Adjuvants for peptide-based cancer vaccines

Journal for ImmunoTherapy of Cancer

Volumn 4, Issue 1, 2016, Pages

  Khong, Hiep ^a,b   Overwijk, Willem W ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Adjuvant; Cancer vaccine; Checkpoint; Peptide; T cells

Indexed keywords

ADJUVANT; ALUMINUM; CANCER VACCINE; FREUND ADJUVANT; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON; PEPTIDE; TOLL LIKE RECEPTOR 9;

ANTIGEN PRESENTATION; CANCER IMMUNIZATION; CANCER THERAPY; GRANULOCYTE; HUMAN; IMMUNOCOMPETENT CELL; LYMPH NODE; PRIORITY JOURNAL; REVIEW; SURVIVAL RATE; T LYMPHOCYTE;

EID: 84997782968     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-016-0160-y     Document Type: Review

References (124)

1. Curtsinger JM, et al. Inflammatory Cytokines Provide a Third Signal for Activation of Naive CD4+ and CD8+ T Cells. J Immunol. 1999;162:3256-62.
2. Cox JC, Coulter AR. Adjuvants-a classification and review of their modes of action. Vaccine. 1997;15:248-56.
3. O'Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat Rev Drug Discov. 2003;2:727-35.
4. Johansen P, Mohanan D, Martínez-Gómez JM, Kündig TM, Gander B. Lympho-geographical concepts in vaccine delivery. J Controlled Release. 2010;148:56-62.
5. Blair DA, et al. Duration of Antigen Availability Influences the Expansion and Memory Differentiation of T Cells. J Immunol. 2011;187:2310-21.
6. Gruta NLL, Turner SJ, Doherty PC. Hierarchies in Cytokine Expression Profiles for Acute and Resolving Influenza Virus-Specific CD8+ T Cell Responses: Correlation of Cytokine Profile and TCR Avidity. J Immunol. 2004;172:5553-60.
7. Reinhardt RL, Bullard DC, Weaver CT, Jenkins MK. Preferential accumulation of antigen-specific effector CD4 T cells at an antigen injection site involves CD62E-dependent migration but not local proliferation. J Exp Med. 2003;197:751-62.
8. Redmond WL, Sherman LA. Peripheral tolerance of CD8 T lymphocytes. Immunity. 2005;22:275-84.
9. Chiang CL-L, Kandalaft LE, Coukos G. Adjuvants for enhancing the immunogenicity of whole tumor cell vaccines. Int Rev Immunol. 2011;30:150-82.
10. Hailemichael Y, et al. Persistent antigen at vaccination sites induces tumor-specific CD8+ T cell sequestration, dysfunction and deletion. Nat Med. 2013;19:465-72.
11. Bijker MS, 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.
12. Melief CJM, van der Burg SH. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat Rev Cancer. 2008;8:351-60.
13. Slingluff CL, et al. A randomized phase II trial of multiepitope vaccination with melanoma peptides for cytotoxic T cells and helper T cells for patients with metastatic melanoma (E1602). Clin Cancer Res. 2013;19:4228-38.
14. Phan GQ, et al. Immunization of patients with metastatic melanoma using both class I- and class II-restricted peptides from melanoma-associated antigens. J Immunother. 2003;26:349-56.
15. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature. 1998;393:480-3.
16. Bos R, Sherman LA. CD4+ T-Cell Help in the Tumor Milieu Is Required for Recruitment and Cytolytic Function of CD8+ T Lymphocytes. Cancer Res. 2010;70:8368-77.
17. Lindblad EB, Schønberg NE. Aluminum Adjuvants: Preparation, Application, Dosage, and Formulation with Antigen. Vaccine Adjuvants. Davies G, editor. Humana Press; 2010. p. 41-58.
18. Lindblad EB, Elhay MJ, Silva R, Appelberg R, Andersen P. Adjuvant modulation of immune responses to tuberculosis subunit vaccines. Infect Immun. 1997;65:623-9.
19. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature. 2008;453:1122-6.
20. Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014;157:1013-22.
21. Dinarello CA, Novick D, Kim S, Kaplanski G. Interleukin-18 and IL-18 binding protein. Front Immunol. 2013;4:289.
