Improving T cell responses to modified peptides in tumor vaccines

Immunologic Research

Volumn 55, Issue 1-3, 2013, Pages 34-47

  Buhrman, Jonathan D ^a   Slansky, Jill E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Affinity; Altered peptide ligands; Heteroclitic peptide; Mimotope; Modified peptide; Vaccine

Indexed keywords

CANCER VACCINE; MIMOTOPE VACCINE; PEPTIDE; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; TUMOR VACCINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGEN STRUCTURE; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL CLONE; CELL FUNCTION; COLON CARCINOMA; CROSS PRESENTATION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; MEMORY CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VACCINATION;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; NEOPLASMS; VACCINES, SUBUNIT;

EID: 84876714147     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-012-8348-9     Document Type: Article

References (125)

1. Coley WB II. Contribution to the knowledge of Sarcoma. Ann Surg. 1891;14:199-220.
2. Burnet M. Cancer: a biological approach. III. Viruses associated with neoplastic conditions. IV. Practical applications. Br Med J. 1957;1:841-7.
3. Thomas L. In Cellular and humoral aspects of the hypersensitive states. Discussion, ed. e.H. Lawrence. 1959; New York: Hoeber-Harper.
4. Quezada SA, et al. Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Immunol Rev. 2011;241:104-18.
5. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480:480-9.
6. Stutman O. Chemical carcinogenesis in nude mice: comparison between nude mice from homozygous matings and heterozygous matings and effect of age and carcinogen dose. J Natl Cancer Inst. 1979;62:353-8.
7. Stutman O. Tumor development after 3-methylcholanthrene in immunologically deficient athymic-nude mice. Science. 1974;183:534-6.
8. Maleckar JR, Sherman LA. The composition of the T cell receptor repertoire in nude mice. J Immunol. 1987;138:3873-6.
9. Street SE, et al. Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J Exp Med. 2002;196:129-34.
10. Shankaran V, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410:1107-11.
11. Dudley ME, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science. 2002;298:850-4.
12. Koebel CM, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature. 2007;450:903-7.
13. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol. 2006;6:836-48.
14. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol. 2004;22:329-60.
15. Maeurer MJ, et al. Tumor escape from immune recognition: lethal recurrent melanoma in a patient associated with downregulation of the peptide transporter protein TAP-1 and loss of expression of the immunodominant MART-1/Melan-A antigen. J Clin Invest. 1996;98:1633-41.
16. Maeurer MJ, et al. Tumor escape from immune recognition: loss of HLA-A2 melanoma cell surface expression is associated with a complex rearrangement of the short arm of chromosome 6. Clin Cancer Res. 1996;2:641-52.
17. Zhou G, et al. Reciprocal changes in tumor antigenicity and antigen-specific T cell function during tumor progression. J Exp Med. 2004;200:1581-92.
18. Matsushita H, et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature. 2012;482:400-4.
19. Jarnicki AG, et al. Suppression of antitumor immunity by IL-10 and TGF-beta-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J Immunol. 2006;177:896-904.
20. Lizee G, et al. Immunosuppression in melanoma immunotherapy: potential opportunities for intervention. Clin Cancer Res. 2006;12:2359s-65s.
21. Gross S, et al. Immunosuppressive mechanisms in cancer: consequences for the development of therapeutic vaccines. Vaccine. 2009;27:3398-400.
22. Zhang N, Bevan MJ. CD8(+) T cells: foot soldiers of the immune system. Immunity. 2011;35:161-8.
23. Buonaguro L, et al. Translating tumor antigens into cancer vaccines. Clin Vaccine Immunol. 2010;18:23-34.
24. Wilson RK, et al. Structure, organization and polymorphism of murine and human T-cell receptor alpha and beta chain gene families. Immunol Rev. 1988;101:149-72.
25. Krogsgaard M, Davis MM. How T cells 'see' antigen. Nat Immunol. 2005;6:239-45.
26. Lefrancois L, Obar JJ. Once a killer, always a killer: from cytotoxic T cell to memory cell. Immunol Rev. 2010;235:206-18.
27. Zehn D, Lee SY, Bevan MJ. Complete but curtailed T-cell response to very low-affinity antigen. Nature. 2009;458:211-4.
28. Lenschow DJ, Walunas TL, Bluestone JA. CD28/B7 system of T cell costimulation. Annu Rev Immunol. 1996;14:233-58.
29. Curtsinger JM, et al. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol. 2005;174:4465-9.
