Optimization of peptide vaccines to induce robust antitumor CD4 T-cell responses

Cancer Immunology Research

Volumn 5, Issue 1, 2017, Pages 72-83

  Kumai, Takumi ^a,b   Lee, Sujin ^c,d   Cho, Hyun Il ^e   Sultan, Hussein ^a   Kobayashi, Hiroya ^b   Harabuchi, Yasuaki ^b   Celis, Esteban ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

^e The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CD40 LIGAND MONOCLONAL ANTIBODY; CPG OLIGODEOXYNUCLEOTIDE; DIPHTHERIA PERTUSSIS TETANUS VACCINE; GDQ; IMMUNOLOGICAL ADJUVANT; LIPOPOLYSACCHARIDE; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG; CD134 ANTIGEN; EPITOPE; INTERFERON; SUBUNIT VACCINE; TOLL LIKE RECEPTOR; TUMOR ANTIGEN;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PREVENTION; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG DESIGN; DRUG EFFECT; DRUG MECHANISM; FEMALE; HELPER CELL; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE FUNCTION; MELANOCYTE; MELANOMA; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; T CELL DEPLETION; TREATMENT OUTCOME; TUMOR GROWTH; VACCINATION; AGONISTS; ANIMAL; CYTOTOXICITY; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; KNOCKOUT MOUSE; METABOLISM; NEOPLASM; PATHOLOGY;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; FEMALE; IMMUNE TOLERANCE; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE; INTERFERONS; MICE; MICE, KNOCKOUT; NEOPLASMS; RECEPTORS, OX40; TOLL-LIKE RECEPTORS; VACCINES, SUBUNIT;

EID: 85016132017     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-16-0194     Document Type: Article

References (52)

