Interferon regulatory factor 8 integrates T-cell receptor and cytokine-signaling pathways and drives effector differentiation of CD8 T cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 30, 2012, Pages 12123-12128

  Miyagawa, Fumi ^a   Zhang, Hong ^a   Terunuma, Atshushi ^a   Ozato, Keiko ^b   Tagaya, Yutaka ^a,c   Katz, Stephen I ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

CD8 effector differentiation; Common c cytokine; Jak3; T cell receptor signaling; Transcription factors

Indexed keywords

EOMESODERMIN; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERLEUKIN 15; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; CYTOTOXICITY; DISEASE ACTIVITY; EFFECTOR CELL; GRAFT VERSUS HOST REACTION; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GRAFT VS HOST DISEASE; INTERFERON REGULATORY FACTORS; MICE; MICE, MUTANT STRAINS; MICROARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION;

EID: 84864355786     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201453109     Document Type: Article

References (41)

1. Dutton RW, Bradley LM, Swain SL (1998) T cell memory. Annu Rev Immunol 16: 201-223. (Pubitemid 28183364)
2. Murali-Krishna K, et al. (1998) Counting antigen-specific CD8 T cells: A reevaluation of bystander activation during viral infection. Immunity 8:177-187. (Pubitemid 28123745)
3. Homann D, Teyton L, Oldstone MB (2001) Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat Med 7:913-919. (Pubitemid 32756428)
4. Kaech SM, Wherry EJ, Ahmed R (2002) Effector and memory T-cell differentiation: Implications for vaccine development. Nat Rev Immunol 2:251-262. (Pubitemid 37323225)
5. Glimcher LH, Townsend MJ, Sullivan BM, Lord GM (2004) Recent developments in the transcriptional regulation of cytolytic effector cells. Nat Rev Immunol 4:900-911. (Pubitemid 39490765)
6. Williams MA, Bevan MJ (2007) Effector and memory CTL differentiation. Annu Rev Immunol 25:171-192. (Pubitemid 46697906)
7. Rutishauser RL, Kaech SM (2010) Generating diversity: Transcriptional regulation of effector and memory CD8 T-cell differentiation. Immunol Rev 235:219-233.
8. Kaech SM, Hemby S, Kersh E, Ahmed R (2002) Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111:837-851. (Pubitemid 36106405)
9. Sullivan BM, Juedes A, Szabo SJ, von Herrath M, Glimcher LH (2003) Antigen-driven effector CD8 T cell function regulated by T-bet. Proc Natl Acad Sci USA 100: 15818-15823. (Pubitemid 38021073)
10. Juedes AE, Rodrigo E, Togher L, Glimcher LH, von Herrath MG (2004) T-bet controls autoaggressive CD8 lymphocyte responses in type 1 diabetes. J ExpMed 199:1153-1162. (Pubitemid 38619911)
11. Pearce EL, et al. (2003) Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302:1041-1043. (Pubitemid 37386196)
12. Intlekofer AM, et al. (2005) Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6:1236-1244. (Pubitemid 43045635)
13. Miyagawa F, et al. (2008) IL-15 serves as a costimulator in determining the activity of autoreactive CD8 T cells in an experimental mouse model of graft-versus-host-like disease. J Immunol 181:1109-1119.
14. Miyagawa F, Gutermuth J, Zhang H, Katz SI (2010) The use of mouse models to better understand mechanisms of autoimmunity and tolerance. J Autoimmun 35:192-198.
15. Rochman Y, Spolski R, Leonard WJ (2009) New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev Immunol 9:480-490.
16. Tamura T, Yanai H, Savitsky D, Taniguchi T (2008) The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 26:535-584. (Pubitemid 351600385)
17. Driggers PH, et al. (1990) An interferon gamma-regulated protein that binds the interferon-inducible enhancer element of major histocompatibility complex class I genes. Proc Natl Acad Sci USA 87:3743-3747.
18. Nelson N, et al. (1996) Expression of IFN regulatory factor family proteins in lymphocytes. Induction of Stat-1 and IFN consensus sequence binding protein expression by T cell activation. J Immunol 156:3711-3720. (Pubitemid 26137656)
