In vivo ligation of CD40 enhances priming against the endogenous tumor antigen and promotes CD8+ T cell effector function in SV40 T antigen transgenic mice

Journal of Immunology

Volumn 171, Issue 2, 2003, Pages 697-707

  Staveley O'Carroll, Kevin ^a   Schell, Todd D ^a   Jimenez, Marcela ^a   Mylin, Lawrence M ^a,c   Tevethia, M Judith ^a   Schoenberger, Stephen P ^b   Tevethia, Satvir S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c MESSIAH COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLASE; CD40 ANTIGEN; CD8 ANTIGEN; EPITOPE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD40; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR I; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VIRUS LARGE T ANTIGEN;

ADOLESCENT; ADOPTIVE TRANSFER; ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CELL FUNCTION; CELLULAR IMMUNITY; EFFECTOR CELL; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; MOUSE STRAIN LINE 501; NONHUMAN; OSTEOSARCOMA; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TUMOR IMMUNITY;

EID: 0038446044     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.2.697     Document Type: Article

References (73)

1. Boon, T., and P. van der Bruggen. 1996. Human tumor antigens recognized by T lymphocytes. J. Exp. Med. 183:725.
2. Wang, R. F., and S. A. Rosenberg. 1996. Human tumor antigens recognized by T lymphocytes: implications for cancer therapy. J. Leukocyte Biol. 60:296.
3. Theobald, M., J. Biggs, J. Hernandez, J. Lustgarten, C. Labadie, and L. A. Sherman. 1997. Tolerance to p53 by A2.1-restricted cytotoxic T lymphocytes. J. Exp. Med. 185:833.
4. Schell, T. D., L. M. Mylin, I. Georgoff, A. K. Teresky, A. J. Levine, and S. S. Tevethia. 1999. Cytotoxic T-lymphocyte epitope immunodominance in the control of choroid plexus tumors in simian virus 40 large T antigen transgenic mice. J. Virol. 73:5981.
5. Colella, T. A., T. N. Bullock, L. B. Russell, D. W, Mullins, W. W. Overwijk, C. J. Luckey, R. A. Pierce, N. P. Restifo, and V. H. Engelhard. 2000. Self-tolerance to the murine homologue of a tyrosinase-derived melanoma antigen: implications for tumor immunotherapy. J. Exp. Med. 191:1221.
6. Zheng, X., J. X. Gao, H. Zhang, T. L. Geiger, Y. Liu, and P. Zheng. 2002. Clonal deletion of simian virus 40 large T antigen-specific T cells in the transgenic adenocarcinoma of mouse prostate mice: an important role for clonal deletion in shaping the repertoire of T cells specific for antigens overexpressed in solid tumors. J. Immunol. 169:4761.
7. Stockinger, B. 1999. T lymphocyte tolerance: from thymic deletion to peripheral control mechanisms. Adv. Immunol. 71:229.
8. Heath. W. R., and F. R, Carbone. 2001. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 19:47.
9. Brinster, R. L., H. Y. Chen, A. Messing, T. van Dyke, A. J. Levine, and R. D. Palmiter. 1984. Transgenic mice harboring SV40 T-antigen genes develop characteristic brain tumors. Cell 37:367.
10. Palmiter, R. D., H. Y. Chen, A. Messing, and R. L. Brinster. 1985. SV40 enhancer and large-T antigen are instrumental in development of choroid plexus tumors in transgenic mice. Nature 316:457.
11. Butel, J. S., and J. A. Lednicky. 1999. Cell and molecular biology of simian virus 40: implications for human infections and disease. J. Natl. Cancer Inst. 91:119.