1. Brudno JN, Somerville RP, Shi V, Rose JJ, Halverson DC, Fowler DH, et al. Allogeneic T cells that express an anti-CD19 chimeric antigen receptor induce remissions of B-cell malignancies that progress after allogeneic hematopoietic stem-cell transplantation without causing graft-versus-host disease. J Clin Oncol 2016;34:1112-21.
2. Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: Long-term follow-up and correlates with response. Clin Cancer Res 2015;21:1019-27.
3. Andersen R, Donia M, Ellebaek E, Borch TH, Kongsted P, Iversen TZ, et al. Long-lasting complete responses in patients with metastatic melanoma after adoptive cell therapy with tumor-infiltrating lymphocytes and an attenuated IL-2 regimen. Clin Cancer Res 2016;22: 3734-45.
4. Koido S, Homma S, Okamoto M, Takakura K, Mori M, Yoshizaki S, et al. Treatment with chemotherapy and dendritic cells pulsed with multiple Wilms' tumor 1 (WT1)-specific MHC class I/II-restricted epitopes for pancreatic cancer. Clin Cancer Res 2014;20:4228-39.
5. Zhang S, Li W, Xia Z, Mao Y. CD4 T cell dependent tumor immunity stimulated by dendritic cell based vaccine. Biochem Biophys Res Commun 2011;413:294-8.
6. Kreiter S, Vormehr M, van de Roemer N, Diken M, Lower M, Diekmann J, et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 2015;520:692-6.
7. Kennedy R, Celis E. T helper lymphocytes rescue CTL from activationinduced cell death. J Immunol 2006;177:2862-72.
8. Kumai T, Matsuda Y, Ohkuri T, Oikawa K, Ishibashi K, Aoki N, et al. c-Met is a novel tumor associated antigen for T-cell based immunotherapy against NK/T cell lymphoma. Oncoimmunology 2015;4:e976077.
9. Kumai T, Matsuda Y, Oikawa K, Aoki N, Kimura S, Harabuchi Y, et al. EGFR inhibitors augment antitumour helper T-cell responses of HER familyspecific immunotherapy. Br J Cancer 2013;109:2155-66.
10. Hailemichael Y, Dai Z, Jaffarzad N, Ye Y, Medina MA, Huang XF, et al. Persistent antigen at vaccination sites induces tumor-specific CD8(+) T cell sequestration, dysfunction and deletion. Nat Med 2013;19:465-72.
11. Ahonen CL, Doxsee CL, McGurran SM, Riter TR, Wade WF, Barth RJ, et al. Combined TLR and CD40 triggering induces potent CD8+T cell expansion with variable dependence on type I IFN. J Exp Med 2004;199:775-84.
12. McWilliams JA, McGurran SM, Dow SW, Slansky JE, Kedl RM. A modified tyrosinase-related protein 2 epitope generates high-affinity tumor-specific T cells but does not mediate therapeutic efficacy in an intradermal tumor model. J Immunol 2006;177:155-61.
13. Ahonen CL, Wasiuk A, Fuse S, Turk MJ, Ernstoff MS, Suriawinata AA, et al. Enhanced efficacy and reduced toxicity of multifactorial adjuvants compared with unitary adjuvants as cancer vaccines. Blood 2008;111:3116-25.
14. Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J, Bumbaca S, et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 2014;515:572-6.
15. Assudani D, Cho HI, DeVito N, Bradley N, Celis E. In vivo expansion, persistence, and function of peptide vaccine-induced CD8 T cells occur independently of CD4 T cells. Cancer Res 2008;68:9892-9.
16. Cho HI, Celis E. Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects. Cancer Res 2009;69:9012-9.
17. Broomfield SA, van der Most RG, Prosser AC, Mahendran S, Tovey MG, Smyth MJ, et al. Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J Immunol 2009;182:5217-24.
18. Dovedi SJ, Lipowska-Bhalla G, Beers SA, Cheadle EJ, Mu L, Glennie MJ, et al. Antitumor efficacy of radiation plus immunotherapy depends upon dendritic cell activation of effector CD8+ T cells. Cancer Immunol Res 2016;4:621-30.
19. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, et al. Tumorspecific Th17-polarized cells eradicate large established melanoma. Blood 2008;112:362-73.
20. Barrios K, Celis E. TriVax-HPV: An improved peptide-based therapeutic vaccination strategy against human papillomavirus-induced cancers. Cancer Immunol Immunother 2012;61:1307-17.
21. Moon JJ, Chu HH, Pepper M, McSorley SJ, Jameson SC, Kedl RM, et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 2007;27:203-13.
22. Wang Z, Celis E. STING activator c-di-GMP enhances the anti-tumor effects of peptide vaccines in melanoma-bearingmice. Cancer Immunol Immunother 2015;64:1057-66.
23. Maecker HT, Umetsu DT, DeKruyff RH, Levy S. Cytotoxic T cell responses to DNA vaccination: Dependence on antigen presentation via class II MHC. J Immunol 1998;161:6532-6.
24. Dawicki W, Bertram EM, Sharpe AH, Watts TH. 4-1BB and OX40 act independently to facilitate robust CD8 and CD4 recall responses. J Immunol 2004;173:5944-51.
25. Moutaftsi M, Bui HH, Peters B, Sidney J, Salek-Ardakani S, Oseroff C, et al. Vaccinia virus-specific CD4+T cell responses target a set of antigens largely distinct from those targeted by CD8+ T cell responses. J Immunol 2007; 178:6814-20.
26. Caron G, Duluc D, Fremaux I, Jeannin P, David C, Gascan H, et al. Direct stimulation of human T cells via TLR5 and TLR7/8: flagellin and R-848 upregulate proliferation and IFN-gamma production by memory CD4+ T cells. J Immunol 2005;175:1551-7.
