Could mycobacterial Hsp70-containing fusion protein lead the way to an affordable therapeutic cancer vaccine?

References

• Blank CU . The perspective of immunotherapy: new molecules and new mechanisms of action in immune modulation. Curr Opin Oncol 2014;26(2):204-14
   PubMed Web of Science ®Google Scholar
• Snell LM , Lin GH , McPherson AJ , et al. T-cell intrinsic effects of GITR and 4-1BB during viral infection and cancer immunotherapy. Immunol Rev 2011;244(1):197-217
   PubMedGoogle Scholar
• Song Y , Margolles-Clark E , Bayer A , Buchwald P . Small-molecule modulators of the OX40-OX40L costimulatory protein-protein interaction. Br J Pharmacol 2014;171(21):4955-69
   PubMed Web of Science ®Google Scholar
• Vaccines: A Report on the Prevention and Treatment of Diseases with Vaccines. 2013 Report. Pharmaceutical Research and Manufacturers of America. 2013. Available from: http://www.phrma.org/sites/default/files/pdf/Vaccines_2013.pdf [Accessed 14 July 2014]
   Google Scholar
• Rammensee HG , Singh-Jasuja H . HLA ligandome tumor antigen discovery for personalized vaccine approach. Expert Rev Vaccines 2013;12(10):1211-17
   PubMed Web of Science ®Google Scholar
• Bijker MS , van den Eeden SJ , Franken KL , et al. Superior induction of anti-tumor CTL immunity by extended peptide vaccines involves prolonged, DC-focused antigen presentation. Eur J Immunol 2008;38:1033-42
   PubMed Web of Science ®Google Scholar
• Melief CJ , van der Burg SH . Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat Rev Cancer 2008;8:351-60
   PubMed Web of Science ®Google Scholar
• Banchereau J , Steinman RM . Dendritic cells and the control of immunity. Nature 1998;392:245-52
   PubMed Web of Science ®Google Scholar
• Kalinski P , Muthuswamy R , Urban J . Dendritic cells in cancer immunotherapy: vaccines and combination immunotherapies. Expert Rev Vaccines 2013;12(3):285-95
   PubMed Web of Science ®Google Scholar
• Palucka K , Banchereau J . Dendritic-cell-based therapeutic cancer vaccines. Immunity 2013;39(1):38-48
   PubMed Web of Science ®Google Scholar
• Jacobs JJ , Snackey C , Geldof AA , et al. Inefficacy of therapeutic cancer vaccines and proposed improvements. Casus of prostate cancer. Anticancer Res 2014;34(6):2689-700
   PubMed Web of Science ®Google Scholar
• Palena C , Schlom J . Vaccines against human carcinomas: strategies to improve antitumor immune responses. J Biomed Biotechnol 2010;2010:380697
   PubMedGoogle Scholar
• Hadrup S , Donia M , Thor Straten P . Effector CD4 and CD8 T cells and their role in the tumor microenvironment. Cancer Microenviron 2013;6(2):123-33
   PubMedGoogle Scholar
• Dobrzanski MJ . Expanding roles for CD4 T cells and their subpopulations in tumor immunity and therapy. Front Oncol 2013;3:63
   PubMedGoogle Scholar
• Rivoltini L , Canese P , Huber V , et al. Escape strategies and reasons for failure in the interaction between tumour cells and the immune system: how can we tilt the balance towards immune-mediated cancer control? Expert Opin Biol Ther 2003;5:463-76
   Web of Science ®Google Scholar
• Kono K , Mizukami Y , Daigo Y , et al. Vaccination with multiple peptides derived from novel cancer-testis antigens can induce specific T-cell responses and clinical responses in advanced esophageal cancer. Cancer Sci 2009;100:1502-9
   PubMed Web of Science ®Google Scholar
• Bae J , Smith R , Daley J , et al. Myeloma-specific multiple peptides able to generate cytotoxic T lymphocytes: a potential therapeutic application in multiple myeloma and other plasma cell disorders. Clin Cancer Res 2012;18:4850-60
