Heat shock protein vaccines against glioblastoma: from bench to bedside

Journal of Neuro-Oncology

Volumn 123, Issue 3, 2015, Pages 441-448

  Ampie, Leonel ^a   Choy, Winward ^a   Lamano, Jonathan B ^a   Fakurnejad, Shayan ^a   Bloch, Orin ^a   Parsa, Andrew T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Clinical trial; Glioblastoma; Glioma; Heat shock protein; Immunotherapy; Vaccine

Indexed keywords

ALPHA CRYSTALLIN; BEVACIZUMAB; DACARBAZINE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 110; HEAT SHOCK PROTEIN 170; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN GLYCOPROTEIN 96; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE VACCINE; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VITESPEN; CANCER VACCINE;

ADVANCED CANCER; ANTIGEN PRESENTING CELL; CANCER IMMUNOTHERAPY; CANCER SURGERY; CELL FUNCTION; CLINICAL EFFECTIVENESS; CYTOTOXIC T LYMPHOCYTE; DRUG DOSE ESCALATION; DRUG SAFETY; DRUG TOLERABILITY; GLIOBLASTOMA; HUMAN; IMMUNE RESPONSE; IMMUNITY; KIDNEY CARCINOMA; LYMPHOCYTE; METASTATIC MELANOMA; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; TREATMENT DURATION; UNSPECIFIED SIDE EFFECT; VACCINATION; ANIMAL; BRAIN NEOPLASMS; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; TRANSLATIONAL RESEARCH;

ANIMALS; BRAIN NEOPLASMS; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; GLIOBLASTOMA; HEAT-SHOCK PROTEINS; HUMANS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84937515633     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-015-1837-7     Document Type: Review