22. Walter E, et al. Hydrophilic poly(DL-lactide-co-glycolide) microspheres for the delivery of DNA to human-derived macrophages and dendritic cells. J Controlled Release. 2001;76:149-68.
23. Reddy ST, Rehor A, Schmoekel HG, Hubbell JA, Swartz MA. In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles. J Controlled Release. 2006;112:26-34.
24. Serda RE. Particle platforms for cancer immunotherapy. Int J Nanomedicine. 2013;8:1683-96.
25. Sharp FA, et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci U S A. 2009;106:870-5.
26. Salvador-Morales C, et al. Complement activation and protein adsorption by carbon nanotubes. Mol Immunol. 2006;43:193-201.
27. Babai I, et al. A novel liposomal influenza vaccine (INFLUSOME-VAC) containing hemagglutinin-neuraminidase and IL-2 or GM-CSF induces protective anti-neuraminidase antibodies cross-reacting with a wide spectrum of influenza A viral strains. Vaccine. 2001;20:505-15.
28. Milla P, Dosio F, Cattel L. PEGylation of proteins and liposomes: a powerful and flexible strategy to improve the drug delivery. Curr Drug Metab. 2012;13:105-19.
29. Ali OA, Huebsch N, Cao L, Dranoff G, Mooney DJ. Infection-mimicking materials to program dendritic cells in situ. Nat Mater. 2009;8:151-8.
30. Ali OA, Emerich D, Dranoff G, Mooney DJ. In Situ Regulation of DC Subsets and T Cells Mediates Tumor Regression in Mice. Sci Transl Med. 2009;1:8ra19.
31. Akondy RS, et al. The Yellow Fever Virus Vaccine Induces a Broad and Polyfunctional Human Memory CD8+ T Cell Response. J Immunol. 2009;183:7919-30.
32. Medzhitov R, Preston-Hurlburt P, Janeway CA. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 1997;388:394-7.
33. Poltorak A, et al. Genetic and Physical Mapping of theLpsLocus: Identification of the Toll-4 Receptor as a Candidate Gene in the Critical Region. Blood Cells Mol Dis. 1998;24:340-55.
34. Yang R-B, et al. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature. 1998;395:284-8.
35. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34:637-50.
36. Kanneganti T-D, Lamkanfi M, Núñez G. Intracellular NOD-like receptors in host defense and disease. Immunity. 2007;27:549-59.
37. Loo Y-M, Gale M. Immune signaling by RIG-I-like receptors. Immunity. 2011;34:680-92.
38. Geijtenbeek TBH, Gringhuis SI. Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol. 2009;9:465-79.
39. Steinhagen F, Kinjo T, Bode C, Klinman DM. TLR-based immune adjuvants. Vaccine. 2011;29:3341-55.
40. Zom GG, et al. Efficient induction of antitumor immunity by synthetic toll-like receptor ligand-peptide conjugates. Cancer Immunol Res. 2014;2:756-64.
41. Desch AN, et al. Dendritic cell subsets require cis-activation for cytotoxic CD8 T-cell induction. Nat Commun. 2014;5:4674.
42. Blasius AL, Beutler B. Intracellular toll-like receptors. Immunity. 2010;32:305-15.
43. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001;413:732-8.
44. Hoebe K, et al. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol. 2003;4:1223-9.
45. Martins KAO, Bavari S, Salazar AM. Vaccine adjuvant uses of poly-IC and derivatives. Expert Rev Vaccines. 2015;14:447-59.
46. Sabbatini P, et al. Phase I Trial of Overlapping Long Peptides from a Tumor Self-Antigen and Poly-ICLC Shows Rapid Induction of Integrated Immune Response in Ovarian Cancer Patients. Clin Cancer Res. 2012;18:6497-508.
47. Thompson EA, et al. Human Anti-CD40 Antibody and Poly IC:LC Adjuvant Combination Induces Potent T Cell Responses in the Lung of Nonhuman Primates. J Immunol. 2015;195:1015-24.
48. Overwijk WW, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med. 2003;198:569-80.
49. Welters MJP, et al. Multiple CD4 and CD8 T-cell activation parameters predict vaccine efficacy in vivo mediated by individual DC-activating agonists. Vaccine. 2007;25:1379-89.
