Programmed death ligand 1 regulates a critical checkpoint for autoimmune myocarditis and pneumonitis in MRL mice

Journal of Immunology

Volumn 181, Issue 4, 2008, Pages 2513-2521

  Lucas, Julie A ^a   Menke, Julia ^a   Rabacal, Whitney A ^a   Schoen, Frederick J ^a   Sharpe, Arlene H ^a   Kelley, Vicki Rubin ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; FAS ANTIGEN; LIGAND; PROGRAMMED DEATH LIGAND 1; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; B7 ANTIGEN; MEMBRANE ANTIGEN; MEMBRANE PROTEIN; PDCD1 PROTEIN, MOUSE; PDCD1LG1 PROTEIN, MOUSE; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE MYOCARDITIS; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL TRANSFER; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENDOTHELIUM CELL; FEMALE; HEART ATRIUM; HEART VENTRICLE; KIDNEY DISEASE; LUNG; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPH NODE; MACROPHAGE; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PHENOTYPE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SKIN; SPLEEN; SYSTEMIC DISEASE; T LYMPHOCYTE; WILD TYPE; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; COMPARATIVE STUDY; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MORTALITY; MOUSE MUTANT; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PATHOLOGY; PHYSIOLOGY; RADIATION CHIMERA; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD80; ANTIGENS, CD95; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; AUTOIMMUNE DISEASES; BONE MARROW TRANSPLANTATION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; IMMUNOPHENOTYPING; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCARDITIS; PEPTIDES; PNEUMONIA; RADIATION CHIMERA; SIGNAL TRANSDUCTION;

EID: 53149113444     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.4.2513     Document Type: Article

References (46)

