocation, but increases GRP78 levels in a rat model of focal ischemia. Neurochem Res 2013;38:686–693
   PubMed Web of Science ®Google Scholar
• Liu X, Wang M, Chen H, Guo Y, Ma F, Shi F, et al. Hypothermia protects the brain from transient global ischemia/reperfusion by attenuating endoplasmic reticulum response-induced apoptosis through CHOP. PLoS One 2013;8:e53431
   PubMed Web of Science ®Google Scholar
• Melnick J, Dul JL, Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature 1994;370:373–375
   PubMed Web of Science ®Google Scholar
• Dierks T, Volkmer J, Schlenstedt G, Jung C, Sandholzer U, Zachmann K, et al. A microsomal ATP-binding protein involved in efficient protein transport into the mammalian endoplasmic reticulum. Embo J 1996;15:6931–6942
   PubMed Web of Science ®Google Scholar
• Spee P, Subjeck J, Neefjes J. Identification of novel peptide binding proteins in the endoplasmic reticulum: ERp72, calnexin, and grp170. Biochemistry 1999;38:10559–10566
   PubMed Web of Science ®Google Scholar
• Tyson JR, Stirling CJ. LHS1 and SIL1 provide a lumenal function that is essential for protein translocation into the endoplasmic reticulum. Embo J 2000;19:6440–6452
   PubMed Web of Science ®Google Scholar
• Craven RA, Egerton M, Stirling CJ. A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. Embo J 1996;15:2640–2650
   PubMed Web of Science ®Google Scholar
• Oh HJ, Easton D, Murawski M, Kaneko Y, Subjeck JR. The chaperoning activity of hsp110. Identification of functional domains by use of targeted deletions. J Biol Chem 1999;274:15712–15718
   PubMed Web of Science ®Google Scholar
• Park J, Easton DP, Chen X, MacDonald IJ, Wang XY, Subjeck JR. The chaperoning properties of mouse grp170, a member of the third family of hsp70 related proteins. Biochemistry 2003;42:14893–14902
   PubMed Web of Science ®Google Scholar
• Zhu X, Zhao X, Burkholder WF, Gragerov A, Ogata CM, Gottesman ME, et al. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996;272:1606–1614
   PubMed Web of Science ®Google Scholar
• Wang XY, Chen X, Manjili MH, Repasky E, Henderson R, Subjeck JR. Targeted immunotherapy using reconstituted chaperone complexes of heat shock protein 110 and melanoma-associated antigen gp100. Cancer Res 2003;63:2553–2560
   PubMed Web of Science ®Google Scholar
• Wang XY, Arnouk H, Chen X, Kazim L, Repasky EA, Subjeck JR. Extracellular targeting of endoplasmic reticulum chaperone glucose-regulated protein 170 enhances tumor immunity to a poorly immunogenic melanoma. J Immunol 2006;177:1543–1551
   PubMed Web of Science ®Google Scholar
• Wang XY, Sun X, Chen X, Facciponte J, Repasky EA, Kane J, et al. Superior antitumor response induced by large stress protein chaperoned protein antigen compared with peptide antigen. J Immunol 2010;184:6309–6319
   PubMed Web of Science ®Google Scholar
• Brodsky JL, Werner ED, Dubas ME, Goeckeler JL, Kruse KB, McCracken AA. The requirement for molecular chaperones during endoplasmic reticulum-associated protein degradation demonstrates that protein export and import are mechanistically distinct. J Biol Chem 1999;274:3453–3460
   PubMed Web of Science ®Google Scholar
• Wang XY, Chen X, Oh HJ, Repasky E, Kazim L, Subjeck J. Characterization of native interaction of hsp110 with hsp25 and hsc70. FEBS Lett 2000;465:98–102
   PubMed Web of Science ®Google Scholar
• Ishihara K, Yasuda K, Hatayama T. Molecular cloning, expression and localization of human 105 kDa heat shock protein, hsp105. Biochim Biophys Acta 1999;1444:138–142