50. Netea MG, der Meer JWMV, Sutmuller RP, Adema GJ, Kullberg B-J. From the Th1/Th2 Paradigm towards a Toll-Like Receptor/T-Helper Bias. Antimicrob Agents Chemother. 2005;49:3991-6.
51. Garçon N, Chomez P, Van Mechelen M. GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Expert Rev Vaccines. 2007;6:723-39.
52. Sosman JA, et al. Adjuvant immunotherapy of resected, intermediate-thickness, node-negative melanoma with an allogeneic tumor vaccine: impact of HLA class I antigen expression on outcome. J Clin Oncol. 2002;20:2067-75.
53. North SA, Graham K, Bodnar D, Venner P. A pilot study of the liposomal MUC1 vaccine BLP25 in prostate specific antigen failures after radical prostatectomy. J Urol. 2006;176:91-5.
54. Atanackovic D, et al. Vaccine-induced CD4+ T cell responses to MAGE-3 protein in lung cancer patients. J Immunol. 2004;172:3289-96.
55. Cervantes JL, Weinerman B, Basole C, Salazar JC. TLR8: the forgotten relative revindicated. Cell Mol Immunol. 2012;9:434-8.
56. Poulin LF, et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8α+dendritic cells. J Exp Med. 2010;207:1261-71.
57. Bishop GA, et al. Molecular mechanisms of B lymphocyte activation by the immune response modifier R-848. J Immunol. 2000;165:5552-7.
58. Caron G, et al. Direct Stimulation of Human T Cells via TLR5 and TLR7/8: Flagellin and R-848 Up-Regulate Proliferation and IFN-γ Production by Memory CD4+ T Cells. J Immunol. 2005;175:1551-7.
59. Beutner KR, et al. Treatment of genital warts with an immune-response modifier (imiquimod). J Am Acad Dermatol. 1998;38:230-9.
60. Love WE, Bernhard JD, Bordeaux JS. Topical imiquimod or fluorouracil therapy for basal and squamous cell carcinoma: a systematic review. Arch Dermatol. 2009;145:1431-8.
61. Smith BD, et al. K562/GM-CSF immunotherapy reduces tumor burden in chronic myeloid leukemia patients with residual disease on imatinib mesylate. Clin Cancer Res. 2010;16:338-47.
62. Daayana S, et al. Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br J Cancer. 2010;102:1129-36.
63. Feyerabend S, et al. Novel multi-peptide vaccination in Hla-A2+ hormone sensitive patients with biochemical relapse of prostate cancer. The Prostate. 2009;69:917-27.
64. Adams S, et al. Immunization of malignant melanoma patients with full-length NY-ESO-1 protein using Toll-like receptor 7 agonist imiquimod as vaccine adjuvant. J Immunol. 2008;181:776-84.
65. Ballas ZK, Rasmussen WL, Krieg AM. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J Immunol. 1996;157:1840-5.
66. Hartmann G, Krieg AM. Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J Immunol. 2000;164:944-53.
67. Vollmer J, et al. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur J Immunol. 2004;34:251-62.
68. Valmori D, et al. Vaccination with NY-ESO-1 protein and CpG in Montanide induces integrated antibody/Th1 responses and CD8 T cells through cross-priming. Proc Natl Acad Sci U S A. 2007;104:8947-52.
69. Karbach J, et al. Tumor-reactive CD8+ T-cell responses after vaccination with NY-ESO-1 peptide, CpG 7909 and Montanide ISA-51: association with survival. Int J Cancer J Int Cancer. 2010;126:909-18.
70. Haining WN, et al. CpG Oligodeoxynucleotides Alter Lymphocyte and Dendritic Cell Trafficking in Humans. Clin Cancer Res. 2008;14:5626-34.
71. Speiser DE, et al. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest. 2005;115:739-46.
72. Baumgaertner P, et al. Vaccination-induced functional competence of circulating human tumor-specific CD8 T-cells. Int J Cancer J Int Cancer. 2012;130:2607-17.
73. Ishii KJ, et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol. 2006;7:40-8.
74. Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 2008;455:674-8.
75. Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 2013;339:786-91.
