A study of T cell tolerance to the tumor-associated antigen MDM2: Cytokines can restore antigen responsiveness, but not high avidity T cell function

PLoS ONE

Volumn 2, Issue 4, 2007, Pages

  Bendle, Gavin M ^a   Xue, Shao An ^a   Holler, Angelika ^a   Stauss, Hans J ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 7; LEUKOSIALIN; PROTEIN BCL 2; PROTEIN MDM2; TUMOR ANTIGEN; MDM2 PROTEIN, MOUSE; PRIMER DNA;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CELL DIVISION; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOSTIMULATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE RECEPTOR GENE; ANIMAL; ANTIBODY AFFINITY; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; FLOW CYTOMETRY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; ANTIBODY AFFINITY; BASE SEQUENCE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; DNA PRIMERS; FLOW CYTOMETRY; IMMUNE TOLERANCE; MICE; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-MDM2; T-LYMPHOCYTES, CYTOTOXIC;

EID: 44849084026     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000353     Document Type: Article

References (44)

1. Boon T, van der Bruggen P (1996) Human tumor antigens recognized by T lymphocytes. J Exp Med 183: 725-729.
2. Rosenberg SA (2001) Progress in human tumour immunology and immunotherapy. Nature 411: 380-384.
3. Weber LW, Bowne WB, Wolchok JD, Srinivasan R, Qin J, et al. (1998) Tumor immunity and autoimmunity induced by immunization with homologous DNA. J Clin Invest 102: 1258-1264.
4. Pardoll DM (2002) Spinning molecular immunology into successful immunotherapy. Nat Rev Immunol 2: 227-238.
5. Overwijk WW, Lee DS, Surman DR, Irvine KR, Touloukian CE, et al. (1999) 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 96: 2982-2987.
6. Kisielow P, Bluthmann H, Staerz UD, Steinmetz M, von Boehmer H (1988) Tolerance in T-cell-receptor transgenic mice involves deletion of nonmature CD4+8+ thymocytes. Nature 333: 742-746.
7. Blackman M, Kappler J, Marrack P (1990) The role of the T cell receptor in positive and negative selection of developing T cells. Science 248: 1335-1341.
8. Lo D, Burkly LC, Widera G, Cowing C, Flavell RA, et al. (1988) Diabetes and tolerance in transgenic mice expressing class II MHC molecules in pancreatic beta cells. Cell 53: 159-168.
9. Morahan G, Allison J, Miller JF (1989) Tolerance of class I histocompatibility antigens expressed extrathymically. Nature 339: 622-624.
10. Schonrich G, Kalinke U, Momburg F, Malissen M, Schmitt-Verhulst AM, et al. (1991) Down-regulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction. Cell 65: 293-304.
11. Schonrich G, Momburg F, Malissen M, Schmitt-Verhulst AM, Malissen B, et al. (1992) Distinct mechanisms of extrathymic T cell tolerance due to differential expression of self antigen. Int Immunol 4: 581-590.
12. Otten GR, Germain RN (1991) Split anergy in a CD8+ T cell: receptor-dependent cytolysis in the absence of interleukin-2 production. Science 251: 1228-1231.
13. Tanchot C, Guillaume S, Delon J, Bourgeois C, Franzke A, et al. (1998) Modifications of CD8+ T cell function during in vivo memory or tolerance induction. Immunity 8: 581-590.
14. Li W, Whaley CD, Mondino A, Mueller DL (1996) Blocked signal transduction to the ERK and JNK protein kinases in anergic CD4+ T cells. Science 271: 1272-1276.
15. Ohashi PS, Oehen S, Buerki K, Pircher H, Ohashi CT, et al. (1991) Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65: 305-317.
16. Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA, et al. (2003) Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 198: 569-580.
17. Ohlen C, Kalos M, Cheng LE, Shur AC, Hong DJ, et al. (2002) CD8(+) T cell tolerance to a tumor-associated antigen is maintained at the level of expansion rather than effector function. J Exp Med 195: 1407-1418.
18. Momand J, Zambetti GP, Olson DC, George D, Levine AJ (1992) The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69: 1237-1245.
19. Trotta R, Vignudelli T, Candini O, Intine RV, Pecorari L, et al. (2003) BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 3: 145-160.
