Defective selection of thymic regulatory T cells accompanies autoimmunity and pulmonary infiltrates in Tcra-deficient mice double transgenic for human La/Sjögren's syndrome-B and human La-specific TCR

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1514-1522

  Yaciuk, Jane C ^a,b   Pan, Yujun ^a,c   Schwarz, Karen ^a   Pan, Zi Jian ^a   Maier Moore, Jacen S ^a,d   Kosanke, Stanley D ^b   Lawrence, Christina ^a   Farris, A Darise ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c HARBIN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; T LYMPHOCYTE RECEPTOR; AUTOANTIBODY; AUTOANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; RIBONUCLEOPROTEIN; SS-B ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL SURVIVAL; CONTROLLED STUDY; GENE; GENE EXPRESSION; HAPLOTYPE; IMMUNOLOGICAL TOLERANCE; INTERSTITIAL LUNG DISEASE; LUNG INFILTRATE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; SJOEGREN SYNDROME; TCRA GENE; THYMOCYTE; ANIMAL; ANTIGEN PRESENTATION; C57BL MOUSE; COMPLICATION; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; POLYMERASE CHAIN REACTION; T LYMPHOCYTE RECEPTOR GENE; THYMUS; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN PRESENTATION; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; GENES, T-CELL RECEPTOR ALPHA; HUMANS; IMMUNE TOLERANCE; IMMUNOHISTOCHEMISTRY; LUNG DISEASES, INTERSTITIAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL; RIBONUCLEOPROTEINS; SJOGREN'S SYNDROME; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 84922567247     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400319     Document Type: Article

References (49)

1. Arbuckle, M. R., M. T. McClain, M. V. Rubertone, R. H. Scofield, G. J. Dennis, J. A. James, and J. B. Harley. 2003. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349: 1526-1533.
2. Ramos, P. S., J. A. Kelly, C. Gray-McGuire, G. R. Bruner, A. N. Leiran, C. M. Meyer, B. Namjou, K. J. Espe, W. A. Ortmann, M. Reichlin, et al. 2006. Familial aggregation and linkage analysis of autoantibody traits in pedigrees multiplex for systemic lupus erythematosus. Genes Immun. 7: 417-432.
3. Emamian, E. S., J. M. Leon, C. J. Lessard, M. Grandits, E. C. Baechler, P. M. Gaffney, B. Segal, N. L. Rhodus, and K. L. Moser. 2009. Peripheral blood gene expression profiling in Sjögren's syndrome. Genes Immun. 10: 285-296.
4. Niewold, T. B., J. Hua, T. J. Lehman, J. B. Harley, and M. K. Crow. 2007. High serum IFN-alpha activity is a heritable risk factor for systemic lupus erythe-matosus. Genes Immun. 8: 492-502.
5. Reichlin, M. 1986. Significance of the Ro antigen system. J. Clin. Immunol. 6: 339-348.
6. Pease, C. T., P. J. Charles, W. Shattles, J. Markwick, and R. N. Maini. 1993. Serological and immunogenetic markers of extraglandular primary Sjögren's syndrome. Br. J. Rheumatol. 32: 574-577.
7. Martínez-Cordero, E., L. Andrade-Ortega, and E. Martínez-Miranda. 1993. Pulmonary function abnormalities in patients with primary Sjögren's syndrome. J. Investig. Allergol. Clin. Immunol. 3: 205-209.
8. Gordon, T. P., M. Greer, P. Reynolds, A. Guidolin, and L. J. McNeilage. 1991. Estimation of amounts of anti-La(SS-B) antibody directed against immunodo-minant epitopes of the La(SS-B) autoantigen. Clin. Exp. Immunol. 85: 402-406.
9. Raats, J. M., W. F. Roeffen, S. Litjens, I. Bulduk, G. Mans, W. J. van Venrooij, and G. J. Pruijn. 2003. Human recombinant anti-La (SS-B) autoantibodies demonstrate the accumulation of phosphoserine-366-containing la isoforms in nucleoplasmic speckles. Eur. J. Cell Biol. 82: 131-141.
10. ∗0201. Arthritis Rheum. 56: 3387-3398.
11. Keech, C. L., A. D. Farris, D. Beroukas, T. P. Gordon, and J. McCluskey. 2001. Cognate T cell help is sufficient to trigger anti-nuclear autoantibodies in naive mice. J. Immunol. 166: 5826-5834.
12. Aplin, B. D., C. L. Keech, A. L. de Kauwe, T. P. Gordon, D. Cavill, and J. McCluskey. 2003. Tolerance through indifference: autoreactive B cells to the nuclear antigen La show no evidence of tolerance in a transgenic model. J. Immunol. 171: 5890-5900.
