Paradoxical arrest in lupus activity in BXSB mice with highly autoreactive T cells

Lupus

Volumn 19, Issue 2, 2010, Pages 182-191

  Stojakovic, M ^a   Tatari Calderone, Z ^a   Maric, C ^b   Hoang, A ^a   Vukmanovic, S ^a  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

IL 10; Lupus; T cells; TCR avidity

Indexed keywords

INTERLEUKIN 10; RNA 18S; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; CD4 CD8 RATIO; CD4+ CD25+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE SEVERITY; FEMALE; IN VIVO STUDY; INCIDENCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; AUTOANTIGENS; CELL DIFFERENTIATION; INTERLEUKIN-10; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; SEVERITY OF ILLNESS INDEX; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 76049100289     PISSN: 09612033     EISSN: None     Source Type: Journal    
DOI: 10.1177/0961203309350756     Document Type: Article

References (50)

1. Zeh HJI, Perry-Lalley D., Dudley ME, Rosenberg SA, Yang JC High avidity CTLs for two self antigens demonstrate superior in vitro and in vivo antitumor efficacy. J Immunol 1999 ; 162: 989-994.
2. Derby MA, Alexander-Miller MA, Tse R., Berzofsky JA High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J Immunol 2001 ; 166: 1690-1697.
3. Starr TK, Jameson SC, Hogquist KA Positive and negative selection of T cells. Ann Rev Immunol 2003 ; 21: 139-176.
4. Palmer E. The T-cell antigen receptor: a logical response to an unknown ligand. J Recept Signal Transduct Res 2006 ; 26: 367-378.
5. Vukmanovic S., Neubert TA, Santori FR Could TCR antagonism explain associations between MHC genes and disease? Trends Mol Med 2003 ; 9: 139-146.
6. Jameson SC T cell homeostasis: keeping useful T cells alive and live T cells useful. Semin Immunol 2005 ; 17: 231-237.
7. Santori FR, Brown SM, Vukmanovic S. Genomics-based identification of self-ligands with T cell receptor-specific biological activity. Immunol Rev 2002 ; 190: 146-160.
8. Holler PD, Chlewiski LK, Kranz DM TCRs with high affinity for foreign pMHC show self reactivity. Nature Immunol 2003 ; 4: 55-62.
9. Amrani A., Verdaguer J., Serra P., Tafuro S., Tan R., Santamaria P. Progression of autoimmune diabetes driven by avidity maturation of a T-cell population. Nature 2000 ; 406: 739-742.
10. Garcia KC, Radu CG, Ho J., Ober RJ, Ward ES Kinetics and thermodynamics of T cell receptor- autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc Nat Acad Sci USA 2001 ; 98: 6818-6823.
11. Gronski MA, Boulter JM, Moskophidis D., et al. TCR affinity and negative regulation limit autoimmunity. Nat Med 2004 ; 10: 1234-1239.
12. Han B., Serra P., Yamanouchi J., et al. Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes. J Clin Invest 2005 ; 115: 1879-1887.
13. Mohan C., Adams S., Stanik V., Datta SK Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J Exp Med 1993 ; 177 (5). 1367-1381.
14. Wofsy D., Seaman WE Successful treatment of autoimmunity in NZB/NZW F1 mice with monoclonal antibody to L3T4. J Exp Med 1985 ; 161 (2). 378-391.
15. Santoro TJ, Portanova JP, Kotzin BL The contribution of L3T4+ T cells to lymphoproliferation and autoantibody production in MRL-lpr/lpr mice. J Exp Med 1988 ; 167 (5). 1713-1718.
16. Peng SL, Madaio MP, Hughes DP, et al. Murine lupus in the absence of alpha beta T cells. J Immunol 1996 ; 156 (10). 4041-4049.
17. Lawson BR, Koundouris SI, Barnhouse M., et al. The role of α+ T cells and homeostatic T cell proliferation in Y-chromosome-associated murine lupus. J Immunol 2001 ; 167: 2354-2360.
18. Peng SL, Fatenejad S., Craft J. 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 1996 ; 157 (12). 5225-5230.
19. Perkins DL, Listman JA, Marshak-Rothstein A., et al. Restriction of the TCR repertoire inhibits the development of memory T cells and prevents autoimmunity in lpr mice. J Immunol 1996 ; 156 (12). 4961-4968.
20. Rozzo SJ, Drake CG, Chiang BL, Gershwin ME, Kotzin BL Evidence for polyclonal T cell activation in murine models of systemic lupus erythematosus. J Immunol 1994 ; 153 (3). 1340-1351.
21. Busser BW, Adair BS, Erikson J., Laufer TM. Activation of diverse repertoires of autoreactive T cells enhances the loss of anti-dsDNA B cell tolerance. J Clin Invest 2003 ; 112 (9). 1361-1371.
22. Stojakovic M., Salazar-Fontana LI, Tatari-Calderone Z., et al. Adaptable TCR avidity thresholds for negative selection. J Immunol 2008 ; 181: 6770-6778.
23. Santori FR, Popmihajlov Z., Badovinac VP, et al. TCR?2 chain that forms peptide-independent alloreactive TCR transfers reduced reactivity with irrelevant peptide/MHC complex. J Immunol 2007 ; 178: 6109-6114.