   PubMedGoogle Scholar
• Yam AY, Albanese V, Lin HT, Frydman J. Hsp110 cooperates with different cytosolic Hsp70 systems in a pathway for de novo folding. J Biol Chem 2005;280:41252–41261
   PubMed Web of Science ®Google Scholar
• Shaner L, Wegele H, Buchner J, Morano KA. The yeast Hsp110 Sse1 functionally interacts with the Hsp70 chaperones Ssa and Ssb. J Biol Chem 2005;280:41262–41269
   PubMed Web of Science ®Google Scholar
• Shorter J. The mammalian disaggregase machinery: Hsp110 synergizes with Hsp70 and Hsp40 to catalyze protein disaggregation and reactivation in a cell-free system. PLoS One 2011;6:e26319
   PubMed Web of Science ®Google Scholar
• Rampelt H, Kirstein-Miles J, Nillegoda NB, Chi K, Scholz SR, Morimoto RI, et al. Metazoan Hsp70 machines use Hsp110 to power protein disaggregation. Embo J 2012;31:4221–4235
   PubMed Web of Science ®Google Scholar
• Yamagishi N, Yokota M, Yasuda K, Saito Y, Nagata K, Hatayama T. Characterization of stress sensitivity and chaperone activity of Hsp105 in mammalian cells. Biochem Biophys Res Commun 2011;409:90–95
   PubMed Web of Science ®Google Scholar
• Yamagishi N, Goto K, Nakagawa S, Saito Y, Hatayama T. Hsp105 reduces the protein aggregation and cytotoxicity by expanded-polyglutamine proteins through the induction of Hsp70. Exp Cell Res 2010;316:2424–2433
   PubMed Web of Science ®Google Scholar
• Saxena A, Banasavadi-Siddegowda YK, Fan Y, Bhattacharya S, Roy G, Giovannucci DR, et al. Human heat shock protein 105/110 kDa (Hsp105/110) regulates biogenesis and quality control of misfolded cystic fibrosis transmembrane conductance regulator at multiple levels. J Biol Chem 2012;287:19158–19170
   PubMed Web of Science ®Google Scholar
• Raviol H, Sadlish H, Rodriguez F, Mayer MP, Bukau B. Chaperone network in the yeast cytosol: Hsp110 is revealed as an Hsp70 nucleotide exchange factor. Embo J 2006;25:2510–2518
   PubMed Web of Science ®Google Scholar
• Dragovic Z, Broadley SA, Shomura Y, Bracher A, Hartl FU. Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. Embo J 2006;25:2519–2528
   PubMed Web of Science ®Google Scholar
• Andreasson C, Fiaux J, Rampelt H, Druffel-Augustin S, Bukau B. Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc Natl Acad Sci USA 2008;105:16519–16524
   PubMed Web of Science ®Google Scholar
• Polier S, Dragovic Z, Hartl FU, Bracher A. Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 2008;133:1068–1079
   PubMed Web of Science ®Google Scholar
• Weitzmann A, Volkmer J, Zimmermann R. The nucleotide exchange factor activity of Grp170 may explain the non-lethal phenotype of loss of Sil1 function in man and mouse. FEBS Lett 2006;580:5237–5240
   PubMed Web of Science ®Google Scholar
• de Keyzer J, Steel GJ, Hale SJ, Humphries D, Stirling CJ. Nucleotide binding by Lhs1p is essential for its nucleotide exchange activity and for function in vivo. J Biol Chem 2009;284:31564–31571
   PubMed Web of Science ®Google Scholar
• Andreasson C, Rampelt H, Fiaux J, Druffel-Augustin S, Bukau B. The endoplasmic reticulum Grp170 acts as a nucleotide exchange factor of Hsp70 via a mechanism similar to that of the cytosolic Hsp110. J Biol Chem 2010;285:12445–12453
   PubMed Web of Science ®Google Scholar
• Xu X, Sarbeng EB, Vorvis C, Kumar DP, Zhou L, Liu Q. Unique peptide substrate binding properties of 110-kDa heat-shock protein (Hsp110) determine its distinct chaperone activity. J Biol Chem 2012;287:5661–5672