30. Sun JC, Bevan MJ. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science. 2003;300:339-42.
31. Slifka MK, Whitton JL. Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat Immunol. 2001;2:711-7.
32. Appay V, Douek DC, Price DA. CD8+ T cell efficacy in vaccination and disease. Nat Med. 2008;14:623-8.
33. Dunbar PR, et al. A shift in the phenotype of melan-A-specific CTL identifies melanoma patients with an active tumor-specific immune response. J Immunol. 2000;165:6644-52.
34. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252-64.
35. La Gruta NL, Doherty PC, Turner SJ. A correlation between function and selected measures of T cell avidity in influenza virus-specific CD8+ T cell responses. Eur J Immunol. 2006;36:2951-9.
36. Almeida JR, et al. Antigen sensitivity is a major determinant of CD8 + T-cell polyfunctionality and HIV-suppressive activity. Blood. 2009;113:6351-60.
37. Lee PP, et al. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat Med. 1999;5:677-85.
38. Prehn RT. Main JM Immunity to methylcholanthrene-induced sarcomas. J Natl Cancer Inst. 1957;18:769-78.
39. Linard B, et al. A ras-mutated peptide targeted by CTL infiltrating a human melanoma lesion. J Immunol. 2002;168:4802-8.
40. Ito D, et al. Immunological characterization of missense mutations occurring within cytotoxic T cell-defined p53 epitopes in HLA-A0201 + squamous cell carcinomas of the head and neck. Int J Cancer. 2007;120:2618-24.
41. Sjoblom T, et al. The consensus coding sequences of human breast and colorectal cancers. Science. 2006;314:268-74.
42. Segal NH, et al. Epitope landscape in breast and colorectal cancer. Cancer Res. 2008;68:889-92.
43. Beaudenon S, et al. A novel type of human papillomavirus associated with genital neoplasias. Nature. 1986;321:246-9.
44. List AF, Greco FA, Vogler LB. Lymphoproliferative diseases in immunocompromised hosts: the role of Epstein-Barr virus. J Clin Oncol. 1987;5:1673-89.
45. Tsukuma H, et al. Risk factors for hepatocellular carcinoma among patients with chronic liver disease. N Engl J Med. 1993;328:1797-801.
46. Beasley RP, et al. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet. 1981;2:1129-33.
47. Koutsky LA, et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med. 2002;347:1645-51.
48. Chang MH, et al. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N Engl J Med. 1997;336:1855-9.
49. Speiser DE, Romero P. Molecularly defined vaccines for cancer immunotherapy, and protective T cell immunity. Semin Immunol. 2010;22:144-54.
50. Sick Andersen R, et al. Dissection of T cell antigen specificity in human melanoma. Cancer Res. 2012;72:1642-50.
51. Hogquist KA, Baldwin TA, Jameson SC. Central tolerance: learning self-control in the thymus. Nat Rev Immunol. 2005;5:772-82.
52. Kappler JW, Roehm N, Marrack P. T cell tolerance by clonal elimination in the thymus. Cell. 1987;49:273-80.
53. Huang AY, et al. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc Natl Acad Sci USA. 1996;93:9730-5.
54. McWilliams JA, et al. Age-dependent tolerance to an endogenous tumor-associated antigen. Vaccine. 2008;26:1863-73.
55. Huijbers IJ, et al. Minimal tolerance to a tumor antigen encoded by a cancer-germline gene. J Immunol. 2012;188:111-21.
56. de Visser KE, et al. Low-avidity self-specific T cells display a pronounced expansion defect that can be overcome by altered peptide ligands. J Immunol. 2001;167:3818-28.
57. Zehn D, Bevan MJ. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity. 2006;25:261-70.
58. Mamula MJ. The inability to process a self-peptide allows autoreactive T cells to escape tolerance. J Exp Med. 1993;177:567-71.
59. Colella TA, et al. Self-tolerance to the murine homologue of a tyrosinase-derived melanoma antigen: implications for tumor immunotherapy. J Exp Med. 2000;191:1221-32.
60. Yu Z, et al. Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance. J Clin Invest. 2004;114:551-9.
61. Redmond WL, Sherman LA. Peripheral tolerance of CD8 T lymphocytes. Immunity. 2005;22:275-84.
62. Casares N, et al. Immunization with a tumor-associated CTL epitope plus a tumor-related or unrelated Th1 helper peptide elicits protective CTL immunity. Eur J Immunol. 2001;31:1780-9.
63. Casares N, et al. CD4 +/CD25 + regulatory cells inhibit activation of tumor-primed CD4 + T cells with IFN-gamma-dependent antiangiogenic activity, as well as long-lasting tumor immunity elicited by peptide vaccination. J Immunol. 2003;171:5931-9.