24. Mankhey RW, Bhatti F., Maric C. 17beta-Estradiol replacement improves renal function and pathology associated with diabetic nephropathy. Am J Physiol Renal Physiol 2005 ; 288: F399-405.
25. Gilbert RE, Cooper ME The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney Int 1999 ; 56: 1627-1637.
26. Groux H., O?Garra A., Bigler M., et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997 ; 389: 737-742.
27. Shi Y., Kaliyaperumal A., Lu L., Southwood S., et al. Promiscuous presentation and recognition of nucleosomal autoepitopes in lupus: role of autoimmune T cell receptor alpha chain. J Exp Med 1998 ; 187 (3). 367-378.
28. Kotzin BL, West SG Clinical immunology, principles and practice. In: Rich RR (ed.), Systemic lupus erythematosus. London: Elsevier Science Limited, 2001, p. 60. 1-60. 24.
29. Haywood ME, Rogers NJ, Rose SJ, et al. Dissection of BXSB lupus phenotype using mice congenic for chromosome 1 demonstrates that separate intervals direct different aspects of disease. J Immunol 2004 ; 173: 4277-4285.
30. Izui S., Ibnou-Zekri N., Fossati-Jimack L., Iwamoto M. Lessons from BXSB and related mouse models. Int Rev Immunol 2000 ; 19: 447-472.
31. Pisitkun P., Deane JA, Difilippantonio MJ, Tarasenko T., Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006 ; 312: 1669-1672.
32. Subramanian S., Tus K., Li QZ, et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Nat Acad Sci USA 2006 ; 103: 9970-9975.
33. Yoh K., Shibuya K., Morito N., Nakano T., et al. Transgenic over-expression of GATA-3 in T lymphocytes improves autoimmune glomerulonephritis in mice with a BXSB/MpJ-Yaa genetic background. J Am Soc Nephrol 2003 ; 14: 2494-2502.
34. Budd RC, Cerottini JC, Horvath C., et al. Distinction of virgin and memory T lymphocytes: stable acquisition of the Pgp-1 glycoprotein concomitant with antigenic stimulation. J Immunol 1987 ; 138: 3120-3129.
35. Buer J., Lanoue A., Franzke A., Garcia C., von Boehmer H., Sarukhan A. Interleukin 10 secretion and impaired effector function of major histocompatibility complex class II restricted T cells anergized in vivo. J Exp Med 1988 ; 187: 177-183.
36. Sundstedt A., Hoiden I., Rosendahl A., Kalland T., van Rooijen N., Dohlsten M. Immunoregulatory role of IL-10 during superantigen-induced hyporesponsiveness in vivo. J Immunol 1997 ; 158: 180-186.
37. Burkhart C., Liu GY, Anderton SM, Metzler B., Wraith DC Peptide-induced T cell regulation of experimental autoimmune encephalomyelitis: a role for IL-10. Int Immunol 1999 ; 11: 1625-1634.
38. Seewaldt S., Alferink J., Forster I. Interleukin-10 is crucial for maintenance but not for developmental induction of peripheral T cell tolerance. Eur J Immunol 2002 ; 32: 3607-3616.
39. Groux H., Cottrez F. The complex role of interleukin-10 in autoimmunity. J Autoimmun 2003 ; 20: 281-285.
40. Beebe AM, Cua DJ, de Waal Malefyt R. The role of interleukin-10 in autoimmune disease: systemic lupus erythematosus (SLE) and multiple sclerosis (MS). Cytokine Growth Factor Rev 2002 ; 13: 403-412.
41. Llorente L., Richaud-Patin Y., García-Padilla C., et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 2000 ; 43: 1790-1800.
42. Ishida H., Muchamuel T., Sakaguchi S., Andrade S., Menon S., Howard M. Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice. J Exp Med 1994 ; 179: 305-310.
43. Yin Z., Bahtiyar G., Zhang N., et al. IL-10 regulates murine lupus. J Immunol 2002 ; 169: 2148-2155.
44. Blenman KR, Duan B., Xu Z., et al. IL-10 regulation of lupus in the NZM2410 murine model. Lab Investig 2006 ; 86: 1136-1148.
45. Hochberg MC Dubois? lupus erythematosus. In: Wallace DJ, Hahn BH (eds.), The epidemiology of systemic lupus erythematosus. Baltimore: Williams & Wilkins, 1997. p. 49-65.
46. Ge Q., Rao VP, Cho BK, Eisen HN, Chen J. Dependence of lymphopenia-induced T cell proliferation on the abundance of peptide/ MHC epitopes and strength of their interaction with T cell receptors. Proc Natl Acad Sci USA 2001 ; 98 (4). 1728-1733.
47. Kassiotis G., Zamoyska R., Stockinger B. Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. J Exp Med 2003 ; 197: 1007-1016.
48. Kieper WC, Burghardt JT, Surh CD A role for TCR affinity in regulating naive T cell homeostasis. J Immunol 2004 ; 172 (1). 40-44.
49. Khattry R., Cox T., Yasayko S-A., Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003 ; 4: 337-342.
50. Bickerstaff AA, Xia D., Pelletier RP, Orosz CG Mechanisms of graft acceptance: evidence that plasminogen activator controls donor-reactive delayed-type hypersensitivity responses in cardiac allograft acceptor mice. J Immunol 2000 ; 164: 5132-5139.