   PubMed Web of Science ®Google Scholar
• Mandal AK, Gibney PA, Nillegoda NB, Theodoraki MA, Caplan AJ, Morano KA. Hsp110 chaperones control client fate determination in the hsp70-Hsp90 chaperone system. Mol Biol Cell 2010;21:1439–1448
   PubMed Web of Science ®Google Scholar
• Henics T, Nagy E, Oh HJ, Csermely P, von Gabain A, Subjeck JR. Mammalian Hsp70 and Hsp110 proteins bind to RNA motifs involved in mRNA stability. J Biol Chem 1999;274:17318–17324
   PubMed Web of Science ®Google Scholar
• Zuo D, Yu X, Guo C, Yi H, Chen X, Conrad DH, et al. Molecular chaperoning by glucose-regulated protein 170 in the extracellular milieu promotes macrophage-mediated pathogen sensing and innate immunity. Faseb J 2012;26:1493–1505
   PubMed Web of Science ®Google Scholar
• Srivastava PK, DeLeo AB, Old LJ. Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc Natl Acad Sci USA 1986;83:3407–3411
   PubMed Web of Science ®Google Scholar
• Ullrich SJ, Robinson EA, Law LW, Willingham M, Appella E. A mouse tumor-specific transplantation antigen is a heat shock-related protein. Proc Natl Acad Sci USA 1986;83:3121–3125
   PubMed Web of Science ®Google Scholar
• Udono H, Srivastava PK. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med 1993;178:1391–1396
   PubMed Web of Science ®Google Scholar
• Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med 1995;182:885–889
   PubMed Web of Science ®Google Scholar
• Nieland TJ, Tan MC, Monne-van Muijen M, Koning F, Kruisbeek AM, van Bleek GM. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein GP96/GRP94. Proc Natl Acad Sci USA 1996;93:6135–6139
   PubMed Web of Science ®Google Scholar
• Ishii T, Udono H, Yamano T, Ohta H, Uenaka A, Ono T, et al. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J Immunol 1999;162:1303–1309
   PubMed Web of Science ®Google Scholar
• Castelli C, Ciupitu AM, Rini F, Rivoltini L, Mazzocchi A, Kiessling R, et al. Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res 2001;61:222–227
   PubMed Web of Science ®Google Scholar
• Rivoltini L, Castelli C, Carrabba M, Mazzaferro V, Pilla L, Huber V, 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 2003;171:3467–3474
   PubMed Web of Science ®Google Scholar
• Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu Rev Immunol 2002;20:395–425
   PubMed Web of Science ®Google Scholar
• Baker-LePain JC, Reed RC, Nicchitta CV. ISO: A critical evaluation of the role of peptides in heat shock/chaperone protein-mediated tumor rejection. Curr Opin Immunol 2003;15:89–94
   PubMed Web of Science ®Google Scholar
• Nicchitta CV, Carrick DM, Baker-Lepain JC. The messenger and the message: gp96 (GRP94)-peptide interactions in cellular immunity. Cell Stress Chaperones 2004;9(4):325–331
   PubMed Web of Science ®Google Scholar
• Tamura Y, Peng P, Liu K, Daou M, Srivastava PK. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 1997;278:117–120
   PubMed Web of Science ®Google Scholar
• Vanaja DK, Grossmann ME, Celis E, Young CY. Tumor prevention and antitumor immunity with heat shock protein 70 induced by 15-deoxy-delta12,14-prostaglandin J2 in transgenic adenocarcinoma of mouse prostate cells. Cancer Res 2000;60:4714–4718
   PubMed Web of Science ®Google Scholar
• Graner M, Raymond A, Romney D, He L, Whitesell L, Katsanis E. Immunoprotective activities of multiple chaperone proteins isolated from murine B-cell leukemia/lymphoma. Clin Cancer Res 2000;6:909–915
   PubMed Web of Science ®Google Scholar
