CTLA-4 ablation and interleukin-12-driven differentiation synergistically augment cardiac pathogenicity of cytotoxic T lymphocytes

Circulation Research

Volumn 101, Issue 3, 2007, Pages 248-257

  Love, Victoria A ^a   Grabie, Nir ^a   Duramad, Paurene ^a   Stavrakis, George ^a   Sharpe, Arlene ^b   Lichtman, Andrew ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

CTLA 4; Cytotoxic T lymphocytes; Myocarditis; Rodent

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE SEVERITY; EXPERIMENTAL MODEL; HEART MUSCLE CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MOUSE; MYOCARDITIS; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TISSUE INJURY; TRANSGENICS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELLS, CULTURED; CROSSES, GENETIC; CYTOTOXICITY, IMMUNOLOGIC; DNA-BINDING PROTEINS; EGG PROTEINS; INTERFERON TYPE II; INTERLEUKIN-12; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOKINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; MYOCARDITIS; OVALBUMIN; SPECIFIC PATHOGEN-FREE ORGANISMS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 34548359396     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.106.147124     Document Type: Article

References (38)

1. Sharpe AH, Freeman GJ. The B7-CD28 superfamily. Nat Rev Immunol. 2002;2:116-126.
2. Krummel MF, Sullivan TJ, Allison JP. Superantigen responses and costimulation: CD28 and CTLA-4 have opposing effects on T cell expansion in vitro and in vivo. Int Immunol. 1996;8:519-523.
3. Greenwald RJ, Oosterwegel MA, van der Woude D, Kubal A, Mandelbrot DA, Boussiotis VA, Sharpe AH. CTLA-4 regulates cell cycle progression during a primary immune response. Eur J Immunol. 2002;32:366-373.
4. Bachmann MF, Waterhouse P, Speiser DE, McKall-Faienza K, Mak TW, Ohashi PS. Normal responsiveness of CTLA-4-deficient anti-viral cytotoxic T cells. J Immunol. 1998;160:95-100.
5. Chambers CA, Sullivan TJ, Truong T, Allison JP. Secondary but not primary T cell responses are enhanced in CTLA-4-deficient CD8+ T cells. Eur J Immunol. 1998;28:3137-3143.
6. Bachmann MF, Gallimore A, Jones E, Ecabert B, Acha-Orbea H, Kopf M. Normal pathogen-specific immune responses mounted by CTLA-4-deficient T cells: a paradigm reconsidered. Eur J Immunol. 2001;31:450-458.
7. Homann D, Dummer W, Wolfe T, Rodrigo E, Theofilopoulos AN, Oldstone MB, von Herrath MG. Lack of intrinsic CTLA-4 expression has minimal effect on regulation of antiviral T-cell immunity. J Virol. 2006;80:270-280.
8. Gajewski TF, Fallarino F, Fields PE, Rivas F, Alegre ML. Absence of CTLA-4 lowers the activation threshold of primed CD8+ TCR-transgenic T cells: lack of correlation with Src homology domain 2-containing protein tyrosine phosphatase. J Immunol. 2001;166:3900-3907.
9. Shrikant P, Khoruts A, Mescher MF. CTLA-4 blockade reverses CD8+ T cell tolerance to tumor by a CD4+ T cell- and IL-2-dependent mechanism. Immunity. 1999;11:483-493.
10. Hodi FS, Mihm MC, Soiffer RJ, Haluska FG, Butler M, Seiden MV, Davis T, Henry-Spires R, MacRae S, Willman A, Padera R, Jaklitsch MT, Shankar S, Chen TC, Korman A, Allison JP, Dranoff G. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A. 2003;100:4712-4717.
11. Ito T, Ueno T, Clarkson MR, Yuan X, Jurewicz MM, Yagita H, Azuma M, Sharpe AH, Auchincloss H Jr, Sayegh MH, Najafian N. Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8 T cell-mediated alloimmune responses in vivo. J Immunol. 2005;174:6648-6656.
12. McCoy KD, Hermans IF, Fraser JH, Le Gros G, Ronchese F. Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) can regulate dendritic cell-induced activation and cytotoxicity of CD8(+) T cells independently of CD4(+) T cell help. J Exp Med. 1999;189:1157-1162.
13. Huber SA. T cells expressing the gamma delta T cell receptor induce apoptosis in cardiac myocytes. Cardiovasc Res. 2000;45:579-587.
14. Afanasyeva M, Georgakopoulos D, Rose NR. Autoimmune myocarditis: cellular mediators of cardiac dysfunction. Autoimmun Rev. 2004;3:476-486.
15. Grabie N, Delfs MW, Westrich JR, Love VA, Stavrakis G, Ahmad F, Seidman CE, Seidman JG, Lichtman AH. IL-12 is required for differentiation of pathogenic CD8+ T cell effectors that cause myocarditis. J Clin Invest. 2003;111:671-680.