   PubMed Web of Science ®Google Scholar
• Suzuki H , Fukuhara M , Yamaura T , et al. Multiple therapeutic peptide vaccines consisting of combined novel cancer testis antigens and anti-angiogenic peptides for patients with non-small cell lung cancer. J Transl Med 2013;11(1):97
   PubMed Web of Science ®Google Scholar
• Walter S , Weinschenk T , Stenzl A , et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med 2012;18(8):1254-61
   PubMed Web of Science ®Google Scholar
• Monjazeb AM , Zamora AE , Grossenbacher SK , et al. Immunoediting and antigen loss: overcoming the Achilles’ heel of immunotherapy with antigen non-specific therapies. Front Oncol 2013;3:197
   PubMedGoogle Scholar
• Baskar S , Kobrin CB , Kwak LW . Autologous lymphoma vaccines induce human T cell responses against multiple, unique epitopes. J Clin Invest 2004;113(10):1498-510
   PubMed Web of Science ®Google Scholar
• Lennerz V , Fatho M , Gentilini C , et al. The response of autologous T cells to a human melanoma is dominated by mutated neoantigens. Proc Natl Acad Sci USA 2005;102:16013-18
   PubMed Web of Science ®Google Scholar
• Dubensky TW Jr , Reed SG . Adjuvants for cancer vaccines. Semin Immunol 2010;22:155-61
   PubMed Web of Science ®Google Scholar
• Tefit JN , Serra V . Outlining novel cellular adjuvant products for therapeutic vaccines against cancer. Expert Rev Vaccines 2011;10(8):1207-20
   PubMed Web of Science ®Google Scholar
• Hailemichael Y , Overwijk WW . Peptide-based anticancer vaccines: the making and unmaking of a T-cell graveyard. Oncoimmunology 2013;2(7):e24743
   PubMed Web of Science ®Google Scholar
• Thayer AM . Making peptides at large scale. Chem Eng News 2011;89(22):21-5
   Web of Science ®Google Scholar
• Strasser EF , Eckstein R . Optimization of leukocyte collection and monocyte isolation for dendritic cell culture. Transfus Med Rev 2010;24(2):130-9
   PubMed Web of Science ®Google Scholar
• Kudrin A . Overview of cancer vaccines: considerations for development. Hum Vaccin Immunother 2012;8(9):1335-53
   PubMed Web of Science ®Google Scholar
• Smith BD , Smith GL , Hurria A , et al. Future of cancer incidence in the United States: burdens upon an aging, changing nation. J Clin Oncol 2009;27(17):2758-65
   PubMed Web of Science ®Google Scholar
• Mariotto AB , Yabroff KR , Shao Y , et al. Projections of the cost of cancer care in the United States: 2010-2020. J Natl Cancer Inst 2011;103(2):117-28
   PubMed Web of Science ®Google Scholar
• Howard P . Sure, we’ll (eventually) beat cancer. But can we afford to? Forbes. 2014. Available from: http://www.forbes.com/sites/theapothecary/2014/05/16/sure-well-eventually-beat-cancer-but-can-we-afford-to/2/ [Accessed 7 July 2014]
   Google Scholar
• Experts in Chronic Myeloid Leukemia . The price of drugs for chronic myeloid leukemia (CML) is a reflection of the unsustainable prices of cancer drugs: from the perspective of a large group of CML experts. Blood 2013;121(22):4439-42
   PubMed Web of Science ®Google Scholar
• Carrol C . New immunotherapies for cancer yield exciting results but high cost. Manag Care 2013;22(10):54-6
   Google Scholar
• Kantarjian H , Steensma D , Rius Sanjuan J , et al. High cancer drug prices in the United States: reasons and proposed solutions. J Oncol Pract 2014;10(4):e208-11
   PubMedGoogle Scholar
• Geynisman DM , Chien CR , Smieliauskas F , et al. Economic evaluation of therapeutic cancer vaccines and immunotherapy: a systematic review. Hum Vaccin Immunother 2014;10(11). [Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Morimoto RI , Kline MP , Bimston DN , Cotto JJ . The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 1997;32:17-29