• Wang XY, Kazim L, Repasky EA, Subjeck JR. 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 2001;166:490–497
   PubMed Web of Science ®Google Scholar
• Wang XY, Kazim L, Repasky EA, Subjeck JR. Immunization with tumor-derived ER chaperone grp170 elicits tumor-specific CD8+ T-cell responses and reduces pulmonary metastatic disease. Int J Cancer 2003;105:226–231
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Calderwood SK. Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 2005;10:86–103
   PubMed Web of Science ®Google Scholar
• Calderwood SK, Khaleque MA, Sawyer DB, Ciocca DR. Heat shock proteins in cancer: Chaperones of tumorigenesis. Trends Biochem Sci 2006;31:164–172
   PubMed Web of Science ®Google Scholar
• Fu Y, Lee AS. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol Ther 2006;5:741–744
   PubMed Web of Science ®Google Scholar
• Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013;32:805–818
   PubMed Web of Science ®Google Scholar
• Arnouk H, Zynda ER, Wang XY, Hylander BL, Manjili MH, Repasky EA, et al. Tumour secreted grp170 chaperones full-length protein substrates and induces an adaptive anti-tumour immune response in vivo. Int J Hyperthermia 2010;26:366–375
   PubMed Web of Science ®Google Scholar
• Kunisawa J, Shastri N. The group II chaperonin TRiC protects proteolytic intermediates from degradation in the MHC class I antigen processing pathway. Molecular Cell 2003;12:565–576
   PubMed Web of Science ®Google Scholar
• Kunisawa J, Shastri N. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 2006;24:523–534
   PubMed Web of Science ®Google Scholar
• Mazzaferro V, Coppa J, Carrabba MG, Rivoltini L, Schiavo M, Regalia E, et al. Vaccination with autologous tumor-derived heat-shock protein gp96 after liver resection for metastatic colorectal cancer. Clin Cancer Res 2003;9:3235–3245
   PubMed Web of Science ®Google Scholar
• Pilla L, Patuzzo R, Rivoltini L, Maio M, Pennacchioli E, Lamaj E, et al. A phase II trial of vaccination with autologous, tumor-derived heat-shock protein peptide complexes Gp96, in combination with GM-CSF and interferon-alpha in metastatic melanoma patients. Cancer Immunol Immunother 2006;55:958–968
   PubMed Web of Science ®Google Scholar
• Testori A, Richards J, Whitman E, Mann GB, Lutzky J, Camacho L, 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 2008;26:955–962
   PubMed Web of Science ®Google Scholar
• Younes A. A phase II study of heat shock protein-peptide complex-96 vaccine therapy in patients with indolent non-Hodgkin’s lymphoma. Clin Lymphoma 2003;4:183–185
   PubMedGoogle Scholar
• Jonasch E, Wood C, Tamboli P, Pagliaro LC, Tu SM, Kim J, et al. Vaccination of metastatic renal cell carcinoma patients with autologous tumour-derived vitespen vaccine: Clinical findings. Br J Cancer 2008;98:1336–1341
   PubMed Web of Science ®Google Scholar
• Wood C, Srivastava P, Bukowski R, Lacombe L, Gorelov AI, Gorelov S, et al. An adjuvant autologous therapeutic vaccine (HSPPC-96; vitespen) versus observation alone for patients at high risk of recurrence after nephrectomy for renal cell carcinoma: A multicentre, open-label, randomised phase III trial. Lancet 2008;372(9633):145–154
   PubMed Web of Science ®Google Scholar
• Oki Y, Younes A. Heat shock protein-based cancer vaccines. Expert Rev Vaccines 2004;3:403–411
   PubMedGoogle Scholar
• Gordon NF, Clark BL. The challenges of bringing autologous HSP-based vaccines to commercial reality. Methods 2004;32:63–69