19. Schiavoni G, et al. (2002) ICSBP is essential for the development of mouse type I interferon-producing cells and for the generation and activation of CD8alpha(+) dendritic cells. J Exp Med 196:1415-1425. (Pubitemid 35424936)
20. Aliberti J, et al. (2003) Essential role for ICSBP in the in vivo development of murine CD8alpha + dendritic cells. Blood 101:305-310. (Pubitemid 36025923)
21. Tsujimura H, Tamura T, Ozato K (2003) Cutting edge: IFN consensus sequence binding protein/IFN regulatory factor 8 drives the development of type I IFN-producing plasmacytoid dendritic cells. J Immunol 170:1131-1135. (Pubitemid 36139475)
22. Holtschke T, et al. (1996) Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 87:307-317. (Pubitemid 26359008)
23. Tamura T, Nagamura-Inoue T, Shmeltzer Z, Kuwata T, Ozato K (2000) ICSBP directs bipotential myeloid progenitor cells to differentiate into mature macrophages. Immunity 13:155-165.
24. Lu R, Medina KL, Lancki DW, Singh H (2003) IRF-4,8 orchestrate the pre-B-to-B transition in lymphocyte development. Genes Dev 17:1703-1708. (Pubitemid 36870333)
25. Lee CH, et al. (2006) Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J Exp Med 203: 63-72.
26. Wang H, et al. (2008) IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood 112:4028-4038.
27. Ouyang X, et al. (2011) Transcription factor IRF8 directs a silencing programme for TH17 cell differentiation. Nat Commun 2:314.
28. Shibaki A, Sato A, Vogel JC, Miyagawa F, Katz SI (2004) Induction of GVHD-like skin disease by passively transferred CD8(+) T-cell receptor transgenic T cells into keratin 14-ovalbumin transgenic mice. J Invest Dermatol 123:109-115. (Pubitemid 38833471)
29. Changelian PS, et al. (2003) Prevention of organ allograft rejection by a specific Janus kinase 3 inhibitor. Science 302:875-878. (Pubitemid 37339629)
30. Ascherman DP, Migone TS, Friedmann MC, Leonard WJ (1997) Interleukin-2 (IL-2)-mediated induction of the IL-2 receptor alpha chain gene. Critical role of two functionally redundant tyrosine residues in the IL-2 receptor beta chain cytoplasmic domain and suggestion that these residues mediate more than Stat5 activation. J Biol Chem 272:8704-8709. (Pubitemid 27147838)
31. Welte T, et al. (1999) The PTK-STAT signaling pathway has essential roles in T-cell activation in response to antigen stimulation. Cold Spring Harb Symp Quant Biol 64: 291-302. (Pubitemid 30329291)
32. Sharpe AH (2009) Mechanisms of costimulation. Immunol Rev 229:5-11.
33. Cao X, et al. (1995) Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 2:223-238.
34. Nosaka T, et al. (1995) Defective lymphoid development in mice lacking Jak3. Science 270:800-802.
35. Thomis DC, Gurniak CB, Tivol E, Sharpe AH, Berg LJ (1995) Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 270:794-797.
36. Valitutti S, Müller S, Dessing M, Lanzavecchia A (1996) Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J Exp Med 183:1917-1921. (Pubitemid 26134333)
37. Auphan-Anezin N, Verdeil G, Schmitt-Verhulst AM (2003) Distinct thresholds for CD8 T cell activation lead to functional heterogeneity: CD8 T cell priming can occur independently of cell division. J Immunol 170:2442-2448. (Pubitemid 36245632)
38. Waldmann TA, Tagaya Y (1999) The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol 17:19-49. (Pubitemid 29241118)
39. Dubois S, Mariner J, Waldmann TA, Tagaya Y (2002) IL-15Ralpha recycles and presents IL-15 in trans to neighboring cells. Immunity 17:537-547. (Pubitemid 35351500)
40. Lodolce JP, Burkett PR, Boone DL, Chien M, Ma A (2001) T cell-independent interleukin 15Ralpha signals are required for bystander proliferation. J Exp Med 194: 1187-1194.
41. Committee on Care and Use of Laboratory Animals (1985) Guide for the Care and Use of Laboratory Animals (Natl Inst Health, Bethesda), DHHS Publ No (NIH) 85-23.