12. Tevethia, S. S., and T. D. Schell. 2001. The immune response to SV40. JCV and BKV. In Human Polyomaviruses: Molecular and Clinical Perspectives. K. Khalili, and G. L. Stoner, eds. Wiley-Liss, New York, p. 585.
13. b-restricted cytotoxic T-lymphocyte recognition epitopes in simian virus 40 T antigen. J. Virol. 66:440.
14. b-restricted cytotoxic T lymphocyte epitopes within simian virus 40 T antigen. J. Virol. 69:6665.
15. b-restricted determinant in simian virus 40 tumor antigen. Virology 208:159.
16. Faas, S. J., S. Pan, C. A. Pinkert, R. L. Brinster, and B. B. Knowles. 1987. Simian virus 40 (SV40)-transgenic mice that develop tumors are specifically tolerant to SV40 T antigen. J. Exp. Med. 165:417.
17. Jolicoeur, C., D. Hanahan, and K. M. Smith. 1994. T cell tolerance towards a transgenic β-cell antigen and transcription of endogenous pancreatic genes in the thymus. Proc. Natl. Acad. Sci. USA 91:6707.
18. Antonia, S. J., T. Geiger, J. Miller, and R. A. Flavell. 1995. Mechanisms of immune tolerance induction through the thymic expression of a peripheral tissue-specific protein. Int. Immunol. 7:715.
19. Schell, T. D., B. B. Knowles, and S. S. Tevethia. 2000. Sequential loss of cytotoxic T lymphocyte responses to simian virus 40 large T antigen epitopes in T antigen transgenic mice developing osteosarcomas. Cancer Res. 60:3002.
20. Knowles, B. B., J. McCarrick, N. Fox, D. Solter, and I. Damjanov. 1990. Osteosarcomas in transgenic mice expressing an α-amylase-SV40 T-antigen hybrid gene. Am. J. Pathol. 137:259.
21. Marton, I., S. E. Johnson, I. Damjanov, K. S. Currier, J. P. Sundberg, and B. B. Knowles. 2000. Expression and immune recognition of SV40 Tag in transgenic mice that develop metastatic osteosarcomas. Transgenic Res. 9:115.
22. Oehen, S. U., P. S. Ohashi, K. Burki, H. Hengartner, R. M. Zinkernagel, and P. Aichele. 1994. Escape of thymocytes and mature T cells from clonal deletion due to limiting tolerogen expression levels. Cell. Immunol. 158:342.
23. Ochsenbein, A. F., S. Sierro, B. Odermatt, M. Pericin, U. Karrer, J. Hermans, S. Hemmi, H. Hengartner. and R. M. Zinkernagel. 2001. Roles of tumour localization, second signals and cross priming in cytotoxic T-cell induction. Nature 411:1058.
24. Scheinecker, C., R. McHugh, E. M. Shevach, and R. N. Germain, 2002. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 196:1079.
25. Ohashi, P. S., S. Oehen, K. Buerki, H. Pircher, C. T. Ohashi, B. Odermatt, B. Malissen, R. M. Zinkernagel, and H. Hengartner. 1991. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65:305.
26. Soldevila, G., T. Geiger, and R. A. Flavell. 1995. Breaking immunologic ignorance to an antigenic peptide of simian virus 40 large T antigen. J. Immunol. 155:5590.
27. Ye, X., J. McCarrick, L. Jewett, and B. B. Knowles. 1994. Timely immunization subverts the development of peripheral nonresponsiveness and suppresses tumor development in simian virus 40 tumor antigen-transgenic mice. Proc. Natl. Acad. Sci. USA 91:3916.
28. + T cells. J. Exp. Med. 186:239.
29. Staveley-O'Carroll, K., E. Sotomayor, J. Montgomery, I. Borrello, L. Hwang, S. Fein, D. Pardoll, and H. Levitsky. 1998. Induction of antigen-specific T cell anergy: an early event in the course of tumor progression. Proc. Natl. Acad. Sci. USA 95:1178.
30. Morgan, D. J., C. Kurts, H. T. Kreuwel, K. L. Holst, W. R. Heath, and L. A. Sherman. 1999. Ontogeny of T cell tolerance to peripherally expressed antigens. Proc. Natl. Acad. Sci. USA 96:3854.