   PubMed Web of Science ®Google Scholar
• Belli F, Testori A, Rivoltini L, Maio M, Andreola G, Sertoli MR, et al. Vaccination of metastatic melanoma patients with autologous tumor-derived heat shock protein gp96-peptide complexes: Clinical and immunologic findings. J Clin Oncol 2002;20:4169–4180
   PubMed Web of Science ®Google Scholar
• Manjili MH, Henderson R, Wang XY, Chen X, Li Y, Repasky E, et al. Development of a recombinant HSP110-HER-2/neu vaccine using the chaperoning properties of HSP110. Cancer Res 2002;62:1737–1742
   PubMed Web of Science ®Google Scholar
• Manjili MH, Wang XY, Chen X, Martin T, Repasky EA, Henderson R, et al. HSP110-HER2/neu chaperone complex vaccine induces protective immunity against spontaneous mammary tumors in HER-2/neu transgenic mice. J Immunol 2003;171:4054–4061
   PubMed Web of Science ®Google Scholar
• Park JE, Facciponte J, Chen X, MacDonald I, Repasky EA, Manjili MH, et al. Chaperoning function of stress protein grp170, a member of the hsp70 superfamily, is responsible for its immunoadjuvant activity. Cancer Res 2006;66:1161–1168
   PubMed Web of Science ®Google Scholar
• Kim H, Sun X, Subjeck J, Wang X-Y. Evaluation of renal cell carcinoma vaccines targeting carbonic anhydrase IX using heat shock protein 110. Cancer Immunology, Immunotherapy 2007;56:1097–1105
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang XY, Subjeck JR, Shrikant PA, Kim HL. Temsirolimus, an mTOR inhibitor, enhances anti-tumour effects of heat shock protein cancer vaccines. Br J Cancer 2011;104:643–652
   PubMed Web of Science ®Google Scholar
• Huo W, Ye J, Liu R, Chen J, Li Q. Vaccination with a chaperone complex based on PSCA and GRP170 adjuvant enhances the CTL response and inhibits the tumor growth in mice. Vaccine 2010;28:6333–6337
   PubMed Web of Science ®Google Scholar
• Yuan B, Xian R, Wu X, Jing J, Chen K, Liu G, et al. Endoplasmic reticulum chaperone glucose regulated protein 170-Pokemon complexes elicit a robust antitumor immune response in vivo. Immunobiology 2012;217:738–742
   PubMed Web of Science ®Google Scholar
• Wang XY, Facciponte JG, Subjeck JR. Molecular chaperones and cancer immunotherapy. Handb Exp Pharmacol 2006;172:305–329
   Google Scholar
• Murshid A, Gong J, Calderwood SK. Heat-shock proteins in cancer vaccines: Agents of antigen cross-presentation. Expert Rev Vaccines 2008;7:1019–1030
   PubMed Web of Science ®Google Scholar
• Murshid A, Gong J, Calderwood SK. The role of heat shock proteins in antigen cross presentation. Frontiers Immunol 2012;3:63
   PubMed Web of Science ®Google Scholar
• Arnold-Schild D, Hanau D, Spehner D, Schmid C, Rammensee HG, de la Salle H, et al. Cutting edge: Receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J Immunol 1999;162:3757–3760
   PubMed Web of Science ®Google Scholar
• Wassenberg JJ, Dezfulian C, Nicchitta CV. Receptor mediated and fluid phase pathways for internalization of the ER Hsp90 chaperone GRP94 in murine macrophages. J Cell Sci 1999;112:2167–2175
   PubMed Web of Science ®Google Scholar
• Castellino F, Boucher PE, Eichelberg K, Mayhew M, Rothman JE, Houghton AN, 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 2000;191:1957–1964
   PubMed Web of Science ®Google Scholar
• Singh-Jasuja H, Toes RE, Spee P, Munz C, Hilf N, Schoenberger SP, et al. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. J Exp Med 2000;191:1965–1974
   PubMed Web of Science ®Google Scholar
• Binder RJ, Han DK, Srivastava PK. CD91: A receptor for heat shock protein gp96. Nat Immunol 2000;1:151–155
