Peptide vaccines for the treatment of glioblastoma

Journal of Neuro-Oncology

Volumn 123, Issue 3, 2015, Pages 433-440

  Swartz, Adam M ^a   Batich, Kristen A ^a   Fecci, Peter E ^a   Sampson, John H ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

EGFRvIII; Glioblastoma; Glioma; Immunotherapy; Peptide vaccine; Rindopepimut

Indexed keywords

CYTOMEGALOVIRUS VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOLOGICAL ADJUVANT; ISOCITRATE DEHYDROGENASE 1 R132H VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE VACCINE; RINDOPEPIMUT; SL 701 VACCINE; UNCLASSIFIED DRUG; SUBUNIT VACCINE;

ANTIGEN EXPRESSION; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; GLIOBLASTOMA; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOPOTENTIATION; LONG TERM SURVIVAL; NONHUMAN; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REVIEW; TREATMENT DURATION; TUMOR ESCAPE; BRAIN NEOPLASMS; IMMUNOLOGY;

BRAIN NEOPLASMS; GLIOBLASTOMA; HUMANS; VACCINES, SUBUNIT;

EID: 84937513342     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-014-1676-y     Document Type: Review

References (47)

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, 9 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. Dandy WE (1928) Removal of right cerebral hemisphere for certain tumors with hemiplegia. JAMA 90:823–825
3. Liu Q, Nguyen DH, Dong Q, Shitaku P, Chung K, Liu OY, Tso JL, Liu JY, Konkankit V, Cloughesy TF, Mischel PS, Lane TF, Liau LM, Nelson SF, Tso CL (2009) Molecular properties of CD133 + glioblastoma stem cells derived from treatment-refractory recurrent brain tumors. J Neurooncol 94:1–19. doi:10.1007/s11060-009-9919-z
4. Rosenberg SA, Yang JC, Restifo NP (2004) Cancer immunotherapy: moving beyond current vaccines. Nat Med 10:909–915. doi:10.1038/nm1100
5. Evel-Kabler K, Chen SY (2006) Dendritic cell-based tumor vaccines and antigen presentation attenuators. Mol Ther 13:850–858. doi:10.1016/j.ymthe.2006.02.009
6. Xu LW, Chow KK, Lim M, Li G (2014) Current vaccine trials in glioblastoma: a review. J Immunol Res 2014:796856. doi:10.1155/2014/796856
7. Purcell AW, McCluskey J, Rossjohn J (2007) More than one reason to rethink the use of peptides in vaccine design. Nat Rev Drug Discov 6:404–414. doi:10.1038/nrd2224
8. Leadbetter EA, Bourque CR, Devaux B, Olson CD, Sunshine GH, Hirani S, Wallner BP, Smilek DE, Happ MP (1998) Experimental autoimmune encephalomyelitis induced with a combination of myelin basic protein and myelin oligodendrocyte glycoprotein is ameliorated by administration of a single myelin basic protein peptide. J Immunol 161:504–512
9. Sturm D, Bender S, Jones DT, Lichter P, Grill J, Becher O, Hawkins C, Majewski J, Jones C, Costello JF, Iavarone A, Aldape K, Brennan CW, Jabado N, Pfister SM (2014) Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge. Nat Rev Cancer 14:92–107. doi:10.1038/nrc3655
10. Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH, Nabors LB, Cobbs CG, Britt WJ (2002) Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 62:3347–3350
11. Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu CJ, Genovese G, Shmulevich I, Barnholtz-Sloan J, Zou L, Vegesna R, Shukla SA, Ciriello G, Yung WK, Zhang W, Sougnez C, Mikkelsen T, Aldape K, Bigner DD, Van Meir EG, Prados M, Sloan A, Black KL, Eschbacher J, Finocchiaro G, Friedman W, Andrews DW, Guha A, Iacocca M, O’Neill BP, Foltz G, Myers J, Weisenberger DJ, Penny R, Kucherlapati R, Perou CM, Hayes DN, Gibbs R, Marra M, Mills GB, Lander E, Spellman P, Wilson R, Sander C, Weinstein J, Meyerson M, Gabriel S, Laird PW, Haussler D, Getz G, Chin L, Network TR (2013) The somatic genomic landscape of glioblastoma. Cell 155:462–477. doi:10.1016/j.cell.2013.09.034
12. Huang PH, Mukasa A, Bonavia R, Flynn RA, Brewer ZE, Cavenee WK, Furnari FB, White FM (2007) Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci USA 104:12867–12872. doi:10.1073/pnas.0705158104
13. Bigner SH, Humphrey PA, Wong AJ, Vogelstein B, Mark J, Friedman HS, Bigner DD (1990) Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res 50:8017–8022
14. Vogt N, Lefevre SH, Apiou F, Dutrillaux AM, Cor A, Leuraud P, Poupon MF, Dutrillaux B, Debatisse M, Malfoy B (2004) Molecular structure of double-minute chromosomes bearing amplified copies of the epidermal growth factor receptor gene in gliomas. Proc Natl Acad Sci USA 101:11368–11373. doi:10.1073/pnas.0402979101
15. Wikstrand CJ, Reist CJ, Archer GE, Zalutsky MR, Bigner DD (1998) The class III variant of the epidermal growth factor receptor (EGFRvIII): characterization and utilization as an immunotherapeutic target. J Neurovirol 4:148–158. doi:10.3109/13550289809114515
16. Sampson JH, Crotty LE, Lee S, Archer GE, Ashley DM, Wikstrand CJ, Hale LP, Small C, Dranoff G, Friedman AH, Friedman HS, Bigner DD (2000) Unarmed, tumor-specific monoclonal antibody effectively treats brain tumors. Proc Natl Acad Sci USA 97:7503–7508. doi:10.1073/pnas.130166597
17. Heimberger AB, Crotty LE, Archer GE, Hess KR, Wikstrand CJ, Friedman AH, Friedman HS, Bigner DD, Sampson JH (2003) Epidermal growth factor receptor VIII peptide vaccination is efficacious against established intracerebral tumors. Clin Cancer Res 9:4247–4254
18. Sampson JH, Archer GE, Mitchell DA, Heimberger AB, Herndon JE 2nd, Lally-Goss D, McGehee-Norman S, Paolino A, Reardon DA, Friedman AH, Friedman HS, Bigner DD (2009) An epidermal growth factor receptor variant III-targeted vaccine is safe and immunogenic in patients with glioblastoma multiforme. Mol Cancer Ther 8:2773–2779. doi:10.1158/1535-7163.MCT-09-0124
19. 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
20. Sampson JH, Aldape KD, Archer GE, Coan A, Desjardins A, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling R, Shi W, Vredenburgh JJ, Bigner DD, Heimberger AB (2011) Greater chemotherapy-induced lymphopenia enhances tumor-specific immune responses that eliminate EGFRvIII-expressing tumor cells in patients with glioblastoma. Neuro Oncol 13:324–333. doi:10.1093/neuonc/noq157
21. Lai RK, Recht LD, Reardon DA, Paleologos N, Groves M, Rosenfeld MR, Davis T, Archer G, Green J, Heimberger A, Sampson JH (2011) Long-term follow-up of ACT III: A Phase II trial of Rindopepimut (CDX-110) in newly diagnosed glioblastoma. Proceedings of the 16th Annual Scientific Meeting of the Society for Neuro-Oncology in Conjunction with the AANS/CNS Section on Tumors: 34–40