References (57)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. doi:10.1056/NEJMoa043330
2. Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB (2006) The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol 8:261–279. doi:10.1215/15228517-2006-008
3. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, Cachola KE, Murray JC, Tihan T, Jensen MC, Mischel PS, Stokoe D, Pieper RO (2007) Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med 13:84–88. doi:10.1038/nm1517
4. Waziri A (2010) Glioblastoma-derived mechanisms of systemic immunosuppression. Neurosurg Clin N Am 21:31–42. doi:10.1016/j.nec.2009.08.005
5. Ampie L, Woolf EC, Dardis C (2015) Immunotherapeutic advancements for glioblastoma. Front Oncol 5:12. doi:10.3389/fonc.2015.00012
6. Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE 2nd, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling RJ, Shi W, Vredenburgh JJ, Bigner DD (2010) Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol 28:4722–4729. doi:10.1200/JCO.2010.28.6963
7. Schirrmacher V, Haas C, Bonifer R, Ahlert T, Gerhards R, Ertel C (1999) Human tumor cell modification by virus infection: an efficient and safe way to produce cancer vaccine with pleiotropic immune stimulatory properties when using Newcastle disease virus. Gene Ther 6:63–73. doi:10.1038/sj.gt.3300787
8. Prins RM, Soto H, Konkankit V, Odesa SK, Eskin A, Yong WH, Nelson SF, Liau LM (2011) Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res 17:1603–1615. doi:10.1158/1078-0432.CCR-10-2563
9. Young JC, Agashe VR, Siegers K, Hartl FU (2004) Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781–791. doi:10.1038/nrm1492
10. Craig E, Weissman JS (1994) Heat shock proteins and molecular chaperones: mediators of protein conformation and turnover in the cell. Cell 78:365–372
11. Graner MW, Bigner DD (2005) Chaperone proteins and brain tumors: potential targets and possible therapeutics. Neuro Oncol 7:260–278. doi:10.1215/s1152851704001188
12. Ciocca DR, Calderwood SK (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implicaitons. Cell Stress Chaperones 10:86–103
13. Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C (2007) Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 81:15–27. doi:10.1189/jlb.0306167
14. Binder RJ (2006) Heat shock protein vaccines: from bench to bedside. Int Rev Immunol 25:353–375
15. Hermisson M, Strik H, Rieger J, Dichgans J, Meyermann R, Weller M (2000) Expression and functional activity of heat shock proteins in human glioblastoma multiforme. Neurology 54:1357–1365
16. Graner MW, Cumming RI, Bigner DD (2007) The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J Neurosci 27:11214–11227
17. Beaman GM, Dennison SR, Chatfield LK, Phoenix DA (2014) Reliability of HSP70 (HSPA) expression as a prognostic marker in glioma. Mol Cell Biochem 393:301–307
18. Flynn GC, Chappell TG, Rothman JE (1989) Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245:385–390
19. Srivastava PK, DeLeo AB, Old LJ (1986) Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc Natl Acad Sci 83:3407–3411
20. Ullrich SJ, Robinson EA, Law LW, Willingham M, Appella E (1986) A mouse tumor-specific transplantation antigen is a heat shock-related protein. Proc Natl Acad Sci 83:3121–3125
21. Srivastava PK, DeLeo AB, Old LJ (1986) Tumor rejection antigens of chemically induced sarcomas of inbred mice. Proc Natl Acad Sci USA 83:3407–3411
22. Ullrich SJ, Robinson EA, Law LW, Willingham M, Appella E (1986) A mouse tumor-specific transplantation antigen is a heat shock-related protein. Proc Natl Acad Sci USA 83:3121–3125
23. Srivastava PK, Maki RG (1991) Stress-induced proteins in immune response to cancer. Curr Top Microbiol Immunol 167:109–123
24. Blachere NE, Li Z, Chandawarkar RY, Suto R, Jaikaria NS, Basu S, Udono H, Srivastava PK (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
25. Binder RJ, Srivastava PK (2004) Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc Natl Acad Sci USA 101:6128–6133. doi:10.1073/pnas.0308180101
26. Basu S, Binder RJ, Ramalingam T, Srivastava PK (2001) CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14:303–313
27. Castellino F, Boucher PE, Eichelberg K, Mayhew M, Rothman JE, Houghton AN, Germain RN (2000) 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
28. Matsutake T, Sawamura T, Srivastava PK (2010) High efficiency CD91- and LOX-1-mediated re-presentation of gp96-chaperoned peptides by MHC II molecules. Cancer Immun 10:7
29. Berwin B, Hart JP, Pizzo SV, Nicchitta CV (2002) Cutting edge: CD91-independent cross-presentation of GRP94(gp96)-associated peptides. J Immunol 168:4282–4286
30. Panjwani NN, Popova L, Srivastava PK (2002) Heat shock proteins gp96 and hsp70 activate the release of nitric oxide by APCs. J Immunol 168:2997–3003
31. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185–194. doi:10.1038/nri749
32. Vanderlugt CL, Begolka WS, Neville KL, Katz-Levy Y, Howard LM, Eagar TN, Bluestone JA, Miller SD (1998) The functional significance of epitope spreading and its regulation by co-stimulatory molecules. Immunol Rev 164:63–72
33. Srivastava PK (1997) Purification of heat shock protein-peptide complexes for use in vaccination against cancers and intracellular pathogens. Methods 12(2):165–171
34. See AP, Pradilla G, Yang I, Han S, Parsa AT, Lim M (2011) Heat shock protein-peptide complex in the treatment of glioblastoma. Expert Rev Vaccines 10:721–731. doi:10.1586/erv.11.49
35. Belli F, Testori A, Rivoltini L, Maio M, Andreola G, Sertoli MR, Gallino G, Piris A (2002) 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. doi:10.1200/JCO.2002.09.134