   PubMed Web of Science ®Google Scholar
• Basu S, Binder RJ, Ramalingam T, Srivastava PK. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 2001;14:303–313
   PubMed Web of Science ®Google Scholar
• Delneste Y, Magistrelli G, Gauchat J, Haeuw J, Aubry J, Nakamura K, et al. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 2002;17:353–362
   PubMed Web of Science ®Google Scholar
• Berwin B, Hart JP, Rice S, Gass C, Pizzo SV, Post SR, et al. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. Embo J. 2003;22:6127–6136
   PubMed Web of Science ®Google Scholar
• Berwin B, Delneste Y, Lovingood RV, Post SR, Pizzo SV. SREC-I, a type F scavenger receptor, is an endocytic receptor for calreticulin. J Biol Chem 2004;279:51250–51257
   PubMed Web of Science ®Google Scholar
• Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 2000;6:435–442
   PubMed Web of Science ®Google Scholar
• Kuppner MC, Gastpar R, Gelwer S, Nossner E, Ochmann O, Scharner A, et al. The role of heat shock protein (hsp70) in dendritic cell maturation: hsp70 induces the maturation of immature dendritic cells but reduces DC differentiation from monocyte precursors. Eur J Immunol 2001;31:1602–1609
   PubMed Web of Science ®Google Scholar
• Singh-Jasuja H, Scherer HU, Hilf N, Arnold-Schild D, Rammensee HG, Toes RE, et al. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor. Eur J Immunol 2000;30:2211–2215
   PubMed Web of Science ®Google Scholar
• Wang Y, Kelly CG, Singh M, McGowan EG, Carrara AS, Bergmeier LA, et al. Stimulation of Th1-polarizing cytokines, C-C chemokines, maturation of dendritic cells, and adjuvant function by the peptide binding fragment of heat shock protein 70. J Immunol 2002;169:2422–2429
   PubMed Web of Science ®Google Scholar
• Theriault JR, Adachi H, Calderwood SK. Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 2006;177:8604–8611
   PubMed Web of Science ®Google Scholar
• Tsan MF, Gao B. Heat shock proteins and immune system. J Leukoc Biol 2009;85:905–910
   PubMed Web of Science ®Google Scholar
• Calderwood SK, Mambula SS, Gray PJ. Jr. Extracellular heat shock proteins in cell signaling and immunity. Ann N Y Acad Sci 2007;1113:28–39
   PubMed Web of Science ®Google Scholar
• Henderson B, Calderwood SK, Coates AR, Cohen I, van Eden W, Lehner T, et al. Caught with their PAMPs down? The extracellular signalling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 2010;15:123–141
   PubMed Web of Science ®Google Scholar
• Chen T, Guo J, Han C, Yang M, Cao X. 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. J Immunol 2009;182:1449–1459
   PubMed Web of Science ®Google Scholar
• Gong J, Zhu B, Murshid A, Adachi H, Song B, Lee A, et al. T cell activation by heat shock protein 70 vaccine requires TLR signaling and scavenger receptor expressed by endothelial cells-1. J Immunol 2009;183:3092–3098
   PubMed Web of Science ®Google Scholar
• Manjili MH, Park J, Facciponte JG, Subjeck JR. HSP110 induces ‘danger signals’ upon interaction with antigen presenting cells and mouse mammary carcinoma. Immunobiology 2005;210:295–303
   PubMed Web of Science ®Google Scholar
• Manjili MH, Park JE, Facciponte JG, Wang XY, Subjeck JR. Immunoadjuvant chaperone, GRP170, induces ‘danger signals’ upon interaction with dendritic cells. Immunol Cell Biol 2006;84:203–208
   PubMed Web of Science ®Google Scholar