31. Mellman, I., and R. M. Steinman. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255.
32. + T cell tolerance to parenchymal self-antigens requires presentation by bone marrow-derived antigen-presenting cells. J. Exp. Med. 187:1555.
33. - dendritic cells cross-prime cytotoxic T cells In vivo. J. Exp. Med. 192:1685.
34. + dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 196:1099.
35. Huang, F. P., N. Platt, M. Wykes, J. R. Major, T. J. Powell, C. D. Jenkins, and G. G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435.
36. Kurts, C., R. M. Sutherland, G. Davey, M. Li, A. M. Lew, E. Blanas, F. R. Carbone, J. F. Miller, and W. R. Heath. 1999. CD8 T cell ignorance or tolerance to islet antigens depends on antigen dose. Proc. Natl. Acad. Sci. USA 96:12703.
37. + T cell tolerance to peripherally expressed antigens. J. Immunol. 163:723.
38. Grewal, I. S., and R. A. Flavell. 1998. CD40 and CD154 in cell-mediated immunity. Annu. Rev. Immunol. 16:111.
39. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184:747.
40. Koch, F., U. Stanzl, P. Jennewein. K. Janke, C. Heufler, E. Kampgen, N. Romani, and G. Schuler. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med 184:741.
41. Schulz, O., A. D. Edwards, M. Schito, J. Aliberti, S. Manickasingham, A. Sher, and C. Reis e Sousa. 2000. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 13:453.
42. Moodycliffe, A. M., V. Shreedhar, S. E. Ullrich, J. Walterscheid, C. Bucana, M. L. Kripke, and L. Flores-Romo. 1999. CD40-CD40 ligand interactions in vivo regulate migration of antigen-bearing dendritic cells from the skin to draining lymph nodes. J. Exp. Med. 191:2011.
43. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480.
44. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393:478.
45. + T-helper and a T-killer cell. Nature 393:474.
46. Diehl, L., A. T. den Boer, S. P. Schoenberger, E. I. van der Voort, T. N. Schumacher, C. J. Melief, R. Offringa, and R. E. Toes. 1999. CD40 activation in vivo overcomes peptide-induced peripheral cytotoxic T-lymphocyte tolerance and augments anti-tumor vaccine efficacy. Nat. Med. 5:774.
47. + T-cell tolerance to T-cell priming through in vivo ligation of CD40. Nat. Med. 5:780.
48. + T cell tolerance. J. Exp. Med. 196:1627.
49. van Mierlo, G. J. D., A. T. den Boer, J. P. Medema, E. I. H. van der Voort, M. F. Fransen, R. Offringa, C. J. M. Melief. and R. E. M. Toes. 2002. CD40 stimulation leads to effective therapy of CD40-tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc. Natl. Acad. Sci. USA 99:5561.
50. + T cells in the absence of tumor-antigen vaccination. Proc. Natl. Acad. Sci. USA 98:10811.
51. Nguyen, L. T., A. R. Elford, K. Murakami, K. M. Garza, S. P. Schoenberger, B. Odermatt, D. E. Speiser, and P. S. Ohashi. 2002. Tumor growth enhances cross-presentation leading to limited T cell activation without tolerance. J. Exp. Med. 195:423.
52. Tanaka, Y., M. J. Tevethia, D. Kalderon, A. E. Smith, and S. S. Tevethia. 1988. Clustering of antigenic sites recognized by cytotoxic T lymphocyte clones in the amino terminal half of SV40 T antigen. Virology 162:427.
53. Saito, H., D. M. Kranz, Y. Takagaki, A. C. Hayday, H. N. Eisen, and S. Tonegawa. 1984. A third rearranged and expressed gene in a clone of cytotoxic T lymphocytes. Nature 312:36.