76. Woo S-R, et al. STING-Dependent Cytosolic DNA Sensing Mediates Innate Immune Recognition of Immunogenic Tumors. Immunity. 2014;41:830-42.
77. Corrales L, Woo S-R, Gajewski TF. Extremely potent immunotherapeutic activity of a STING agonist in the B16 melanoma model in vivo. J Immunother Cancer. 2013;1:1-1.
78. Fu J, et al. STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade. Sci Transl Med. 2015;7:283ra52.
79. Morgan DA, Ruscetti FW, Gallo R. Selective in vitro growth of T lymphocytes from normal human bone marrows. Science. 1976;193:1007-8.
80. Mingari MC, et al. Human interleukin-2 promotes proliferation of activated B cells via surface receptors similar to those of activated T cells. Nature. 1984;312:641-3.
81. Lanier LL, et al. Interleukin 2 activation of natural killer cells rapidly induces the expression and phosphorylation of the Leu-23 activation antigen. J Exp Med. 1988;167:1572-85.
82. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol. 1996;14:259-74.
83. Horvat B, Loukides JA, Anandan L, Brewer E, Flood PM. Production of interleukin 2 and interleukin 4 by immune CD4-CD8+ and their role in the generation of antigen-specific cytotoxic T cells. Eur J Immunol. 1991;21:1863-71.
84. Miller JS, et al. Endogenous IL-2 production by natural killer cells maintains cytotoxic and proliferative capacity following retroviral-mediated gene transfer. Exp Hematol. 1997;25:1140-8.
85. Granucci F, et al. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol. 2001;2:882-8.
86. McDermott DF, Atkins MB. Interleukin-2 therapy of metastatic renal cell carcinoma--predictors of response. Semin Oncol. 2006;33:583-7.
87. Bhatia S, Tykodi SS, Thompson JA. Treatment of Metastatic Melanoma: An Overview. Oncol Williston Park N. 2009;23:488-96.
88. Stoklasek T, Colpitts S, Obar J, Guo C, Lefrancois L. Visualization of IL-15 expression in innate immune cells during homeostasis and inflammation. J Immunol. 2010;184:134.3.
89. Schwartzentruber DJ, et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med. 2011;364:2119-27.
90. de la Rosa M, Rutz S, Dorninger H, Scheffold A. Interleukin-2 is essential for CD4+CD25+ regulatory T cell function. Eur J Immunol. 2004;34:2480-8.
91. Krieg C, Létourneau S, Pantaleo G, Boyman O. Improved IL-2 immunotherapy by selective stimulation of IL-2 receptors on lymphocytes and endothelial cells. Proc Natl Acad Sci U S A. 2010;107:11906-11.
92. Carmenate T, et al. Human IL-2 Mutein with Higher Antitumor Efficacy Than Wild Type IL-2. J Immunol. 2013;190:6230-8.
93. Boyman O, Kovar M, Rubinstein MP, Surh CD, Sprent J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science. 2006;311:1924-7.
94. Murali A, et al. Synergistic antitumor activity of the CD122-biased immunostimulatory cytokine NKTR-214 when combined with anti-PD-1 in murine tumor models. J Immunother Cancer. 2015;3:P231.
95. Griffin JD, et al. The biology of GM-CSF: regulation of production and interaction with its receptor. Int J Cell Cloning. 1990;8 Suppl 1:35-44. 45.
96. Shi Y, et al. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know. Cell Res. 2006;16:126-33.
97. Mach N, et al. Differences in Dendritic Cells Stimulated in Vivo by Tumors Engineered to Secrete Granulocyte-Macrophage Colony-stimulating Factor or Flt3-Ligand. Cancer Res. 2000;60:3239-46.
98. Gillessen S, et al. CD1d-restricted T cells regulate dendritic cell function and antitumor immunity in a granulocyte-macrophage colony-stimulating factor-dependent fashion. Proc Natl Acad Sci U S A. 2003;100:8874-9.
99. Duraiswamy J, Kaluza KM, Freeman GJ, Coukos G. Dual Blockade of PD-1 and CTLA-4 Combined with Tumor Vaccine Effectively Restores T-Cell Rejection Function in Tumors. Cancer Res. 2013;73:3591-603.