20. Oliner JD, Kinzler KW, Meltzer PS, George DL, Vogelstein B (1992) Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358: 80-83.
21. Bueso-Ramos CE, Yang Y, deLeon E, McCown P, Stass SA, et al. (1993) The human MDM-2 oncogene is overexpressed in leukemias. Blood 82: 2617-2623.
22. Ladanyi M, Cha C, Lewis R, Jhanwar SC, Huvos AG, et al. (1993) MDM2 gene amplification in metastatic osteosarcoma. Cancer Res 53: 16-18.
23. Reifenberger G, Liu L, Ichimura K, Schmidt EE, Collins VP (1993) Amplification and overexpression of the MDM2 gene in a subset of human malignant gliomas without p53 mutations. Cancer Res 53: 2736-2739.
24. Momand J, Wu HH, Dasgupta G (2000) MDM2-master regulator of the p53 tumor suppressor protein. Gene 242: 15-29.
25. Freedman DA, Levine AJ (1999) Regulation of the p53 protein by the MDM2 oncoprotein-thirty-eighth G.H.A. Clowes Memorial Award Lecture. Cancer Res 59: 1-7.
26. Stanislawski T, Voss RH, Lotz C, Sadovnikova E, Willemsen RA, et al. (2001) Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat Immunol 2: 962-970.
27. Sadovnikova E, Stauss HJ (1996) Peptide-specific cytotoxic T lymphocytes restricted by nonself major histocompatibility complex class I molecules: reagents for tumor immunotherapy. Proc Natl Acad Sci U S A 93: 13114-13118.
28. Bendle GM, Holler A, Pang LK, Hsu S, Krampera M, et al. (2004) Induction of unresponsiveness limits tumor protection by adoptively transferred MDM2-specific cytotoxic T lymphocytes. Cancer Res 64: 8052-8056.
29. Dahl AM, Beverley PC, Stauss HJ (1996) A synthetic peptide derived from the tumor-associated protein mdm2 can stimulate autoreactive, high avidity cytotoxic T lymphocytes that recognize naturally processed protein. J Immunol 157: 239-246.
30. Ljunggren HG, Karre K (1985) Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J Exp Med 162: 1745-1759.
31. Ljunggren HG, Stam NJ, Ohlen C, Neefjes JJ, Hoglund P, et al. (1990) Empty MHC class I molecules come out in the cold. Nature 346: 476-480.
32. McCoy JL, Fefer A, Glynn JP (1967) Comparative studies on the induction of transplantation resistance in BALB-c and C57BL-6 mice in three murine leukemia systems. Cancer Res 27: 1743-1748.
33. Sadovnikova E, Zhu X, Collins SM, Zhou J, Vousden K, et al. (1994) Limitations of predictive motifs revealed by cytotoxic T lymphocyte epitope mapping of the human papilloma virus E7 protein. Int Immunol 6: 289-296.
34. Heusel JW, Wesselschmidt RL, Shresta S, Russell JH, Ley TJ (1994) Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76: 977-987.
35. Trapani JA, Sutton VR (2003) Granzyme B: pro-apoptotic, antiviral and antitumor functions. Curr Opin Immunol 15: 533-543.
36. Harrington LE, Galvan M, Baum LG, Altman JD, Ahmed R (2000) Differentiating between Memory and Effector CD8 T cells by Altered Expression of Cell Surface O-Glycans. J Exp Med 191: 1241-1246.
37. + T cells. J Immunol 175: 5126-5134.
38. Alves NL, Arosa FA, van Lier RA (2005) IL-21 sustains CD28 expression on IL-15-activated human naive CD8+ T cells. J Immunol 175: 755-762.
39. Klebanoff CA, Finkelstein SE, Surman DR, Lichtman MK, Gattinoni L, et al. (2004) IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc Natl Acad Sci U S A 101: 1969-1974.
40. Bream JH, Hodge DL, Gonsky R, Spolski R, Leonard WJ, et al. (2004) A distal region in the interferon-gamma gene is a site of epigenetic remodeling and transcriptional regulation by interleukin-2. J Biol Chem 279: 41249-41257.
41. Zeng R, Spolski R, Finkelstein SE, Oh S, Kovanen PE, et al. (2005) Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med 201: 139-148.
42. Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, et al. (2003) Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med 9: 279-286.
43. Teague RM, Sather BD, Sacks JA, Huang MZ, Dossett ML, et al. (2006) Interleukin-15 rescues tolerant CD8+ T cells for use in adoptive immunotherapy of established tumors. Nat Med 12: 335-341.
44. Rosenberg SA, Dudley ME (2004) Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes. Proc Natl Acad Sci U S A 101 Suppl 2: 14639-14645.