22. Sanchez-Perez LA, Choi BD, Archer GE, Cui X, Flores C, Johnson LA, Schmittling RJ, Snyder D, Herndon JE 2nd, Bigner DD, Mitchell DA, Sampson JH (2013) Myeloablative temozolomide enhances CD8(+) T-cell responses to vaccine and is required for efficacy against brain tumors in mice. PLoS ONE 8:e59082. doi:10.1371/journal.pone.0059082
23. Mitchell DA, Cui X, Schmittling RJ, Sanchez-Perez L, Snyder DJ, Congdon KL, Archer GE, Desjardins A, Friedman AH, Friedman HS, Herndon JE 2nd, McLendon RE, Reardon DA, Vredenburgh JJ, Bigner DD, Sampson JH (2011) Monoclonal antibody blockade of IL-2 receptor alpha during lymphopenia selectively depletes regulatory T cells in mice and humans. Blood 118:3003–3012. doi:10.1182/blood-2011-02-334565
24. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773. doi:10.1056/NEJMoa0808710
25. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, Cross JR, Fantin VR, Hedvat CV, Perl AE, Rabinowitz JD, Carroll M, Su SM, Sharp KA, Levine RL, Thompson CB (2010) The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 17:225–234. doi:10.1016/j.ccr.2010.01.020
26. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, Ito S, Yang C, Wang P, Xiao MT, Liu LX, Jiang WQ, Liu J, Zhang JY, Wang B, Frye S, Zhang Y, Xu YH, Lei QY, Guan KL, Zhao SM, Xiong Y (2011) Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19:17–30. doi:10.1016/j.ccr.2010.12.014
27. Leonardi R, Subramanian C, Jackowski S, Rock CO (2012) Cancer-associated isocitrate dehydrogenase mutations inactivate NADPH-dependent reductive carboxylation. J Biol Chem 287:14615–14620. doi:10.1074/jbc.C112.353946
28. Mullen AR, Wheaton WW, Jin ES, Chen PH, Sullivan LB, Cheng T, Yang Y, Linehan WM, Chandel NS, DeBerardinis RJ (2012) Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481:385–388. doi:10.1038/nature10642
29. Schumacher T, Bunse L, Pusch S, Sahm F, Wiestler B, Quandt J, Menn O, Osswald M, Oezen I, Ott M, Keil M, Balss J, Rauschenbach K, Grabowska AK, Vogler I, Diekmann J, Trautwein N, Eichmuller SB, Okun J, Stevanovic S, Riemer AB, Sahin U, Friese MA, Beckhove P, von Deimling A, Wick W, Platten M (2014) A vaccine targeting mutant IDH1 induces antitumour immunity. Nature. doi:10.1038/nature13387
30. Takamura Y, Ikeda H, Kanaseki T, Toyota M, Tokino T, Imai K, Houkin K, Sato N (2004) Regulation of MHC class II expression in glioma cells by class II transactivator (CIITA). Glia 45:392–405. doi:10.1002/glia.10343
31. Dey M, Ahmed AU, Lesniak MS (2014) Cytomegalovirus and glioma: putting the cart before the horse. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp-2014-307727
32. Dziurzynski K, Chang SM, Heimberger AB, Kalejta RF, McGregor Dallas SR, Smit M, Soroceanu L, Cobbs CS, Hcmv, Gliomas S (2012) Consensus on the role of human cytomegalovirus in glioblastoma. Neuro Oncol 14: 246–255. doi:10.1093/neuonc/nor227
33. James A, Mulholland P, Peoples S, Al-Salihi O, Twelves C, Jefferies S, McBain C, Schoor O, Hilf N, Lindner J, Kutscher S, Peters J, Halford S, McGuigan L, Ritchie J, Singh-Jasuja H, Rampling R (2012) Updated results from a Cancer Research UK first in man Phase I trial of IMA950 (a novel multi peptide vaccine) plus GM-CSF in patients with newly diagnosed glioblastoma. European Society for Medical Oncology. Vienna, Austria
