Stimulation of tumor-reactive T lymphocytes using mixtures of synthetic peptides derived from tumor-associated antigens with diverse MHC binding affinities

Journal of Immunological Methods

Volumn 276, Issue 1-2, 2003, Pages 103-119

  Riley, John P ^a   Rosenberg, Steven A ^a   Parkhurst, Maria R ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cancer; Immunotherapy; MHC binding affinity; Peptides; Reverse immunology; T lymphocytes; Tumor associated antigen

Indexed keywords

EPITOPE; GLYCOPROTEIN GP 100; HLA A ANTIGEN; SYNTHETIC PEPTIDE; TUMOR ANTIGEN; TYROSINASE RELATED PROTEIN 2;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BLOOD DONOR; CONCENTRATION RESPONSE; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MASS SPECTROMETRY; MELANOMA CELL; NONHUMAN; PEPTIDE SYNTHESIS; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; RAT; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; T LYMPHOCYTE ACTIVATION;

ANIMALIA;

EID: 0037407511     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-1759(03)00078-4     Document Type: Article

References (71)

1. Arai J., Yasukawa M., Ohminami H., Kakimoto M., Hasegawa A., Fujita S. Identification of human telomerase reverse transcriptase-derived peptides that induce HLA-A24-restricted antileukemia cytotoxic T lymphocytes. Blood. 97(9):2001;2903-2907.
2. Bakker A.B., Schreurs M.W., de Boer A.J., Kawakami Y., Rosenberg S.A., Adema G.J., Figdor C.G. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J. Exp. Med. 179(3):1994;1005-1009.
3. Bakker A.B., Schreurs M.W., Tafazzul G., de Boer A.J., Kawakami Y., Adema G.J., Figdor C.G. Identification of a novel peptide derived from the melanocyte-specific gp100 antigen as the dominant epitope recognized by an HLA-A2.1-restricted anti-melanoma CTL line. Int. J. Cancer. 62(1):1995;97-102.
4. Berard F., Blanco P., Davoust J., Neidhart-Berard E.M., Nouri-Shirazi M., Taquet N., Rimoldi D., Cerottini J.C., Banchereau J., Palucka A.K. Cross-priming of naive CD8 T cells against melanoma antigens using dendritic cells loaded with killed allogeneic melanoma cells. J. Exp. Med. 192(11):2000;1535-1544.
5. Boczkowski D., Nair S.K., Nam J.H., Lyerly H.K., Gilboa E. Induction of tumor immunity and cytotoxic T lymphocyte responses using dendritic cells transfected with messenger RNA amplified from tumor cells. Cancer Res. 60(4):2000;1028-1034.
6. Boehncke W.H., Takeshita T., Pendleton C.D., Houghten R.A., Sadegh-Nasseri S., Racioppi L., Berzofsky J.A., Germain R.N. The importance of dominant negative effects of amino acid side chain substitution in peptide-MHC molecule interactions and T cell recognition. J. Immunol. 150(2):1993;331-341.
7. Boon T., Coulie P.G., Van den E.B. Tumor antigens recognized by T cells. Immunol. Today. 18(6):1997;267-268.
8. Butterfield L.H., Jilani S.M., Chakraborty N.G., Bui L.A., Ribas A., Dissette V.B., Lau R., Gamradt S.C., Glaspy J.A., McBride W.H., Mukherji B., Economou J.S. Generation of melanoma-specific cytotoxic T lymphocytes by dendritic cells transduced with a MART-1 adenovirus. J. Immunol. 161(10):1998;5607-5613.
9. Butterfield L.H., Koh A., Meng W., Vollmer C.M., Ribas A., Dissette V., Lee E., Glaspy J.A., McBride W.H., Economou J.S. Generation of human T-cell responses to an HLA-A2.1-restricted peptide epitope derived from alpha-fetoprotein. Cancer Res. 59(13):1999;3134-3142.