• Wang XY, Li Y, Manjili MH, Repasky EA, Pardoll DM, Subjeck JR. Hsp110 over-expression increases the immunogenicity of the murine CT26 colon tumor. Cancer Immunol Immunother 2002;51:311–319
   PubMed Web of Science ®Google Scholar
• Muchemwa FC, Nakatsura T, Fukushima S, Nishimura Y, Kageshita T, Ihn H. Differential expression of heat shock protein 105 in melanoma and melanocytic naevi. Melanoma Res 2008;18:166–171
   PubMed Web of Science ®Google Scholar
• Oda T, Morii E, Inoue M, Ikeda J, Aozasa K, Okumura M. Prognostic significance of heat shock protein 105 in lung adenocarcinoma. Mol Med Rep 2009;2:603–607
   PubMed Web of Science ®Google Scholar
• Zappasodi R, Bongarzone I, Ghedini GC, Castagnoli L, Cabras AD, Messina A, et al. Serological identification of HSP105 as a novel non-Hodgkin lymphoma therapeutic target. Blood 2011;118:4421–4430
   PubMed Web of Science ®Google Scholar
• Miyazaki M, Nakatsura T, Yokomine K, Senju S, Monji M, Hosaka S, et al. DNA vaccination of HSP105 leads to tumor rejection of colorectal cancer and melanoma in mice through activation of both CD4 T cells and CD8 T cells. Cancer Sci 2005;96:695–705
   PubMed Web of Science ®Google Scholar
• Gao P, Sun X, Chen X, Subjeck J, Wang XY. Secretion of stress protein grp170 promotes immune-mediated inhibition of murine prostate tumor. Cancer Immunol Immunother 2009;58:1319–1328
   PubMed Web of Science ®Google Scholar
• Gao P, Sun X, Chen X, Wang Y, Foster BA, Subjeck J, et al. Secretable chaperone Grp170 enhances therapeutic activity of a novel tumor suppressor, mda-7/IL-24. Cancer Res 2008;68:3890–3898
   PubMed Web of Science ®Google Scholar
• Dash R, Bhutia SK, Azab B, Su ZZ, Quinn BA, Kegelmen TP, et al. mda-7/IL-24: A unique member of the IL-10 gene family promoting cancer-targeted toxicity. Cytokine Growth Factor Rev 2010;21:381–391
   PubMed Web of Science ®Google Scholar
• Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: Integrating immunity’s roles in cancer suppression and promotion. Science 2011;331:1565–1570
   PubMed Web of Science ®Google Scholar
• Quezada SA, Peggs KS, Simpson TR, Allison JP. Shifting the equilibrium in cancer immunoediting: From tumor tolerance to eradication. Immunol Rev 2011;241:104–118
   PubMed Web of Science ®Google Scholar
• Yu X, Guo C, Yi H, Qian J, Fisher PB, Subjeck JR, et al. A multifunctional chimeric chaperone serves as a novel immune modulator inducing therapeutic antitumor immunity. Cancer Res 2013;73:2093–103
   PubMed Web of Science ®Google Scholar
• Murthy KGK, Deb A, Goonesekera S, SzabÃ3 C, Salzman AL. Identification of conserved domains in Salmonella muenchen flagellin that are essential for its ability to activate TLR5 and to induce an inflammatory response in vitro. J Biol Chem 2004;279:5667–5675
   PubMed Web of Science ®Google Scholar
• van Eden W, van der Zee R, Prakken B. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat Rev Immunol 2005;5:318–330
   PubMed Web of Science ®Google Scholar
• de Kleer I, Vercoulen Y, Klein M, Meerding J, Albani S, van der Zee R, et al. CD30 discriminates heat shock protein 60-induced FOXP3+ CD4+ T cells with a regulatory phenotype. J Immunol 2010;185:2071–2079
   PubMed Web of Science ®Google Scholar
• van Herwijnen MJ, Wieten L, van der Zee R, van Kooten PJ, Wagenaar-Hilbers JP, Hoek A, et al. Regulatory T cells that recognize a ubiquitous stress-inducible self-antigen are long-lived suppressors of autoimmune arthritis. Proc Natl Acad Sci USA. 2012;109:14134–14139
   PubMed Web of Science ®Google Scholar
