Spontaneous autoimmunity in the absence of IL-2 is driven by uncontrolled dendritic cells

Journal of Immunology

Volumn 189, Issue 4, 2012, Pages 1585-1593

  Isakson, Sara H ^a   Katzman, Shoshana D ^a   Hoyer, Katrina K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERFERON; INTERLEUKIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BIOACCUMULATION; CELL FUNCTION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE SEVERITY; ERYTHROCYTE; IMMUNOPATHOGENESIS; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURVIVAL TIME; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; TH1 CELL; WILD TYPE;

ADOPTIVE TRANSFER; ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERFERON TYPE I; INTERLEUKIN-12; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84864823601     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200342     Document Type: Article

References (34)

1. Sadlack, B., J. Löhler, H. Schorle, G. Klebb, H. Haber, E. Sickel, R. J. Noelle, and I. Horak. 1995. Generalized autoimmune disease in interleukin-2-deficient mice is triggered by an uncontrolled activation and proliferation of CD4+ T cells. Eur. J. Immunol. 25: 3053-3059.
2. Barron, L., H. Dooms, K. K. Hoyer, W. Kuswanto, J. Hofmann, W. E. O'Gorman, and A. K. Abbas. 2010. Cutting edge: mechanisms of IL-2-dependent maintenance of functional regulatory T cells. J. Immunol. 185: 6426-6430.
3. Malek, T. R., B. O. Porter, E. K. Codias, P. Scibelli, and A. Yu. 2000. Normal lymphoid homeostasis and lack of lethal autoimmunity in mice containing mature T cells with severely impaired IL-2 receptors. J. Immunol. 164: 2905-2914. (Pubitemid 30148947)
4. Fontenot, J. D., J. P. Rasmussen, M. A. Gavin, and A. Y. Rudensky. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6: 1142-1151. (Pubitemid 41541792)
5. Hoyer, K. K., K. Wolslegel, H. Dooms, and A. K. Abbas. 2007. Targeting T cell-specific costimulators and growth factors in a model of autoimmune hemolytic anemia. J. Immunol. 179: 2844-2850.
6. Hoyer, K. K., W. F. Kuswanto, E. Gallo, and A. K. Abbas. 2009. Distinct roles of helper T-cell subsets in a systemic autoimmune disease. Blood 113: 389-395.
7. Bossie, A., and E. S. Vitetta. 1991. IFN-gamma enhances secretion of IgG2a from IgG2a-committed LPS-stimulated murine B cells: implications for the role of IFN-gamma in class switching. Cell. Immunol. 135: 95-104.
8. Wirth, J. J., F. Kierszenbaum, G. Sonnenfeld, and A. Zlotnik. 1985. Enhancing effects of gamma interferon on phagocytic cell association with and killing of Trypanosoma cruzi. Infect. Immun. 49: 61-66. (Pubitemid 15062869)
9. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779. (Pubitemid 32983013)
10. Süss, G., and K. Shortman. 1996. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. J. Exp. Med. 183: 1789-1796.
11. Rogge, L., D. D'Ambrosio, M. Biffi, G. Penna, L. J. Minetti, D. H. Presky, L. Adorini, and F. Sinigaglia. 1998. The role of Stat4 in species-specific regulation of Th cell development by type I IFNs. J. Immunol. 161: 6567-6574. (Pubitemid 28562196)
12. Koch, F., U. Stanzl, P. Jennewein, K. Janke, C. Heufler, E. Kämpgen, N. Romani, and G. Schuler. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 184: 741-746. (Pubitemid 26324128)
13. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y. J. Liu. 1999. The nature of the principal type 1 interferon-producing cells in human blood. Science 284: 1835-1837.
14. Ohnmacht, C., A. Pullner, S. B. King, I. Drexler, S. Meier, T. Brocker, and D. Voehringer. 2009. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J. Exp. Med. 206: 549-559.
15. Blanco, P., A. K. Palucka, M. Gill, V. Pascual, and J. Banchereau. 2001. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 294: 1540-1543. (Pubitemid 33063928)
16. Teichmann, L. L., M. L. Ols, M. Kashgarian, B. Reizis, D. H. Kaplan, and M. J. Shlomchik. 2010. Dendritic cells in lupus are not required for activation of Tand B cells but promote their expansion, resulting in tissue damage. Immunity 33: 967-978.