10. Chen W., Khilko S., Fecondo J., Margulies D.H., McCluskey J. Determinant selection of major histocompatibility complex class I-restricted antigenic peptides is explained by class I-peptide affinity and is strongly influenced by nondominant anchor residues. J. Exp. Med. 180(4):1994;1471-1483.
11. Chen Y.T., Scanlan M.J., Sahin U., Tureci O., Gure A.O., Tsang S., Williamson B., Stockert E., Pfreundschuh M., Old L.J. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. U. S. A. 94(5):1997;1914-1918.
12. Cox A.L., Skipper J., Chen Y., Henderson R.A., Darrow T.L., Shabanowitz J., Engelhard V.H., Hunt D.F., Slingluff C.L. Jr. Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines. Science. 264:1994;716-719.
13. Dong T., Boyd D., Rosenberg W., Alp N., Takiguchi M., McMichael A., Rowland-Jones S. An HLA-B35-restricted epitope modified at an anchor residue results in an antagonist peptide. Eur. J. Immunol. 26(2):1996;335-339.
14. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., Topalian S.L., Sherry R., Restifo N.P., Hubicki A.M., Robinson M.R., Raffeld M., Duray P., Seipp C.A., Rogers-Freezer L., Morton K.E., Mavroukakis S.A., White D.E., Rosenberg S.A. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science. 298:2002;850-854.
15. Dyall R., Bowne W.B., Weber L.W., LeMaoult J., Szabo P., Moroi Y., Piskun G., Lewis J.J., Houghton A.N., Nikolic-Zugic J. Heteroclitic immunization induces tumor immunity. J. Exp. Med. 188(9):1998;1553-1561.
16. Eder J.P., Kantoff P.W., Roper K., Xu G.X., Bubley G.J., Boyden J., Gritz L., Mazzara G., Oh W.K., Arlen P., Tsang K.Y., Panicali D., Schlom J., Kufe D.W. A phase I trial of a recombinant vaccinia virus expressing prostate-specific antigen in advanced prostate cancer. Clin. Cancer Res. 6(5):2000;1632-1638.
17. Firat H., Zennou V., Garcia-Pons F., Ginhoux F., Cochet M., Danos O., Lemonnier F.A., Langlade-Demoyen P., Charneau P. Use of a lentiviral flap vector for induction of CTL immunity against melanoma. Perspectives for immunotherapy. J. Gene Med. 4(1):2002;38-45.
18. Graff-Dubois S., Faure O., Gross D.A., Alves P., Scardino A., Chouaib S., Lemonnier F.A., Kosmatopoulos K. Generation of CTL recognizing an HLA-A*0201-restricted epitope shared by MAGE-A1, -A2, -A3, -A4, -A6, -A10, and -A12 tumor antigens: implication in a broad-spectrum tumor immunotherapy. J. Immunol. 169(1):2002;575-580.
19. Harada M., Li Y.F., El Gamil M., Rosenberg S.A., Robbins P.F. Use of an in vitro immunoselected tumor line to identify shared melanoma antigens recognized by HLA-A*0201-restricted T cells. Cancer Res. 61(3):2001;1089-1094.
20. Houghton A.N. Cancer antigens: immune recognition of self and altered self. J. Exp. Med. 180(1):1994;1-4.
21. Hunt D.F., Henderson R.A., Shabanowitz J., Sakaguchi K., Michel H., Sevilir N., Cox A.L., Appella E., Engelhard V.H. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science. 255:1992;1261-1263.
22. Kawakami Y., Rosenberg S.A. T-cell recognition of self peptides as tumor rejection antigens. Immunol. Res. 15(3):1996;179-190.
23. Kawakami Y., Eliyahu S., Jennings C., Sakaguchi K., Kang X., Southwood S., Robbins P.F., Sette A., Appella E., Rosenberg S.A. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol. 154(8):1995;3961-3968.
24. Kawakami Y., Robbins P.F., Wang X., Tupesis J.P., Parkhurst M.R., Kang X., Sakaguchi K., Appella E., Rosenberg S.A. Identification of new melanoma epitopes on melanosomal proteins recognized by tumor infiltrating T lymphocytes restricted by HLA-A1,- A2, and -A3 alleles. J. Immunol. 161(12):1998;6985-6992.