54. Gascoigne, N. R., Y. Chien, D. M. Becker, J. Kavaler, and M. M. Davis. 1984. Genomic organization and sequence of T-cell receptor β-chain constant- and joining-region genes. Nature 310:387.
55. Chen, F., L. Rowen, L. Hood, and E. V. Rothenberg. 2001. Differential transcriptional regulation of individual TCR Vβ segments before gene rearrangement. J. Immunol. 166:1771.
56. Koop, B. F., R. K. Wilson, K. Wang, B. Vemooij, D. Zallwer, C. L. Kuo, D. Seto, M. Toda, and L. Hood. 1992. Organization, structure, and function of 95 kb of DNA spanning the murine T-cell receptor Cα/Cδ region. Genomics 13:1209.
57. Kouskoff, V., K. Signorelli, C. Benoist, and D. Mathis. 1995. Cassette vectors directing expression of T cell receptor genes in transgenic mice. J. Immunol. Methods 180:273.
58. Tevethia, M. J., R. H. Bonneau, J. W. Griffith, and L. Mylin. 1997. A simian virus 40 large T-antigen segment containing amino acids 1 to 127 and expressed under the control of the rat elastase-1 promoter produces pancreatic acinar carcinomas in transgenic mice. J. Virol. 71:8157.
59. Kastan, M. B., Q. Zhan, W. S. el-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fomace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxiatelangiectasia. Cell 71:587.
60. Sim, B. C., L. Zerva, M. I. Greene, and N. R. Gascoigne. 1996. Control of MHC restriction by TCR Vα CDR1 and CDR2. Science 273:963.
61. + T-lymphocyte responses to multiple epitopes from simian virus 40 (SV40) large T antigen in C57BL/6 mice immunized with SV40, SV40 T-antigen-transformed cells, or vaccinia virus recombinants expressing full-length T antigen or epitope minigenes. J. Virol. 74:6922.
62. Rolink, A., F. Melchers, and J. Andersson. 1996. The SCID but not the RAG-2 gene product is required for Sμ-Sε heavy chain class switching. Immunity. 5:319.
63. Lyons, A. B., and C. R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171:131.
64. Fulcher, D. A., A. B. Lyons, S. L. Korn, M. C. Cook, C. Koleda, C. Parish, B. Fazekas de St Groth, and A. Basten. 1996. The late of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of T cell help. J. Exp. Med. 183:2313.
65. Caux, C., C. Massacrier, B. Vanbervliet, B. Dubois, C. Van Kooten, I. Durand, and J. Banchereau. 1994. Activation of human dendritic cells through CD40 cross-linking. J. Exp. Med. 180:1263.
66. + T cells undergoing peripheral deletion in response to cross-presentation of self-antigen. J. Exp. Med. 194:707.
67. Diehl, L., A. T. Den Boer, E. I. van der Voort, C. J. Melief, R. Offringa, and R. E. Toes, 2000. The role of CD40 in peripheral T cell tolerance and immunity. J. Mol. Med. 78:363.
68. Liu, K., T. Iyoda, M. Saternus, Y, Kimura, K. Inaba, and R. M. Steinman. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 196:1091.
69. + T cells responding to self-antigens. J, Exp. Med. 196:323.
70. Geiger, T., G. Soldevila, and R. A. Flavell. 1993. T cells are responsive to the simian virus 40 large tumor antigen transgenically expressed in pancreatic islets. J. Immunol. 151:7030.
71. Mauri, C., L. T. Mars, and M. Londei. 2000. Therapeutic activity of agonistic monoclonal antibodies against CD40 in a chronic autoimmune inflammatory process. Nat. Med. 6:673.
72. Higgins, A. D., M. A. Mihalyo, and A. J. Adler. 2002. Effector CD4 cells are tolerized upon exposure to parenchymal self-antigen. J. Immunol. 169:3622.
73. + T cells undergo peripheral tolerance. Immunity 17:73.