1. Theofilopoulos, A. N., and F. J. Dixon. 1981. Etiopathogenesis of murine SLE. Immunol. Rev. 55: 179-216.
2. Kelley, V. E., and J. B. Roths. 1985. Interaction of mutant lpr gene with background strain influences renal disease. Clin. Immunol. Immunopathol. 37: 220-229.
3. Moyer, C. F., J. D. Strandberg, and C. L. Reinisch. 1987. Systemic mononuclear-cell vasculitis in MRL/Mp-lpr/lpr mice: a histologic and immunocytochemical analysis. Am. J. Pathol. 127: 229-242.
4. Andrews, B. S., R. A. Eisenberg, A. N. Theofilopoulos, S. Izui, C. B. Wilson, P. J. McConahey, E. D. Murphy, J. B. Roths, and F. J. Dixon. 1978. Spontaneous murine lupus-like syndromes: clinical and immunopathological manifestations in several strains. J. Exp. Med. 148: 1198-1215.
5. Matsuzawa, A., T. Moriyama, T. Kaneko, M. Tanaka, M. Kimura, H. Ikeda, and T. Katagiri. 1990. A new allele of the lpr locus, lprcg, that complements the gld gene in induction of lymphadenopathy in the mouse. J. Exp. Med. 171: 519-531.
6. Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356: 314-317.
7. Peng, S. L., M. P. Madaio, D. P. Hughes, I. N. Crispe, M. J. Owen, L. Wen, A. C. Hayday, and J. Craft. 1996. Murine lupus in the absence of α β T cells. J. Immunol. 156: 4041-4049.
8. Christianson, G. J., R. L. Blankenburg, T. M. Duffy, D. Panka, J. B. Roths, A. Marshak-Rothstein, and D. C. Roopenian. 1996. β2-microglobulin dependence of the lupus-like autoimmune syndrome of MRL-lpr mice. J. Immunol. 156: 4932-4939.
9. Chesnutt, M. S., B. K. Finck, N. Killeen, M. K. Connolly, H. Goodman, and D. Wofsy. 1998. Enhanced lymphoproliferation and diminished autoimmunity in CD4-deficient MRL/lpr mice. Clin. Immunol. Immunopathol. 87: 23-32.
10. Lenda, D. M., E. R. Stanley, and V. R. Kelley. 2004. Negative role of colony-stimulating factor-1 in macrophage, T cell, and B cell mediated autoimmune disease in MRL-Fas(lpr) mice. J. Immunol. 173: 4744-4754.
11. Chan, O. T., M. P. Madaio, and M. J. Shlomchik. 1999. The central and multiple roles of B cells in lupus pathogenesis. Immunol. Rev. 169: 107-121.
12. Hewicker, M., and G. Trautwein. 1986. Glomerular lesions in MRL mice. A light and immunofluorescence microscopic study. Zentralbl. Veterinarmed. B 33: 727-739.
13. Watson, M. L., J. K. Rao, G. S. Gilkeson, P. Ruiz, E. M. Eicher, D. S. Pisetsky, A. Matsuzawa, J. M. Rochelle, and M. F. Seldin. 1992. Genetic analysis of MRL-lpr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. J. Exp. Med. 176: 1645-1656.
14. Vidal, S., D. H. Kono, and A. N. Theofilopoulos. 1998. Loci predisposing to autoimmunity in MRL-Faslpr and C57BL/6-Faslpr mice. J. Clin. Invest. 101: 696-702.
15. Kinoshita, K., G. Tesch, A. Schwarting, R. Maron, A. H. Sharpe, and V. R. Kelley. 2000. Costimulation by B7-1 and B7-2 is required for autoimmune disease in MRL-Faslpr mice. J. Immunol. 164: 6046-6056.
16. Agata, Y., A. Kawasaki, H. Nishimura, Y. Ishida, T. Tsubata, H. Yagita, and T. Honjo. 1996. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 8: 765-772.
17. Menke, J., J. A. Lucas, G. C. Zeller, M. E. Keir, X. R. Huang, N. Tsuboi, T. N. Mayadas, H. Y. Lan, A. H. Sharpe, and V. R. Kelley. 2007. Programmed death 1 ligand (PD-L) 1 and PD-L2 limit autoimmune kidney disease: distinct roles. J. Immunol. 179: 7466-7477.
18. Gotsman, I., N. Grabie, R. Dacosta, G. Sukhova, A. Sharpe, and A. H. Lichtman. 2007. Proatherogenic immune responses are regulated by the PD-1/PD-L pathway in mice. J. Clin. Invest. 117: 2974-2982.
19. Sharpe, A. H., E. J. Wherry, R. Ahmed, and G. J. Freeman. 2007. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8: 239-245.
20. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26: 677-704.
21. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151.
22. Latchman, Y. E., S. C. Liang, Y. Wu, T. Chernova, R. A. Sobel, M. Klemm, V. K. Kuchroo, G. J. Freeman, and A. H. Sharpe. 2004. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. USA 101: 10691-10696.
23. Watson, M. L., J. K. Rao, G. S. Gilkeson, P. Ruiz, E. M. Eicher, D. S. Pisetsky, A. Matsuzawa, J. M. Rochelle, and M. F. Seldin. 1992. Genetic analysis of MRL-lpr mice: relationship of the Fas apoptosis gene to disease manifestations and renal disease-modifying loci. J. Exp. Med. 176: 1645-1656.
24. Taqueti, V. R., N. Grabie, R. Colvin, H. Pang, P. Jarolim, A. D. Luster, L. H. Glimcher, and A. H. Lichtman. 2006. T-bet controls pathogenicity of CTLs in the heart by separable effects on migration and effector activity. J. Immunol. 177: 5890-5901.