64. Kemmler CB, et al. Elevated tumor-associated antigen expression suppresses variant Peptide vaccine responses. J Immunol. 2011;187:4431-9.
65. Fletcher AL, Malhotra D, Turley SJ. Lymph node stroma broaden the peripheral tolerance paradigm. Trends Immunol. 2010;32:12-8.
66. Cohen JN, et al. Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J Exp Med. 2010;207:681-8.
67. Lund AW, et al. VEGF-C promotes immune tolerance in B16 melanomas and cross-presentation of tumor antigens by lymph node lymphatics. Cell Rep. 2012;1:191-9.
68. Kawakami Y, et al. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc Natl Acad Sci USA. 1994;91:6458-62.
69. Dougan M, Dranoff G. Immune therapy for cancer. Annu Rev Immunol. 2009;27:83-117.
70. Kantoff PW, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363:411-22.
71. Dutoit V, et al. Dissecting TCR-MHC/peptide complex interactions with A2/peptide multimers incorporating tumor antigen peptide variants: crucial role of interaction kinetics on functional outcomes. Eur J Immunol. 2002;32:3285-93.
72. Klebanoff CA, et al. Therapeutic cancer vaccines: are we there yet? Immunol Rev. 2011;239:27-44.
73. McMahan RH, et al. Relating TCR-peptide-MHC affinity to immunogenicity for the design of tumor vaccines. J Clin Invest. 2006;116:2543-51.
74. Cole DK, et al. Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition. J Immunol. 2010;185:2600-10.
75. Kersh GJ, Allen PM. Structural basis for T cell recognition of altered peptide ligands: a single T cell receptor can productively recognize a large continuum of related ligands. J Exp Med. 1996;184:1259-68.
76. Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol. 1996;14:1-27.
77. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today. 1998;19:395-404.
78. Wooldridge L, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem. 2011;287:1168-77.
79. Parkhurst MR, et al. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A0201-binding residues. J Immunol. 1996;157:2539-48.
80. Borbulevych OY, et al. Increased immunogenicity of an anchor-modified tumor-associated antigen is due to the enhanced stability of the peptide/MHC complex: implications for vaccine design. J Immunol. 2005;174:4812-20.
81. Zaremba S, et al. Identification of an enhancer agonist cytotoxic T lymphocyte peptide from human carcinoembryonic antigen. Cancer Res. 1997;57:4570-7.
82. Salazar E, et al. Agonist peptide from a cytotoxic t-lymphocyte epitope of human carcinoembryonic antigen stimulates production of tc1-type cytokines and increases tyrosine phosphorylation more efficiently than cognate peptide. Int J Cancer. 2000;85:829-38.
83. Wasserman HA, et al. MHC variant peptide-mediated anergy of encephalitogenic T cells requires SHP-1. J Immunol. 2008;181:6843-9.
84. Katsara M, et al. The good, the bad and the ugly: how altered peptide ligands modulate immunity. Exp Opin Biol Ther. 2008;8:1873-84.
85. Tang Y, et al. An altered peptide ligand for naive cytotoxic T lymphocyte epitope of TRP-2(180-188) enhanced immunogenicity. Cancer Immunol Immunother. 2007;56:319-29.
86. Mimura K, et al. Substitution analog peptide derived from HER-2 can efficiently induce HER-2-specific, HLA-A24 restricted CTLs. Cancer Immunol Immunother. 2006;55:1358-66.
87. Iero M, et al. Modified peptides in anti-cancer vaccines: are we eventually improving anti-tumour immunity? Cancer Immunol Immunother. 2009;58:1159-67.
88. Clay TM, et al. Changes in the fine specificity of gp100(209-217)- reactive T cells in patients following vaccination with a peptide modified at an HLA-A2.1 anchor residue. J Immunol. 1999;162:1749-55.
89. Stuge TB, et al. Diversity and recognition efficiency of T cell responses to cancer. PLoS Med. 2004;1:e28.
90. Tynan FE, et al. A T cell receptor flattens a bulged antigenic peptide presented by a major histocompatibility complex class I molecule. Nat Immunol. 2007;8:268-76.
91. Tynan FE, et al. T cell receptor recognition of a 'super-bulged' major histocompatibility complex class I-bound peptide. Nat Immunol. 2005;6:1114-22.
92. Iero M, et al. Low TCR avidity and lack of tumor cell recognition in CD8(+) T cells primed with the CEA-analogue CAP1-6D peptide. Cancer Immunol Immunother. 2007;56:1979-91.
93. Speiser DE, et al. Unmodified self antigen triggers human CD8 T cells with stronger tumor reactivity than altered antigen. Proc Natl Acad Sci USA. 2008;105:3849-54.
94. Sharma AK, et al. Class I major histocompatibility complex anchor substitutions alter the conformation of T cell receptor contacts. J Biol Chem. 2001;276:21443-9.