13. Kawahata, K., Y. Misaki, Y. Komagata, K. Setoguchi, S. Tsunekawa, Y. Yoshikawa, J. Miyazaki, and K. Yamamoto. 1999. Altered expression level of a systemic nuclear autoantigen determines the fate of immune response to self. J. Immunol. 162: 6482-6491.
14. Murphy, K. M., A. B. Heimberger, and D. Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250: 1720-1723.
15. Vasquez, N. J., J. Kaye, and S. M. Hedrick. 1992. In vivo and in vitro clonal deletion of double-positive thymocytes. J. Exp. Med. 175: 1307-1316.
16. Viret, C., X. He, and C. A. Janeway, Jr. 2000. On the self-referential nature of naive MHC class II-restricted T cells. J. Immunol. 165: 6183-6192.
17. Jordan, M. S., A. Boesteanu, A. J. Reed, A. L. Petrone, A. E. Holenbeck, M. A. Lerman, A. Naji, and A. J. Caton. 2001. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2: 301-306.
18. Apostolou, I., A. Sarukhan, L. Klein, and H. von Boehmer. 2002. Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 3: 756-763.
19. Kawahata, K., Y. Misaki, M. Yamauchi, S. Tsunekawa, K. Setoguchi, J. Miyazaki, and K. Yamamoto. 2002. Generation of CD4(+)CD25(+) regulatory T cells from autoreactive T cells simultaneously with their negative selection in the thymus and from nonautoreactive T cells by endogenous TCR expression. J. Immunol. 168: 4399-4405.
20. Bogen, B., L. Gleditsch, S. Weiss, and Z. Dembic. 1992. Weak positive selection of transgenic T cell receptor-bearing thymocytes: importance of major histo-compatibility complex class II, T cell receptor and CD4 surface molecule densities. Eur. J. Immunol. 22: 703-709.
21. Sebzda, E., V. A. Wallace, J. Mayer, R. S. Yeung, T. W. Mak, and P. S. Ohashi. 1994. Positive and negative thymocyte selection induced by different concentrations of a single peptide. Science 263: 1615-1618.
22. Alam, S. M., P. J. Travers, J. L. Wung, W. Nasholds, S. Redpath, S. C. Jameson, and N. R. Gascoigne. 1996. T-cell-receptor affinity and thymocyte positive selection. Nature 381: 616-620.
23. Berg, L. J., G. D. Frank, and M. M. Davis. 1990. The effects of MHC gene dosage and allelic variation on T cell receptor selection. Cell 60: 1043-1053.
24. Van de Keere, F., and S. Tonegawa. 1998. CD4(+) T cells prevent spontaneous experimental autoimmune encephalomyelitis in anti-myelin basic protein T cell receptor transgenic mice. J. Exp. Med. 188: 1875-1882.
25. Olivares-Villagómez, D., Y. Wang, and J. J. Lafaille. 1998. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomy-elitis. J. Exp. Med. 188: 1883-1894.
26. Kanagawa, O., A. Militech, and B. A. Vaupel. 2002. Regulation of diabetes development by regulatory T cells in pancreatic islet antigen-specific TCR transgenic nonobese diabetic mice. J. Immunol. 168: 6159-6164.
27. Hori, S., M. Haury, A. Coutinho, and J. Demengeot. 2002. Specificity requirements for selection and effector functions of CD25+4+ regulatory T cells in antimyelin basic protein T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 99: 8213-8218.
28. Pan, Z. J., K. Davis, S. Maier, M. P. Bachmann, X. R. Kim-Howard, C. Keech, T. P. Gordon, J. McCluskey, and A. D. Farris. 2006. Neo-epitopes are required for immunogenicity of the La/SS-B nuclear antigen in the context of late apo-ptotic cells. Clin. Exp. Immunol. 143: 237-248.
29. Zhumabekov, T., P. Corbella, M. Tolaini, and D. Kioussis. 1995. Improved version of a human CD2 minigene based vector for T cell-specific expression in transgenic mice. J. Immunol. Methods 185: 133-140.
30. Julius, M. H., E. Simpson, and L. A. Herzenberg. 1973. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur. J. Immunol. 3: 645-649.
31. Williams, K. M., H. Mella, P. J. Lucas, J. A. Williams, W. Telford, and R. E. Gress. 2009. Single cell analysis of complex thymus stromal cell populations: rapid thymic epithelia preparation characterizes radiation injury. Clin. Transl. Sci. 2: 279-285.
32. Dumas, E. K., M. L. Nguyen, P. M. Cox, H. Rodgers, J. L. Peterson, J. A. James, and A. D. Farris. 2013. Stochastic humoral immunity to Bacillus anthracis protective antigen: identification of anti-peptide IgG correlating with serocon-version to Lethal Toxin neutralization. Vaccine 31: 1856-1863.