25. Kawashima I., Hudson S.J., Tsai V., Southwood S., Takesako K., Appella E., Sette A., Celis E. The multi-epitope approach for immunotherapy for cancer: identification of several CTL epitopes from various tumor-associated antigens expressed on solid epithelial tumors. Hum. Immunol. 59(1):1998;1-14.
26. Khong H.T., Rosenberg S.A. Pre-existing immunity to tyrosinase-related protein (TRP)-2, a new TRP-2 isoform, and the NY-ESO-1 melanoma antigen in a patient with a dramatic response to immunotherapy. J. Immunol. 168(2):2002;951-956.
27. La Rosa C., Krishnan R., Markel S., Schneck J.P., Houghten R., Pinilla C., Diamond D.J. Enhanced immune activity of cytotoxic T-lymphocyte epitope analogs derived from positional scanning synthetic combinatorial libraries. Blood. 97(6):2001;1776-1786.
28. Lawendowski C.A., Giurleo G.M., Huang Y.Y., Franklin G.J., Kaplan J.M., Roberts B.L., Nicolette C.A. Solid-phase epitope recovery: a high throughput method for antigen identification and epitope optimization. J. Immunol. 169(5):2002;2414-2421.
29. Linette G.P., Shankara S., Longerich S., Yang S., Doll R., Nicolette C., Preffer F.I., Roberts B.L., Haluska F.G. In vitro priming with adenovirus/gp100 antigen-transduced dendritic cells reveals the epitope specificity of HLA-A*0201-restricted CD8+ T cells in patients with melanoma. J. Immunol. 164(6):2000;3402-3412.
30. Liotta L., Petricoin E. Molecular profiling of human cancer. Nat. Rev. Genet. 1(1):2000;48-56.
31. Marshall J.L., Hawkins M.J., Tsang K.Y., Richmond E., Pedicano J.E., Zhu M.Z., Schlom J. Phase I study in cancer patients of a replication-defective avipox recombinant vaccine that expresses human carcinoembryonic antigen. J. Clin. Oncol. 17(1):1999;332-337.
32. Marshall J.L., Hoyer R.J., Toomey M.A., Faraguna K., Chang P., Richmond E., Pedicano J.E., Gehan E., Peck R.A., Arlen P., Tsang K.Y., Schlom J. Phase I study in advanced cancer patients of a diversified prime-and-boost vaccination protocol using recombinant vaccinia virus and recombinant nonreplicating avipox virus to elicit anti-carcinoembryonic antigen immune responses. J. Clin. Oncol. 18(23):2000;3964-3973.
33. Moudgil K.D., Sercarz E.E. Can antitumor immune responses discriminate between self and nonself? Immunol. Today. 15(8):1994;353-355.
34. Moudgil K.D., Ametani A., Grewal I.S., Kumar V., Sercarz E.E. Processing of self-proteins and its impact on shaping the T cell repertoire, autoimmunity and immune regulation. Int. Rev. Immunol. 10(4):1993;365-377.
35. Nestle F.O., Alijagic S., Gilliet M., Sun Y., Grabbe S., Dummer R., Burg G., Schadendorf D. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat. Med. 4(3):1998;328-332.
36. Noppen C., Levy F., Burri L., Zajac P., Remmel E., Schaefer C., Luscher U., Heberer M., Spagnoli G.C. Naturally processed and concealed HLA-A2.1-restricted epitopes from tumor-associated antigen tyrosinase-related protein-2. Int. J. Cancer. 87(2):2000;241-246.
37. Ohno S. How cytotoxic T cells manage to discriminate nonself from self at the nonapeptide level. Proc. Natl. Acad. Sci. U. S. A. 89(10):1992;4643-4647.
38. Parker K.C., Bednarek M.A., Coligan J.E. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152(1):1994;163-175.
39. Parkhurst M.R., Salgaller M.L., Southwood S., Robbins P.F., Sette A., Rosenberg S.A., Kawakami Y. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J. Immunol. 157(6):1996;2539-2548.