17. Blasius, A. L., E. Giurisato, M. Cella, R. D. Schreiber, A. S. Shaw, and M. Colonna. 2006. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177: 3260-3265. (Pubitemid 44277845)
18. Sheehan, K. C., K. S. Lai, G. P. Dunn, A. T. Bruce, M. S. Diamond, J. D. Heutel, C. Dungo-Arthur, J. A. Carrero, J. M. White, P. J. Hertzog, and R. D. Schreiber. 2006. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26: 804-819. (Pubitemid 44764543)
19. Lohr, J., B. Knoechel, J. J. Wang, A. V. Villarino, and A. K. Abbas. 2006. Role of IL-17 and regulatory T lymphocytes in a systemic autoimmune disease. J. Exp. Med. 203: 2785-2791. (Pubitemid 46026156)
20. Lee, N. J., R. J. Rigby, H. Gill, J. J. Boyle, L. Fossati-Jimack, B. J. Morley, and T. J. Vyse. 2004. Multiple loci are linked with anti-red blood cell antibody production in NZB mice - comparison with other phenotypes implies complex modes of action. Clin. Exp. Immunol. 138: 39-46. (Pubitemid 39279963)
21. Schell, J. B., C. A. Crane, M. F. Smith, Jr., and M. R. Roberts. 2007. Differential ex vivo nitric oxide production by acutely isolated neonatal and adult microglia. J. Neuroimmunol. 189: 75-87. (Pubitemid 47379435)
22. Tang, Q., K. J. Henriksen, M. Bi, E. B. Finger, G. Szot, J. Ye, E. L. Masteller, H. McDevitt, M. Bonyhadi, and J. A. Bluestone. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199: 1455-1465. (Pubitemid 38780401)
23. Chang, T. T., C. Jabs, R. A. Sobel, V. K. Kuchroo, and A. H. Sharpe. 1999. Studies in B7-deficient mice reveal a critical role for B7 costimulation in both induction and effector phases of experimental autoimmune encephalomyelitis. J. Exp. Med. 190: 733-740. (Pubitemid 29428655)
24. Lohr, J., B. Knoechel, S. Jiang, A. H. Sharpe, and A. K. Abbas. 2003. The inhibitory function of B7 costimulators in T cell responses to foreign and selfantigens. Nat. Immunol. 4: 664-669. (Pubitemid 36874443)
25. Borriello, F., M. P. Sethna, S. D. Boyd, A. N. Schweitzer, E. A. Tivol, D. Jacoby, T. B. Strom, E. M. Simpson, G. J. Freeman, and A. H. Sharpe. 1997. B7-1 and B7-2 have overlapping, critical roles in immunoglobulin class switching and germinal center formation. Immunity 6: 303-313. (Pubitemid 27148597)
26. Chen, J., M. Trounstine, F. W. Alt, F. Young, C. Kurahara, J. F. Loring, and D. Huszar. 1993. Immunoglobulin gene rearrangement in B cell deficient mice generated by targeted deletion of the JH locus. Int. Immunol. 5: 647-656. (Pubitemid 23209419)
27. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17: 211-220. (Pubitemid 35245963)
28. Misra, N., J. Bayry, S. Lacroix-Desmazes, M. D. Kazatchkine, and S. V. Kaveri. 2004. Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J. Immunol. 172: 4676-4680. (Pubitemid 38456386)
29. Onishi, Y., Z. Fehervari, T. Yamaguchi, and S. Sakaguchi. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA 105: 10113-10118.
30. Wing, K., Y. Onishi, P. Prieto-Martin, T. Yamaguchi, M. Miyara, Z. Fehervari, T. Nomura, and S. Sakaguchi. 2008. CTLA-4 control over Foxp3+ regulatory T cell function. Science 322: 271-275.
31. Smit, J. J., D. M. Lindell, L. Boon, M. Kool, B. N. Lambrecht, and N. W. Lukacs. 2008. The balance between plasmacytoid DC versus conventional DC determines pulmonary immunity to virus infections. PLoS One 3: e1720.
32. Cederbom, L., H. Hall, and F. Ivars. 2000. CD4+CD25+ regulatory T cells downregulate co-stimulatory molecules on antigen-presenting cells. Eur. J. Immunol. 30: 1538-1543. (Pubitemid 30342794)
33. Darrasse-Jèze, G., S. Deroubaix, H. Mouquet, G. D. Victora, T. Eisenreich, K. H. Yao, R. F. Masilamani, M. L. Dustin, A. Rudensky, K. Liu, and M. C. Nussenzweig. 2009. Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J. Exp. Med. 206: 1853-1862.
34. Lau-Kilby, A. W., C. C. Kretz, S. Pechhold, J. D. Price, S. Dorta, H. Ramos, G. Trinchieri, and K. V. Tarbell. 2011. Interleukin-2 inhibits FMS-like tyrosine kinase 3 receptor ligand (flt3L)-dependent development and function of conventional and plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. USA 108: 2408-2413.