• Keijzer C, Wieten L, van Herwijnen M, van der Zee R, Van Eden W, Broere F. Heat shock proteins are therapeutic targets in autoimmune diseases and other chronic inflammatory conditions. Expert opinion on therapeutic targets. 2012;16:849–857
   PubMed Web of Science ®Google Scholar
• Murshid A, Gong J, Calderwood SK. Heat shock protein 90 mediates efficient antigen cross presentation through the scavenger receptor expressed by endothelial cells-I. J Immunol 2010;185:2903–2917
   PubMed Web of Science ®Google Scholar
• 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 2007;37:2268–2279
   PubMed Web of Science ®Google Scholar
• Wang XY, Facciponte J, Chen X, Subjeck JR, Repasky EA. Scavenger receptor-A negatively regulates antitumor immunity. Cancer Res 2007;67:4996–5002
   PubMed Web of Science ®Google Scholar
• Qian J, Yi H, Guo C, Yu X, Zuo D, Chen X, et al. CD204 suppresses large heat shock protein-facilitated priming of tumor antigen gp100-specific T cells and chaperone vaccine activity against mouse melanoma. J Immunol 2011;187:2905–2914
   PubMed Web of Science ®Google Scholar
• Yi H, Yu X, Gao P, Wang Y, Baek SH, Chen X, et al. Pattern recognition scavenger receptor SRA/CD204 down-regulates Toll-like receptor 4 signaling-dependent CD8 T-cell activation. Blood 2009;113:5819–5828
   PubMed Web of Science ®Google Scholar
• Yi H, Zuo D, Yu X, Hu F, Manjili MH, Chen Z, et al. Suppression of antigen-specific CD4(+) T cell activation by SRA/CD204 through reducing the immunostimulatory capability of antigen-presenting cell. J Mol Med 2012;90:413–426
   PubMed Web of Science ®Google Scholar
• Zuo D, Yu X, Guo C, Wang H, Qian J, Yi H, et al. Scavenger receptor a restrains T-cell activation and protects against concanavalin A-induced hepatic injury. Hepatology 2013;57:228–238
   PubMed Web of Science ®Google Scholar
• Guo C, Yi H, Yu X, Hu F, Zuo D, Subjeck JR, et al. Absence of scavenger receptor A promotes dendritic cell-mediated cross-presentation of cell-associated antigen and antitumor immune response. Immunol Cell Biol 2012;90:101–108
   PubMed Web of Science ®Google Scholar
• Yu X, Yi H, Guo C, Zuo D, Wang Y, Kim HL, et al. Pattern pecognition scavenger receptor CD204 attenuates Toll-like receptor 4-induced NF-{kappa}B activation by directly inhibiting ubiquitination of tumor necrosis factor (TNF) receptor-associated factor 6. J Biol Chem 2011;286:18795–18806
   PubMed Web of Science ®Google Scholar
• Andreakos E, Williams RO, Wales J, Foxwell BM, Feldmann M. Activation of NF-kappaB by the intracellular expression of NF-kappaB-inducing kinase acts as a powerful vaccine adjuvant. Proc Natl Acad Sci 2006;103:14459–14464
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050–1059
   PubMed Web of Science ®Google Scholar
• Yi H, Guo C, Yu X, Gao P, Qian J, Zuo D, et al. Targeting the immunoregulator SRA/CD204 potentiates specific dendritic cell vaccine-induced T cell response and antitumor immunity. Cancer Res 2011;71:6611–6620
   PubMed Web of Science ®Google Scholar
• Guo C, Yi H, Yu X, Zuo D, Qian J, Yang G, et al. In situ vaccination with CD204 gene-silenced dendritic cell, not unmodified dendritic cell, enhances radiation therapy of prostate cancer. Mol Cancer Ther 2012;11:2331–2341
   PubMed Web of Science ®Google Scholar
• Matsutake T, Sawamura T, Srivastava PK. High efficiency CD91- and LOX-1-mediated re-presentation of gp96-chaperoned peptides by MHC II molecules. Cancer Immun 2010;10:7
   PubMedGoogle Scholar