   PubMed Web of Science ®Google Scholar
• Piotrowicz RS , Levin EG . Basolateral membrane-associated 27-kDa heat shock protein and microfilament polymerization. J Biol Chem 1997;272(41):25920-7
   PubMed Web of Science ®Google Scholar
• Tsvetkova NM , Horváth I , Török Z , et al. Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci USA 2002;99(21):13504-9
   PubMed Web of Science ®Google Scholar
• Kirkegaard T , Roth AG , Petersen NH , et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010;463(7280):549-53
   PubMed Web of Science ®Google Scholar
• Beere HM . The stress of dying: the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 2004;117(Pt 13):2641-51
   PubMed Web of Science ®Google Scholar
• Pockley AG . Heat shock proteins as regulators of the immune response. Lancet 2003;362(9382):469-76
   PubMed Web of Science ®Google Scholar
• Quintana FJ , Cohen IR . Heat shock proteins as endogenous adjuvants in sterile and septic inflammation. J Immunol 2005;175:2777-82
   PubMed Web of Science ®Google Scholar
• van Wijk F , Prakken B . Heat shock proteins: darwinistic immune modulation on dangerous grounds. J Leukoc Biol 2011;88(3):431-4
   Web of Science ®Google Scholar
• Friedland JS , Shattock R , Remake DG , Griffin GE . Mycobacterial 65-kd heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 1993;91:58-62
   PubMed Web of Science ®Google Scholar
• Vabulas RM , Braedel S , Hilf N , et al. The endoplasmic reticulum-resident heat shock proteinGp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 2002;277:20847-53
   PubMed Web of Science ®Google Scholar
• Zhang Y , Doerfler M , Lee TC , et al. Mechanisms of stimulation of interleukin-1 beta and tumor necrosis factor alpha by Mycobacterium tuberculosis components. J Clin Invest 2003;91:2076-83
   Google Scholar
• 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 2000;30(8):2211-15
   PubMed Web of Science ®Google Scholar
• Kuppner MC , Gastpar R , Gelwer S , 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(5):1602-9
   PubMed Web of Science ®Google Scholar
• Flohé SB , Brüggemann J , Lendemans S , et al. Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype. J Immunol 2003;170(5):2340-8
   PubMed Web of Science ®Google Scholar
• Udono H , Ichiyanagi T , Mizukami S , Imai T . Heat shock proteins in antigen trafficking–implications on antigen presentation to T cells. Int J Hyperthermia 2009;25(8):617-25
   PubMed Web of Science ®Google Scholar
• Murshid A , Gong J , Stevenson MA , Calderwood SK . Heat shock proteins and cancer vaccines: developments in the past decade and chaperoning in the decade to come. Expert Rev Vaccines 2011;10(11):1553-68
   PubMed Web of Science ®Google Scholar
• Calderwood SK , Mambula SS , Gray PJ Jr , Theriault JR . Extracellular heat shock proteins in cell signaling. FEBS Lett 2007;581(19):3689-94
   PubMed Web of Science ®Google Scholar
• Oura J , Tamura Y , Kamiguchi K , et al. Extracellular heat shock protein 90 plays a role in translocating chaperoned antigen from endosome to proteasome for generating antigenic peptide to be cross-presented by dendritic cells. Int Immunol 2011;23(4):223-37
   PubMed Web of Science ®Google Scholar
• Udono H . Heat shock protein magic in antigen trafficking within dendritic cells: implications in antigen cross-presentation in immunity. Acta Med Okayama 2012;66(1):1-6
   PubMed Web of Science ®Google Scholar