16. Grabie N, Hsieh DT, Buono C, Westrich JR, Allen JA, Pang H, Stavrakis G, Lichtman AH. Neutrophils sustain pathogenic CD8+ T cell responses in the heart. Am J Pathol. 2003;163:2413-2420.
17. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. T cell receptor antagonist peptides induce positive selection. Cell. 1994;76:17-27.
18. Schneider H, Mandelbrot DA, Greenwald RJ, Ng F, Lechler R, Sharpe AH, Rudd CE. Cutting edge: CTLA-4 (CD152) differentially regulates mitogen-activated protein kinases (extracellular signal-regulated kinase and c-Jun N-terminal kinase) in CD4+ T cells from receptor/liganddeficient mice. J Immunol. 2002;169:3475-3479.
19. Cai YH, Alvarez A, Alcaide P, Duramad P, Lim Y-C, Jarolim P, Lowe JB, Luscinskas FW, Lichtman AH. Abrogation of functional selectin-ligand expression reduces migration of pathogenic CD8+ T cells into heart. J Immunol. 2006;176:6568-6575.
20. Taqueti VR, Grabie N, Colvin R, Pang H, Jarolim P, Luster AD, Glimcher LH, Lichtman AH. T-bet controls pathogenicity of CTLs in the heart by separable effects on migration and effector activity. J Immunol. 2006;177:5890-5901.
21. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity. 1995;3:541-547.
22. Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, Thompson CB, Griesser H, Mak TW. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270:985-988.
23. Chambers CA, Kuhns MS, Allison JP. Cytotoxic T lymphocyte antigen-4 (CTLA-4) regulates primary and secondary peptide-specific CD4(+) T cell responses. Proc Natl Acad Sci U S A. 1999;96:8603-8608.
24. Podack ER, Kupfer A. T-cell effector functions: mechanisms for delivery of cytotoxicity and help. Annu Rev Cell Biol. 1991;7:479-504.
25. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-264.
26. Taqueti VR, Mitchell RN, Lichtman AH. Protecting the pump: controlling myocardial inflammatory responses. Annu Rev Physiol. 2006;68:67-95.
27. Kurts C, Carbone FR, Krummel MF, Koch KM, Miller JF, Heath WR. Signalling through CD30 protects against autoimmune diabetes mediated by CD8 T cells. Nature. 1999;398:341-344.
28. Barone KS, Herms B, Karlosky L, Murray S, Qualls J. Effect of in vivo administration of anti-CTLA-4 monoclonal antibody and IL-12 on the induction of low-dose oral tolerance. Clin Exp Immunol. 2002;130:196-203.
29. Van Parijs L, Perez VL, Biuckians A, Maki RG, London CA, Abbas AK. Role of interleukin 12 and costimulators in T cell anergy in vivo. J Exp Med. 1997;186:1119-1128.
30. Schmidt CS, Mescher MF. Adjuvant effect of IL-12: conversion of peptide antigen administration from tolerizing to immunizing for CD8+ T cells in vivo. J Immunol. 1999;163:2561-2567.
31. Schmidt CS, Mescher MF. Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J Immunol. 2002;168:5521-5529.
32. Valenzuela J, Schmidt C, Mescher M. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J Immunol. 2002;169:6842-6849.
33. Curtsinger JM, Lins DC, Mescher MF. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med. 2003;197:1141-1151.
34. Simon MM, Hausmann M, Tran T, Ebnet K, Tschopp J, ThaHla R, Mullbacher A. In vitro- and ex vivo-derived cytolytic leukocytes from granzyme A x B double knockout mice are defective in granule-mediated apoptosis but not lysis of target cells. J Exp Med. 1997;186:1781-1786.
35. Curtsinger JM, Lins DC, Johnson CM, Mescher MF. Signal 3 tolerant CD8 T cells degranulate in response to antigen but lack granzyme B to mediate cytolysis. J Immunol. 2005;175:4392-4399.
36. Atkins MB. Cytokine-based therapy and biochemotherapy for advanced melanoma. Clin Cancer Res. 2006;12:2353s-2358s.
37. Lee P, Wang F, Kuniyoshi J, Rubio V, Stuges T, Groshen S, Gee C, Lau R, Jeffery G, Margolin K, Marty V, Weber J. Effects of interleukin-12 on the immune response to a multipeptide vaccine for resected metastatic melanoma. J Clin Oncol. 2001;19:3836-3847.
38. Sanderson K, Scotland R, Lee P, Liu D, Groshen S, Snively J, Sian S, Nichol G, Davis T, Keler T, Yellin M, Weber J. Autoimmunity in a phase I trial of a fully human anti-cytotoxic T-lymphocyte antigen-4 monoclonal antibody with multiple melanoma peptides and Montanide ISA 51 for patients with resected stages III and IV melanoma. J Clin Oncol. 2005;23:741-750.