40. Parkhurst M.R., Fitzgerald E.B., Southwood S., Sette A., Rosenberg S.A., Kawakami Y. Identification of a shared HLA-A*0201-restricted T-cell epitope from the melanoma antigen tyrosinase-related protein 2 (TRP2). Cancer Res. 58(21):1998;4895-4901.
41. Rammensee H., Bachmann J., Emmerich N.P., Bachor O.A., Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics. 50(3-4):1999;213-219.
42. Reeves M.E., Royal R.E., Lam J.S., Rosenberg S.A., Hwu P. Retroviral transduction of human dendritic cells with a tumor-associated antigen gene. Cancer Res. 56(24):1996;5672-5677.
43. Restifo N.P., Ying H., Hwang L., Leitner W.W. The promise of nucleic acid vaccines. Gene Ther. 7(2):2000;89-92.
44. Riley J.P., Rosenberg S.A., Parkhurst M.R. Identification of a new shared HLA-A2.1 restricted epitope from the melanoma antigen tyrosinase. J. Immunother. 24(3):2001;212-220.
45. Rosenberg S.A. A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity. 10(3):1999;281-287.
46. Rosenberg S.A., Yang J.C., Schwartzentruber D.J., Hwu P., Marincola F.M., Topalian S.L., Restifo N.P., Dudley M.E., Schwarz S.L., Spiess P.J., Wunderlich J.R., Parkhurst M.R., Kawakami Y., Seipp C.A., Einhorn J.H., White D.E. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 4(3):1998;321-327.
47. Rosenberg S.A., Zhai Y., Yang J.C., Schwartzentruber D.J., Hwu P., Marincola F.M., Topalian S.L., Restifo N.P., Seipp C.A., Einhorn J.H., Roberts B., White D.E. Immunizing patients with metastatic melanoma using recombinant adenoviruses encoding MART-1 or gp100 melanoma antigens. J. Natl. Cancer Inst. 19(24):1998;1894-1900.
48. Rughetti A., Biffoni M., Sabbatucci M., Rahimi H., Pellicciotta I., Fattorossi A., Pierelli L., Scambia G., Lavitrano M., Frati L., Nuti M. Transfected human dendritic cells to induce antitumor immunity. Gene Ther. 7(17):2000;1458-1466.
49. Salazar-Onfray F., Nakazawa T., Chhajlani V., Petersson M., Karre K., Masucci G., Celis E., Sette A., Southwood S., Appella E., Kiessling R. Synthetic peptides derived from the melanocyte-stimulating hormone receptor MC1R can stimulate HLA-A2-restricted cytotoxic T lymphocytes that recognize naturally processed peptides on human melanoma cells. Cancer Res. 57(19):1997;4348-4355.
50. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science. 270:1995;467-470.
51. Schroers R., Huang X.F., Hammer J., Zhang J., Chen S.Y. Identification of HLA DR7-restricted epitopes from human telomerase reverse transcriptase recognized by CD4+ T-helper cells. Cancer Res. 62(9):2002;2600-2605.
52. Sercarz E.E., Lehmann P.V., Ametani A., Benichou G., Miller A., Moudgil K. Dominance and crypticity of T cell antigenic determinants. Annu. Rev. Immunol. 11:1993;729-766.
53. Sette A., Vitiello A., Reherman B., Fowler P., Nayersina R., Kast W.M., Melief C.J., Oseroff C., Yuan L., Ruppert J. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol. 153(12):1994;5586-5592.
54. Sharma A.K., Kuhns J.J., Yan S., Friedline R.H., Long B., Tisch R., Collins E.J. Class I major histocompatibility complex anchor substitutions alter the conformation of T cell receptor contacts. J. Biol. Chem. 276(24):2001;21443-21449.
55. Shen Z., Reznikoff G., Dranoff G., Rock K.L. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158(6):1997;2723-2730.
56. Skipper J.C., Gulden P.H., Hendrickson R.C., Harthun N., Caldwell J.A., Shabanowitz J., Engelhard V.H., Hunt D.F., Slingluff C.L. Jr. Mass-spectrometric evaluation of HLA-A*0201-associated peptides identifies dominant naturally processed forms of CTL epitopes from MART-1 and gp100. Int. J. Cancer. 82(5):1999;669-677.