95. Chen JL, et al. Ca2 + release from the endoplasmic reticulum of NY-ESO-1-specific T cells is modulated by the affinity of TCR and by the use of the CD8 coreceptor. J Immunol. 2010;184:1829-39.
96. Chen JL, et al. Structural and kinetic basis for heightened immunogenicity of T cell vaccines. J Exp Med. 2005;201:1243-55.
97. Pinilla-Ibarz J, et al. Improved human T-cell responses against synthetic HLA-0201 analog peptides derived from the WT1 oncoprotein. Leukemia. 2006;20:2025-33.
98. Borbulevych OY, Do P, Baker BM. Structures of native and affinity-enhanced WT1 epitopes bound to HLA-A0201: implications for WT1-based cancer therapeutics. Mol Immunol. 2010;47:2519-24.
99. Borbulevych OY, et al. Structures of MART-126/27-35 Peptide/HLA-A2 complexes reveal a remarkable disconnect between antigen structural homology and T cell recognition. J Mol Biol. 2007;372:1123-36.
100. Wieckowski S, et al. Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J Immunol. 2009;183:5397-406.
101. Dietrich PY, et al. TCR analysis reveals significant repertoire selection during in vitro lymphocyte culture. Int Immunol. 1997;9:1073-83.
102. Slansky JE, et al. Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. Immunity. 2000;13:529-38.
103. Jordan KR, et al. Peptide vaccines prevent tumor growth by activating T cells that respond to native tumor antigens. Proc Natl Acad Sci USA. 2010;107:4652-7.
104. Jordan KR, et al. Baculovirus-infected insect cells expressing peptide-MHC complexes elicit protective antitumor immunity. J Immunol. 2008;180:188-97.
105. Stone JD, Chervin AS, Kranz DM. T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology. 2009;126:165-76.
106. Corse E, et al. Attenuated T cell responses to a high-potency ligand in vivo. PLoS Biol. 2010;8(9):e1000481.
107. Jordan KR, et al. TCR hypervariable regions expressed by T cells that respond to effective tumor vaccines. Cancer Immunol Immunother. 2012;. doi: 10.1007/s00262-012-1217-5.
108. Crawford F, et al. Use of baculovirus MHC/peptide display libraries to characterize T-cell receptor ligands. Immunol Rev. 2006;210:156-70.
109. Crawford F, et al. Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity. 1998;8:675-82.
110. Pinilla C, et al. Combinatorial peptide libraries as an alternative approach to the identification of ligands for tumor-reactive cytolytic T lymphocytes. Cancer Res. 2001;61:5153-60.
111. Adams JJ, et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity. 2011;35:681-93.
112. Vetsika EK, et al. Sequential administration of the native TERT572 cryptic peptide enhances the immune response initiated by its optimized variant TERT(572Y) in cancer patients. J Immunother. 2011;34:641-50.
113. Rosenberg SA, et al. Altered CD8(+) T-cell responses when immunizing with multiepitope peptide vaccines. J Immunother. 2006;29:224-31.
114. Slingluff CL Jr, Engelhard VH, Ferrone S. Peptide and dendritic cell vaccines. Clin Cancer Res. 2006;12:2342s-5s.
115. Chauvin JM, et al. HLA anchor optimization of the melan-A-HLA-A2 epitope within a long peptide is required for efficient cross-priming of human tumor-reactive T cells. J Immunol. 2012;188:2102-10.
116. Slingluff CL Jr, 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.
117. Valmori D, et al. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J Immunol. 1998;160:1750-8.
118. Gross DA, et al. High vaccination efficiency of low-affinity epitopes in antitumor immunotherapy. J Clin Invest. 2004;113:425-33.
119. Keogh E, et al. Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-A0201-binding affinity. J Immunol. 2001;167:787-96.
120. Terasawa H, et al. Identification and characterization of a human agonist cytotoxic T-lymphocyte epitope of human prostate-specific antigen. Clin Cancer Res. 2002;8:41-53.
121. Andersen MH, et al. Identification of a cytotoxic T lymphocyte response to the apoptosis inhibitor protein survivin in cancer patients. Cancer Res. 2001;61:869-72.
122. Hou Y, Kavanagh B, Fong L. Distinct CD8 + T cell repertoires primed with agonist and native peptides derived from a tumor-associated antigen. J Immunol. 2008;180:1526-34.
123. Le Gal FA, et al. Distinct structural TCR repertoires in naturally occurring versus vaccine-induced CD8 + T-cell responses to the tumor-specific antigen NY-ESO-1. J Immunother. 2005;28:252-7.
124. Grabherr R, et al. Developments in the use of baculoviruses for the surface display of complex eukaryotic proteins. Trends Biotechnol. 2001;19:231-6.
125. Sakihama T, et al. A simple detection method for low-affinity membrane protein interactions by baculoviral display. PLoS One. 2008;3:e4024.