• MacAry PA , Javid B , Floto RA , et al. HSP70 peptide binding mutants separate antigen delivery from dendritic cell stimulation. Immunity 2004;20:95-106
   PubMed Web of Science ®Google Scholar
• Dai J , Liu B , Caudill MM , et al. 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 2003;28(3):1
   Google Scholar
• Liu H , Wu BH , Rowse GJ , Emtage PC . Induction of CD4-independent E7-specific CD8+ memory response by heat shock fusion protein. Clin Vaccine Immunol 2007;14(8):1013-23
   PubMed Web of Science ®Google Scholar
• Gao B , Tsan MF . Endotoxin contamination in recombinant human Hsp70 preparation is responsible for the induction of TNFalpha release by murine macrophages. J Biol Chem 2003;278:174-9
   PubMed Web of Science ®Google Scholar
• Gao B , Tsan MF . Recombinant human heat shock protein 60 does not induce the release of tumor necrosis factor a from murine macrophages. J Biol Chem 2003;278:22523-9
   PubMed Web of Science ®Google Scholar
• Ye Z , Gan YH . Flagellin contamination of recombinant heat shock protein 70 is responsible for its activity on T cells. J Biol Chem 2007;282:4479-84
   PubMed Web of Science ®Google Scholar
• Bendz H , Marincek BC , Momburg F , et al. 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 2008;283:26477-83
   PubMed Web of Science ®Google Scholar
• Henderson B , Calderwood SK , Coates AR , 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(2):123-41
   PubMed Web of Science ®Google Scholar
• Brenu EW , Staines DR , Tajouri L , et al. Heat shock proteins and regulatory T cells. Autoimmune Dis 2013;2013:813256
   PubMedGoogle Scholar
• Shields AM , Panayi GS , Corrigall VM . Resolution-associated molecular patterns (RAMP): RAMParts defending immunological homeostasis? Clin Exp Immunol 2011;165(3):292-300
   PubMed Web of Science ®Google Scholar
• Calderwood SK , Stevenson MA , Murshid A . Heat shock proteins, autoimmunity, and cancer treatment. Autoimmune Dis 2012;2012:486069
   PubMedGoogle Scholar
• Srivastava PK . Peptide-binding heat shock proteins in the endoplasmic reticulum: role in immune response to cancer and in antigen presentation. Adv Cancer Res 1993;62:153-77
   PubMed Web of Science ®Google Scholar
• Suzue K , Young RA . Adjuvant-free hsp70 fusion protein system elicits humoral and cellular immune responses to HIV-1 p24. J Immunol 1996;156(2):873-9
   PubMed Web of Science ®Google Scholar
• Ciocca DR , Cayado-Gutierrez N , Maccioni M , Cuello-Carrion FD . Heat shock proteins (HSPs) based anti-cancer vaccines. Curr Mol Med 2012;12(9):1183-97
   PubMed Web of Science ®Google Scholar
• Maciag PC , Paterson Y . Technology evaluation: hspE7 (Stressgen). Curr Opin Mol Ther 2005;7(3):256-63
   PubMedGoogle Scholar
• Bloch O , Crane CA , Fuks Y , et al. Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro Oncol 2014;16(2):274-9
   PubMed Web of Science ®Google Scholar
• Yang I , Han S , Parsa AT . Heat-shock protein vaccines as active immunotherapy against human gliomas. Expert Rev Anticancer Ther 2009;9(11):1577-82
   PubMed Web of Science ®Google Scholar
• Gelfand J . Engineered antibody-stress protein fusions. US7749501 B2. 2006
   Google Scholar
• Yuan J , Kashiwagi S , Reeves P , et al. A novel mycobacterial Hsp70-containing fusion protein targeting mesothelin augments antitumor immunity and prolongs survival in murine models of ovarian cancer and mesothelioma. J Hematol Oncol 2014;7:15
   PubMed Web of Science ®Google Scholar
• Becker T , Hartl FU , Wieland F . CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J Cell Biol 2002;158(7):1277-85