100. Wada S, et al. Sequencing CTLA-4 blockade with cell-based immunotherapy for prostate cancer. J Transl Med. 2013;11:89.
101. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci. 2010;107:4275-80.
102. Jinushi M, et al. MFG-E8-mediated uptake of apoptotic cells by APCs links the pro- and antiinflammatory activities of GM-CSF. J Clin Invest. 2007;117:1902-13.
103. Slingluff CL, et al. Randomized Multicenter Trial of the Effects of Melanoma-Associated Helper Peptides and Cyclophosphamide on the Immunogenicity of a Multipeptide Melanoma Vaccine. J Clin Oncol. 2011;29:2924-32.
104. Walter S, et al. Multipeptide immune response to cancer vaccine IMA901 after single-dose cyclophosphamide associates with longer patient survival. Nat Med. 2012;18:1254-61.
105. Schuster SJ, et al. Vaccination With Patient-Specific Tumor-Derived Antigen in First Remission Improves Disease-Free Survival in Follicular Lymphoma. J Clin Oncol JCO.2010.33.3005 (2011). doi: 10.1200/JCO.2010.33.3005
106. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity. 2006;25:373-81.
107. Summers J, Cohen MH, Keegan P, Pazdur R. FDA Drug Approval Summary: Bevacizumab plus Interferon for Advanced Renal Cell Carcinoma. Oncologist. 2010;15:104-11.
108. Sikora AG, et al. IFN-α Enhances Peptide Vaccine-Induced CD8+ T Cell Numbers, Effector Function, and Antitumor Activity. J Immunol. 2009;182:7398-407.
109. Schoenborn JR, Wilson CB. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol. 2007;96:41-101.
110. Miller CHT, Maher SG, Young HA. Clinical Use of Interferon-γ. Ann N Y Acad Sci. 2009;1182:69-79.
111. Alberts DS, et al. Randomized phase 3 trial of interferon gamma-1b plus standard carboplatin/paclitaxel versus carboplatin/paclitaxel alone for first-line treatment of advanced ovarian and primary peritoneal carcinomas: results from a prospectively designed analysis of progression-free survival. Gynecol Oncol. 2008;109:174-81.
112. Kenter GG, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med. 2009;361:1838-47.
113. Bai X-F, Liu J, Li O, Zheng P, Liu Y. Antigenic drift as a mechanism for tumor evasion of destruction by cytolytic T lymphocytes. J Clin Invest. 2003;111:1487-96.
114. Hodi FS, et al. Improved Survival with Ipilimumab in Patients with Metastatic Melanoma. N Engl J Med. 2010;363:711-23.
115. Melero I, et al. Therapeutic vaccines for cancer: an overview of clinical trials. Nat Rev Clin Oncol. 2014;11:509-24.
116. Ahonen CL, 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.
117. Sanchez PJ, McWilliams JA, Haluszczak C, Yagita H, Kedl RM. Combined TLR/CD40 Stimulation Mediates Potent Cellular Immunity by Regulating Dendritic Cell Expression of CD70 In Vivo. J Immunol. 2007;178:1564-72.
118. McWilliams JA, Sanchez PJ, Haluszczak C, Gapin L, Kedl RM. Multiple innate signaling pathways cooperate with CD40 to induce potent, CD70-dependent cellular immunity. Vaccine. 2010;28:1468-76.
119. Garçon N, Van Mechelen M, Wettendorff M. Development and evaluation of AS04, a novel and improved adjuvant system containing MPL. Immunopotentiators in Modern Vaccines. O'Hagan, Virgil E.J.C.S., editor. Academic Press; 2006. p. 161-77.
120. Rudra JS, Tian YF, Jung JP, Collier JH. A self-assembling peptide acting as an immune adjuvant. Proc Natl Acad Sci U S A. 2010;107:622-7.
121. Rudra JS, et al. Modulating adaptive immune responses to peptide self-assemblies. ACS Nano. 2012;6:1557-64.
122. Chesson CB, et al. Antigenic peptide nanofibers elicit adjuvant-free CD8+ T cell responses. Vaccine. 2014;32:1174-80.
123. Stils, H. F. Adjuvants and Antibody Production: Dispelling the Myths Associated with Freund's. Complete and Other Adjuvants. ILAR J. 2005;46:280-93.
124. Lindblad, E. B. Aluminium compounds for use in vaccines. Immunol. Cell Biol. 2004;82:497-505.