33. Oukka, M., E. Colucci-Guyon, P. L. Tran, M. Cohen-Tannoudji, C. Babinet, V. Lotteau, and K. Kosmatopoulos. 1996. CD4 T cell tolerance to nuclear proteins induced by medullary thymic epithelium. Immunity 4: 545-553.
34. Michaels, M. A., H. K. Kang, A. Kaliyaperumal, E. Satyaraj, Y. Shi, and S. K. Datta. 2005. A defect in deletion of nucleosome-specific autoimmune T cells in lupus-prone thymus: role of thymic dendritic cells. J. Immunol. 175: 5857-5865.
35. Maloy, K. J., and F. Powrie. 2001. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2: 816-822.
36. Hinterberger, M., M. Aichinger, O. Prazeres da Costa, D. Voehringer, R. Hoffmann, and L. Klein. 2010. Autonomous role of medullary thymic epithelial cells in central CD4(+) T cell tolerance. Nat. Immunol. 11: 512-519.
37. Grossman, Z., and A. Singer. 1996. Tuning of activation thresholds explains flexibility in the selection and development of T cells in the thymus. Proc. Natl. Acad. Sci. USA 93: 14747-14752.
38. Wirnsberger, G., M. Hinterberger, and L. Klein. 2011. Regulatory T-cell differentiation versus clonal deletion of autoreactive thymocytes. Immunol. Cell Biol. 89: 45-53.
39. Topfer, F., T. Gordon, and J. McCluskey. 1995. Intra- and intermolecular spreading of autoimmunity involving the nuclear self-antigens La (SS-B) and Ro (SS-A). Proc. Natl. Acad. Sci. USA 92: 875-879.
40. Farris, A. D., L. Brown, P. Reynolds, J. B. Harley, J. A. James, R. H. Scofield, J. McCluskey, and T. P. Gordon. 1999. Induction of autoimmunity by multivalent immunodominant and subdominant T cell determinants of La (SS-B). J. Immunol. 162: 3079-3087.
41. Keech, C. L., T. P. Gordon, P. Reynolds, and J. McCluskey. 1993. Expression and functional conservation of the human La (SS-B) nuclear autoantigen in murine cell lines. J. Autoimmun. 6: 543-555.
42. Scofield, R. H., S. Asfa, D. Obeso, R. Jonsson, and B. T. Kurien. 2005. Immunization with short peptides from the 60-kDa Ro antigen recapitulates the serological and pathological findings as well as the salivary gland dysfunction of Sjogren's syndrome. J. Immunol. 175: 8409-8414.
43. Peng, S. L., S. Fatenejad, and J. Craft. 1996. Induction of nonpathologic, humoral autoimmunity in lupus-prone mice by a class II-restricted, transgenic alpha beta T cell. Separation of autoantigen-specific and - nonspecific help. J. Immunol. 157: 5225-5230.
44. Maier-Moore, J. S., C. G. Horton, S. A. Mathews, A. W. Confer, C. Lawrence, Z. Pan, K. M. Coggeshall, and A. D. Farris. 2014. Interleukin-6 deficiency corrects nephritis, lymphocyte abnormalities, and secondary Sjögren's syndrome features in lupus-prone Sle1. Yaa mice. Arthritis Rheum. (Munch) 66: 2521-2531.
45. Papiris, S. A., M. Saetta, G. Turato, R. La Corte, L. Trevisani, C. E. Mapp, P. Maestrelli, L. M. Fabbri, and A. Potena. 1997. CD4-positive T-lymphocytes infiltrate the bronchial mucosa of patients with Sjögren's syndrome. Am. J. Respir. Crit. Care Med. 156: 637-641.
46. Pagani, J. J., J. D. Collins, and M. J. Reza. 1979. Sjogren syndrome presenting as pulmonary pseudolymphoma: report of a case. J. Natl. Med. Assoc. 71: 677-678.
47. Deheinzelin, D., V. L. Capelozzi, R. A. Kairalla, J. V. Barbas Filho, P. H. Saldiva, and C. R. de Carvalho. 1996. Interstitial lung disease in primary Sjögren's syndrome. Clinical-pathological evaluation and response to treatment. Am. J. Respir. Crit. Care Med. 154: 794-799.
48. Fox, R. I., F. V. Howell, R. C. Bone, and P. Michelson. 1984. Primary Sjogren syndrome: clinical and immunopathologic features. Semin. Arthritis Rheum. 14: 77-105.
49. Locht, H., R. Pelck, and R. Manthorpe. 2008. Diagnostic and prognostic significance of measuring antibodies to alpha-fodrin compared to anti-Ro-52, anti-Ro-60, and anti-La in primary Sjögren's syndrome. J. Rheumatol. 35: 845-849.