27. Kobayashi H, Celis E. Peptide epitope identification for tumor-reactive CD4 T cells. Curr Opin Immunol 2008;20:221-7.
28. Nagato T, Lee YR, Harabuchi Y, Celis E. Combinatorial immunotherapy of polyinosinic-polycytidylic acid and blockade of programmed death-ligand 1 induce effective CD8 T-cell responses against established tumors. Clin Cancer Res 2014;20:1223-34.
29. Cho HI, Reyes-Vargas E, Delgado JC, Celis E. A potent vaccination strategy that circumvents lymphodepletion for effective antitumor adoptive T-cell therapy. Cancer Res 2012;72:1986-95.
30. Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, et al. Cancer immunotherapy based on mutation-specific CD4+T cells in a patient with epithelial cancer. Science 2014;344:641-5.
31. Gramaglia I, Jember A, Pippig SD, Weinberg AD, Killeen N, Croft M. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J Immunol 2000;165: 3043-50.
32. Kurche JS, Burchill MA, Sanchez PJ, Haluszczak C, Kedl RM. Comparison of OX40 ligand and CD70 in the promotion of CD4+ T cell responses. J Immunol 2010;185:2106-15.
33. Ruby CE, Montler R, Zheng R, Shu S, Weinberg AD. IL-12 is required for anti-OX40-mediated CD4 T cell survival. J Immunol 2008;180:2140-8.
34. Rogers PR, Song J, Gramaglia I, Killeen N, Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity 2001;15:445-55.
35. Caserta S, Alessi P, Basso V, Mondino A. IL-7 is superior to IL-2 for ex vivo expansion of tumour-specific CD4(+) T cells. Eur J Immunol 2010;40: 470-9.
36. Yamaki S, Ine S, Kawabe T, Okuyama Y, Suzuki N, Soroosh P, et al. OX40 and IL-7 play synergistic roles in the homeostatic proliferation of effector memory CD4(+) T cells. Eur J Immunol 2014;44:3015-25.
37. Kim YH, Shin SM, Choi BK, Oh HS, Kim CH, Lee SJ, et al. Authentic GITR signaling fails to induce tumor regression unless Foxp3+ regulatory T cells are depleted. J Immunol 2015;195:4721-9.
38. Kato T, Hakamada R, Yamane H, Nariuchi H. Induction of IL-12 p40 messenger RNA expression and IL-12 production of macrophages via CD40-CD40 ligand interaction. J Immunol 1996;156:3932-8.
39. Takeda I, Ine S, Killeen N, Ndhlovu LC, Murata K, Satomi S, et al. Distinct roles for the OX40-OX40 ligand interaction in regulatory and nonregulatory T cells. J Immunol 2004;172:3580-9.
40. So T, Croft M. Cutting edge: OX40 inhibits TGF-beta-and antigen-driven conversion of naive CD4 T cells into CD25+Foxp3+ T cells. J Immunol 2007;179:1427-30.
41. Kim IK, Kim BS, Koh CH, Seok JW, Park JS, Shin KS, et al. Glucocorticoid-induced tumor necrosis factor receptor-related protein co-stimulation facilitates tumor regression by inducing IL-9-producing helper T cells. Nat Med 2015;21:1010-7.
42. Munks MW, Mourich DV, Mittler RS, Weinberg AD, Hill AB. 4-1BB and OX40 stimulation enhance CD8 and CD4 T-cell responses to aDNAprime, poxvirus boost vaccine. Immunology 2004;112:559-66.
43. Warger T, Osterloh P, Rechtsteiner G, Fassbender M, Heib V, Schmid B, et al. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood 2006;108:544-50.
44. Kim JJ, Nottingham LK, Sin JI, Tsai A, Morrison L, Oh J, et al. CD8 positive T cells influence antigen-specific immuneresponses through the expression of chemokines. J Clin Invest 1998;102:1112-24.
45. Teague TK, Marrack P, Kappler JW, Vella AT. IL-6 rescues resting mouse T cells from apoptosis. J Immunol 1997;158:5791-6.
46. Cozza EM, Cooper TK, Budgeon LR, Christensen ND, Schell TD. Protection from tumor recurrence following adoptive immunotherapy varies with host conditioning regimen despite initial regression of autochthonous murine brain tumors. Cancer Immunol Immunother 2015;64:325-36.
47. de Goer de Herve MG, Cariou A, Simonetta F, Taoufik Y. Heterospecific CD4 help to rescue CD8 T cell killers. J Immunol 2008;181:5974-80.
48. Ahrends T, Babala N, Xiao Y, Yagita H, van Eenennaam H, Borst J. CD27 Agonism plus PD-1 blockade recapitulates CD4+T-cell help in therapeutic anticancer vaccination. Cancer Res 2016;76:2921-31.
49. Gebe JA, Falk BA, Rock KA, Kochik SA, Heninger AK, Reijonen H, et al. Lowavidity recognition by CD4+ T cells directed to self-antigens. Eur J Immunol 2003;33:1409-17.
50. Overwijk WW, Lee DS, Surman DR, Irvine KR, Touloukian CE, Chan CC, et al. Vaccination with a recombinant vaccinia virus encoding a "self" antigen induces autoimmune vitiligo and tumor cell destruction in mice: requirement for CD4(+) T lymphocytes. Proc Natl Acad Sci U S A 1999; 96:2982-7.
51. Johnson DB, Estrada MV, Salgado R, Sanchez V, Doxie DB, Opalenik SR, et al. Melanoma-specific MHC-II expression represents a tumour-autonomous phenotype and predicts response to anti-PD-1/PD-L1 therapy. Nat Commun 2016;7:10582.
52. Kinter AL, Godbout EJ, McNally JP, Sereti I, Roby GA, O'Shea MA, et al. The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J Immunol 2008; 181:6738-46.