34. Heufler C, Koch F, Schuler G (1988) Granulocyte/macrophage colony-stimulating factor and interleukin 1 mediate the maturation of murine epidermal Langerhans cells into potent immunostimulatory dendritic cells. J Exp Med 167:700–705
35. Bregy A, Wong TM, Shah AH, Goldberg JM, Komotar RJ (2013) Active immunotherapy using dendritic cells in the treatment of glioblastoma multiforme. Cancer Treat Rev 39:891–907. doi:10.1016/j.ctrv.2013.05.007
36. Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, Garcia R, Demaria S, Newcomb EW (2005) Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Lab Investig 85:328–341. doi:10.1038/labinvest.3700233
37. Di Tomaso T, Mazzoleni S, Wang E, Sovena G, Clavenna D, Franzin A, Mortini P, Ferrone S, Doglioni C, Marincola FM, Galli R, Parmiani G, Maccalli C (2010) Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin Cancer Res 16:800–813. doi:10.1158/1078-0432.CCR-09-2730
38. Wei J, Barr J, Kong LY, Wang Y, Wu A, Sharma AK, Gumin J, Henry V, Colman H, Sawaya R, Lang FF, Heimberger AB (2010) Glioma-associated cancer-initiating cells induce immunosuppression. Clin Cancer Res 16:461–473. doi:10.1158/1078-0432.CCR-09-1983
39. Kershaw MH, Devaud C, John LB, Westwood JA, Darcy PK (2013) Enhancing immunotherapy using chemotherapy and radiation to modify the tumor microenvironment. Oncoimmunology 2:e25962. doi:10.4161/onci.25962
40. Wainwright DA, Chang AL, Dey M, Balyasnikova IV, Kim C, Tobias AL, Cheng Y, Kim J, Zhang L, Qiao J, Han Y, Lesniak MS (2014) Durable therapeutic efficacy utilizing combinatorial blockade against IDO, CTLA-4 and PD-L1 in mice with brain tumors. Clin Cancer Res. doi:10.1158/1078-0432.CCR-14-0514
41. Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM (2005) Gemcitabine selectively eliminates splenic Gr-1 +/CD11b + myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 11:6713–6721. doi:10.1158/1078-0432.CCR-05-0883
42. Sampson JH, Schmittling RJ, Archer GE, Congdon KL, Nair SK, Reap EA, Desjardins A, Friedman AH, Friedman HS, Herndon JE 2nd, Coan A, McLendon RE, Reardon DA, Vredenburgh JJ, Bigner DD, Mitchell DA (2012) A pilot study of IL-2Ralpha blockade during lymphopenia depletes regulatory T-cells and correlates with enhanced immunity in patients with glioblastoma. PLoS ONE 7:e31046. doi:10.1371/journal.pone.0031046
43. Del Vecchio CA, Giacomini CP, Vogel H, Jensen KC, Florio T, Merlo A, Pollack JR, Wong AJ (2013) EGFRvIII gene rearrangement is an early event in glioblastoma tumorigenesis and expression defines a hierarchy modulated by epigenetic mechanisms. Oncogene 32:2670–2681. doi:10.1038/onc.2012.280
44. Agarwal S, Sharma MC, Jha P, Pathak P, Suri V, Sarkar C, Chosdol K, Suri A, Kale SS, Mahapatra AK, Jha P (2013) Comparative study of IDH1 mutations in gliomas by immunohistochemistry and DNA sequencing. Neuro Oncol 15:718–726. doi:10.1093/neuonc/not015
45. Cancer Genome Atlas Research N (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068. doi:10.1038/nature07385
46. Jackson C, Ruzevick J, Brem H, Lim M (2013) Vaccine strategies for glioblastoma: progress and future directions. Immunotherapy 5:155–167. doi:10.2217/imt.12.155
47. Aguilar LK, Arvizu M, Aguilar-Cordova E, Chiocca EA (2012) The spectrum of vaccine therapies for patients with glioblastoma multiforme. Curr Treat Options Oncol 13:437–450. doi:10.1007/s11864-012-0208-2