25. O'Connor, K. C., K. Nguyen, and B. D. Stollar. 2001. Recognition of DNA by VH and Fv domains of an IgG anti-poly(dC) antibody with a singly mutated VH domain. J. Mol. Recognit. 14: 18-28.
26. Keir, M. E., S. C. Liang, I. Guleria, Y. E. Latchman, A. Qipo, L. A. Albacker, M. Koulmanda, G. J. Freeman, M. H. Sayegh, and A. H. Sharpe. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203: 883-895.
27. Njoroge, J. M., L. B. Mitchell, M. Centola, D. Kastner, M. Raffeld, and J. L. Miller. 2001. Characterization of viable autofluorescent macrophages among cultured peripheral blood mononuclear cells. Cytometry 44: 38-44.
28. Lund, F. E. 2008. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 20: 332-338.
29. Li, Y., J. S. Heuser, L. C. Cunningham, S. D. Kosanke, and M. W. Cunningham. 2006. Mimicry and antibody-mediated cell signaling in autoimmune myocarditis. J. Immunol. 177: 8234-8240.
30. Cunningham, M. W. 2004. T cell mimicry in inflammatory heart disease. Mol. Immunol. 40: 1121-1127.
31. Okazaki, T., Y. Tanaka, R. Nishio, T. Mitsuiye, A. Mizoguchi, J. Wang, M. Ishida, H. Hiai, A. Matsumori, N. Minato, and T. Honjo. 2003. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat. Med. 9: 1477-1483.
32. Nishimura, H., T. Okazaki, Y. Tanaka, K. Nakatani, M. Hara, A. Matsumori, S. Sasayama, A. Mizoguchi, H. Hiai, N. Minato, and T. Honjo. 2001. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291: 319-322.
33. Schoen, F. J. 2004. The heart. In Robbins/Cotran Pathologic Basis of Disease, 7th Ed. V. Kumar, N. Fausto, and A. Abbas, eds. W.B. Saunders, Philadelphia, pp. 555-618.
34. Bloom, R. D., S. Florquin, G. G. Singer, D. C. Brennan, and V. R. Kelley. 1993. Colony stimulating factor-1 in the induction of lupus nephritis. Kidney Int. 43: 1000-1009.
35. Yui, M. A., W. H. Brissette, D. C. Brennan, R. P. Wuthrich, and V. E. Rubin-Kelley. 1991. Increased macrophage colony-stimulating factor in neonatal and adult autoimmune MRL-lpr mice. Am. J. Pathol. 139: 255-261.
36. Kolattukudy, P. E., T. Quach, S. Bergese, S. Breckenridge, J. Hensley, R. Altschuld, G. Gordillo, S. Klenotic, C. Orosz, and J. Parker-Thornburg. 1998. Myocarditis induced by targeted expression of the MCP-1 gene in murine cardiac muscle. Am. J. Pathol. 152: 101-111.
37. Elliott, J. F., J. Liu, Z. N. Yuan, N. Bautista-Lopez, S. L. Wallbank, K. Suzuki, D. Rayner, P. Nation, M. A. Robertson, et al. 2003. Autoimmune cardiomyopathy and heart block develop spontaneously in HLA-DQ8 transgenic IAβ knockout NOD mice. Proc. Natl. Acad. Sci. USA 100: 13447-13452.
38. Taylor, J. A., E. Havari, M. F. McInerney, R. Bronson, K. W. Wucherpfennig, and M. A. Lipes. 2004. A spontaneous model for autoimmune myocarditis using the human MHC molecule HLA-DQ8. J. Immunol. 172: 2651-2658.
39. Hayward, S. L., N. Bautista-Lopez, K. Suzuki, A. Atrazhev, P. Dickie, and J. F. Elliott. 2006. CD4 T cells play major effector role and CD8 T cells initiating role in spontaneous autoimmune myocarditis of HLA-DQ8 transgenic IAb knockout nonobese diabetic mice. J. Immunol. 176: 7715-7725.
40. Tanaka, K., M. J. Albin, X. Yuan, K. Yamaura, A. Habicht, T. Murayama, M. Grimm, A. M. Waaga, T. Ueno, R. F. Padera, et al. 2007. PDL1 is required for peripheral transplantation tolerance and protection from chronic allograft rejection. J. Immunol. 179: 5204-5210.
41. Shen, L., Y. Jin, G. J. Freeman, A. H. Sharpe, and M. R. Dana. 2007. The function of donor versus recipient programmed death-ligand 1 in corneal allograft survival. J. Immunol. 179: 3672-3679.
42. Liao, L., R. Sindhwani, M. Rojkind, S. Factor, L. Leinwand, and B. Diamond. 1995. Antibody-mediated autoimmune myocarditis depends on genetically determined target organ sensitivity. J. Exp. Med. 181: 1123-1131.
43. Kuan, A. P., W. Chamberlain, S. Malkiel, H. D. Lieu, S. M. Factor, B. Diamond, and B. L. Kotzin. 1999. Genetic control of autoimmune myocarditis mediated by myosin-specific antibodies. Immunogenetics 49: 79-85.
44. Kuan, A. P., L. Zuckier, L. Liao, S. M. Factor, and B. Diamond. 2000. Immunoglobulin isotype determines pathogenicity in antibody-mediated myocarditis in naive mice. Circ. Res. 86: 281-285.
45. Goser, S., M. Andrassy, S. J. Buss, F. Leuschner, C. H. Volz, R. Ottl, S. Zittrich, N. Blaudeck, S. E. Hardt, G. Pfitzer, et al. 2006. Cardiac troponin I but not cardiac troponin T induces severe autoimmune inflammation in the myocardium. Circulation 114: 1693-1702.
46. Okazaki, T., and T. Honjo. 2007. PD-1 and PD-1 ligands: from discovery to clinical application. Int. Immunol. 19: 813-824.