57. Strobel I., Krumbholz M., Menke A., Hoffmann E., Dunbar P.R., Bender A., Hobom G., Steinkasserer A., Schuler G., Grassmann R. Efficient expression of the tumor-associated antigen MAGE-3 in human dendritic cells, using an avian influenza virus vector. Hum. Gene Ther. 11(16):2000;2207-2218.
58. Sun Y., Song M., Stevanovic S., Jankowiak C., Paschen A., Rammensee H.G., Schadendorf D. Identification of a new HLA-A(*)0201-restricted T-cell epitope from the tyrosinase-related protein 2 (TRP2) melanoma antigen. Int. J. Cancer. 87(3):2000;399-404.
59. Surman D.R., Dudley M.E., Overwijk W.W., Restifo N.P. Cutting edge: CD4+ T cell control of CD8+ T cell reactivity to a model tumor antigen. J. Immunol. 164(2):2000;562-565.
60. Szabolcs P., Gallardo H.F., Ciocon D.H., Sadelain M., Young J.W. Retrovirally transduced human dendritic cells express a normal phenotype and potent T-cell stimulatory capacity. Blood. 90(6):1997;2160-2167.
61. Touloukian C.E., Leitner W.W., Topalian S.L., Li Y.F., Robbins P.F., Rosenberg S.A., Restifo N.P. Identification of a MHC class II-restricted human gp100 epitope using DR4-IE transgenic mice. J. Immunol. 164(7):2000;3535-3542.
62. Tsai V., Southwood S., Sidney J., Sakaguchi K., Kawakami Y., Appella E., Sette A., Celis E. Identification of subdominant CTL epitopes of the GP100 melanoma-associated tumor antigen by primary in vitro immunization with peptide-pulsed dendritic cells. J. Immunol. 158(4):1997;1796-1802.
63. Velculescu V.E., Zhang L., Vogelstein B., Kinzler K.W. Serial analysis of gene expression. Science. 270:1995;484-487.
64. Vissers J.L., De Vries I.J., Schreurs M.W., Engelen L.P., Oosterwijk E., Figdor C.G., Adema G.J. The renal cell carcinoma-associated antigen G250 encodes a human leukocyte antigen (HLA)-A2.1-restricted epitope recognized by cytotoxic T lymphocytes. Cancer Res. 59(21):1999;5554-5559.
65. Vissers J.L., De Vries I.J., Engelen L.P., Scharenborg N.M., Molkenboer J., Figdor C.G., Oosterwijk E., Adema G.J. Renal cell carcinoma-associated antigen G250 encodes a naturally processed epitope presented by human leukocyte antigen-DR molecules to CD4(+) T lymphocytes. Int. J. Cancer. 100(4):2002;441-444.
66. Vonderheide R.H., Hahn W.C., Schultze J.L., Nadler L.M. The telomerase catalytic subunit is a widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity. 10(6):1999;673-679.
67. Vonderheide R.H., Anderson K.S., Hahn W.C., Butler M.O., Schultze J.L., Nadler L.M. Characterization of HLA-A3-restricted cytotoxic T lymphocytes reactive against the widely expressed tumor antigen telomerase. Clin. Cancer Res. 7(11):2001;3343-3348.
68. Walter E.A., Greenberg P.D., Gilbert M.J., Finch R.J., Watanabe K.S., Thomas E.D., Riddell S.R. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N. Engl. J. Med. 333(16):1995;1038-1044.
69. Wen Y.J., Min R., Tricot G., Barlogie B., Yi Q. Tumor lysate-specific cytotoxic T lymphocytes in multiple myeloma: promising effector cells for immunotherapy. Blood. 99(9):2002;3280-3285.
70. Yee C., Gilbert M.J., Riddell S.R., Brichard V.G., Fefer A., Thompson J.A., Boon T., Greenberg P.D. Isolation of tyrosinase-specific CD8+ and CD4+ T cell clones from the peripheral blood of melanoma patients following in vitro stimulation with recombinant vaccinia virus. J. Immunol. 157(9):1996;4079-4086.
71. Zhou Y., Bosch M.L., Salgaller M.L. Current methods for loading dendritic cells with tumor antigen for the induction of antitumor immunity. J. Immunother. 25(4):2002;289-303.