36. Janetzki S, Palla D, Rosenhauer V, Lochs H, Lewis JJ, Srivastava PK (2000) Immunization of cancer patients with autologous cancer-derived heat shock protein gp96 preparations: a pilot study. Int J Cancer 88:232–238
37. Hishii M, Andrews D, Boyle LA, Wong JT, Pandolfi F, van den Elsen PJ, Kurnick JT (1997) In vivo accumulation of the same anti-melanoma T cell clone in two different metastatic sites. Proc Natl Acad Sci USA 94:1378–1383
38. Jager E, Ringhoffer M, Dienes HP, Arand M, Karbach J, Jager D, Ilsemann C, Hagedorn M, Oesch F, Knuth A (1996) Granulocyte-macrophage-colony-stimulating factor enhances immune responses to melanoma-associated peptides in vivo. Int J Cancer 67:54–62. doi:10.1002/(SICI)1097-0215(19960703)67
39. Rivoltini L, Castelli C, Carrabba M, Mazzaferro V, Pilla L, Huber V, Coppa J, Gallino G, Scheibenbogen C, Squarcina P, Cova A, Camerini R, Lewis JJ, Srivastava PK, Parmiani G (2003) 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
40. Mazzaferro V, Coppa J, Carrabba MG, Rivoltini L, Schiavo M, Regalia E, Mariani L, Camerini T, Marchiano A, Andreola S, Camerini R, Corsi M, Lewis JJ, Srivastava PK, Parmiani G (2003) Vaccination with autologous tumor-derived heat-shock protein gp96 after liver resection for metastatic colorectal cancer. Clin Cancer Res 9:3235–3245
41. Santis G, Senzer NN, Champagne P, Isakov L, Teofilovici F (2008) Phase II feasibility study of autologous vaccine (HSPPC-96) in patients with resectable lung cancer. J Clin Oncol 26(15):7584
42. Maki RG, Livingston PO, Lewis JJ, Janetzki S, Klimstra D, Desantis D, Srivastava PK, Brennan MF (2007) A phase I pilot study of autologous heat shock protein vaccine HSPPC-96 in patients with resected pancreatic adenocarcinoma. Dig Dis Sci 52:1964–1972. doi:10.1007/s10620-006-9205-2
43. Pilla L, Patuzzo R, Rivoltini L, Maio M, Pennacchioli E, Lamaj E, Maurichi A, Massarut S, Marchiano A, Santantonio C, Tosi D, Arienti F, Cova A, Sovena G, Piris A, Nonaka D, Bersani I, Di Florio A, Luigi M, Srivastava PK, Hoos A, Santinami M, Parmiani G (2006) 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 55:958–968. doi:10.1007/s00262-005-0084-8
44. Oki Y, McLaughlin P, Fayad LE, Pro B, Mansfield PF, Clayman GL, Medeiros LJ, Kwak LW, Srivastava PK, Younes A (2007) Experience with heat shock protein-peptide complex 96 vaccine therapy in patients with indolent non-Hodgkin lymphoma. Cancer 109:77–83. doi:10.1002/cncr.22389
45. Testori A, Richards J, Whitman E, Mann GB, Lutzky J, Camacho L, Parmiani G, Tosti G, Kirkwood JM, Hoos A, Yuh L, Gupta R, Srivastava PK, Group CS (2008) 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. doi:10.1200/JCO.2007.11.9941
46. Wood C, Srivastava P, Bukowski R, Lacombe L, Gorelov AI, Gorelov S, Mulders P, Zielinski H, Hoos A, Teofilovici F, Isakov L, Flanigan R, Figlin R, Gupta R, Escudier B, Group CRS (2008) 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 372:145–154. doi:10.1016/S0140-6736(08)60697-2
47. Messing EM, Manola J, Wilding G, Propert K, Fleischmann J, Crawford ED, Pontes JE, Hahn R, Trump D, Eastern Cooperative Oncology Group/Intergroup trail (2003) Phase III study of interferon alfa-NL as adjuvant treatment for resectable renal cell carcinoma: an Eastern Cooperative Oncology Group/Intergroup trial. J Clin Oncol 21:1214–1222
48. Wood CG, Srivastava P, Lacombe L, Gorelov AI, Gorelov S, Mulders P, Zielinski H, Teofilovici F, Isakov L, Escudier B (2009) Survival update from a multicenter, randomized, phase III trial of vitespen versus observation as adjuvant therapy for renal cell carcinoma in patients at high risk of recurrence. J Clin Oncol 27(15S):3009
49. Crane CA, Han SJ, Ahn B, Oehlke J, Kivett V, Fedoroff A, Butowski N, Chang SM, Clarke J, Berger MS, McDermott MW, Prados MD, Parsa AT (2013) Individual patient-specific immunity against high-grade glioma after vaccination with autologous tumor derived peptides bound to the 96 KD chaperone protein. Clin Cancer Res 19:205–214. doi:10.1158/1078-0432.CCR-11-3358
50. Bloch O, Crane CA, Fuks Y, Kaur R, Aghi MK, Berger MS, Butowski NA, Chang SM, Clarke JL, McDermott MW, Prados MD, Sloan AE, Bruce JN, Parsa AT (2014) Heat-shock protein peptide complex-96 vaccination for recurrent glioblastoma: a phase II, single-arm trial. Neuro Oncol 16:274–279. doi:10.1093/neuonc/not203
51. Kunwar S, Chang S, Westphal M, Vogelbaum M, Sampson J, Barnett G, Shaffrey M, Ram Z, Piepmeier J, Prados M, Croteau D, Pedain C, Leland P, Husain SR, Joshi BH, Puri RK, Group PS (2010) Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol 12:871–881. doi:10.1093/neuonc/nop054
52. Bloch O, Kaur R, Aghi M, McDermott M, Berger M, Parsa A (2013) Glioma-induced immunosuppression shortens progression-free survival in a trial of immunotherapy for glioblastoma. J Neurosurg, 119: A565
53. Khasraw M, Ameratunga MS, Grant R, Wheeler H, Pavlakis N (2014) Antiangiogenic therapy for high-grade glioma. Cochrane Database Syst Rev. doi:10.1002/14651858
54. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, Brandes AA, Hilton M, Abrey L, Cloughesy T (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722. doi:10.1056/NEJMoa1308345
55. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, Jeraj R, Brown PD, Jaeckle KA, Schiff D, Stieber VW, Brachman DG, Werner-Wasik M, Tremont-Lukats IW, Sulman EP, Aldape KD, Curran WJ Jr, Mehta MP (2014) A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 370:699–708. doi:10.1056/NEJMoa1308573
56. Bloch O, Parsa AT (2014) Heat shock protein peptide complex-96 (HSPPC-96) vaccination for recurrent glioblastoma: a phase II, single arm trial. Neuro Oncol 16:758–759. doi:10.1093/neuonc/nou054
57. Chamberlain MC (2014) Is there a role for vaccine-based therapy in recurrent glioblastoma? Neuro Oncol 16:757. doi:10.1093/neuonc/nou031