   PubMed Web of Science ®Google Scholar
• Floto RA , MacAry PA , Boname JM , et al. Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science 2006;314(5798):454-8
   PubMed Web of Science ®Google Scholar
• Tobian AA , Canaday DH , Boom WH , Harding CV . Bacterial heat shock proteins promote CD91-dependent class I MHC cross-presentation of chaperoned peptide to CD8+ T cells by cytosolic mechanisms in dendritic cells versus vacuolar mechanisms in macrophages. J Immunol 2004;172:5277-86
   PubMed Web of Science ®Google Scholar
• Elsaghier A , Prantera C , Bothamley G , et al. Disease association of antibodies to human and mycobacterial hsp70 and hsp60 stress proteins. Clin Exp Immunol 1992;89(2):305-9
   PubMed Web of Science ®Google Scholar
• Zlacka D , Vavrincova P , Hien Nguyen TT , Hromadnikova I . Frequency of anti-hsp60, -65 and -70 antibodies in sera of patients with juvenile idiopathic arthritis. J Autoimmun 2006;27(2):81-8
   PubMed Web of Science ®Google Scholar
• Komiya I , Arimura Y , Nakabayashi K , et al. Increased concentrations of antibody against heat shock protein in patients with myeloperoxidase anti-neutrophil cytoplasmic autoantibody positive microscopic polyangiitis. Microbiol Immunol 2011;55(8):531-8
   PubMed Web of Science ®Google Scholar
• Detanico T , Rodrigues L , Sabritto AC , et al. Mycobacterial heat shock protein 70 induces interleukin-10 production: immunomodulation of synovial cell cytokine profile and dendritic cell maturation. Clin Exp Immunol 2004;135(2):336-42
   PubMed Web of Science ®Google Scholar
• Van Eden W , Wick G , Albani S , Cohen I . Stress, heat shock proteins, and autoimmunity: how immune responses to heat shock proteins are to be used for the control of chronic inflammatory diseases. Ann N Y Acad Sci 2007;1113:217-37
   PubMed Web of Science ®Google Scholar
• Cheng WF , Huang CY , Chang MC , et al. High mesothelin correlates with chemoresistance and poor survival in epithelial ovarian carcinoma. Br J Cancer 2009;100:1144-53
   PubMed Web of Science ®Google Scholar
• Chang MC , Chen CA , Chen PJ , et al. Mesothelin enhances invasion of ovarian cancer by inducing MMP-7 through MAPK/ERK and JNK pathways. Biochem J 2012;442(2):293-302
   PubMedGoogle Scholar
• Yen MJ , Hsu CY , Mao TL , et al. Diffuse mesothelin expression correlates with prolonged patient survival in ovarian serous carcinoma. Clin Cancer Res 2006;12(3 Pt 1):827-31
   PubMed Web of Science ®Google Scholar
• GP96 Heat Shock Protein-Peptide Complex Vaccine in Treating Patients With Recurrent or Progressive Glioma. Available from: http://clinicaltrials.gov/show/NCT00293423
   Google Scholar
• Vaccine Therapy With Bevacizumab Versus Bevacizumab Alone in Treating Patients With Recurrent Glioblastoma Multiforme That Can Be Removed by Surgery. Available from: http://clinicaltrials.gov/show/NCT01814813
   Google Scholar
• HSPPC-96 Vaccine With Temozolomide in Patients With Newly Diagnosed GBM (HeatShock). Available from: http://clinicaltrials.gov/show/NCT00905060:NCT009056
   Google Scholar
• Research for Immunotherapy of Glioblastoma With Autologous Heat Shock Protein gp96. Available from: http://clinicaltrials.gov/show/NCT02122822
   Google Scholar
• Immunotherapy of Tumor With Autologous Tumor Derived Heat Shock Protein gp96. Available from: http://clinicaltrials.gov/show/NCT02133079
   Google Scholar
• Vaccine Therapy in Treating Patients With Advanced Stage III-IV Melanoma. Available from: http://clinicaltrials.gov/show/NCT01744171
   Google Scholar