Molecular control of Tfh-cell differentiation by Roquin family proteins

Immunological Reviews

Volumn 253, Issue 1, 2013, Pages 273-289

  Heissmeyer, Vigo ^a,b   Vogel, Katharina U ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Autoimmunity; Induced mRNA decay; Post transcriptional gene regulation; RNA binding proteins; Roquin

Indexed keywords

CD28 ANTIGEN; GAMMA INTERFERON; ICOS PROTEIN; MESSENGER RNA; OX40 LIGAND; RNA BINDING PROTEIN; ROQUIN 1; ROQUIN 2; T LYMPHOCYTE RECEPTOR; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANTIGEN PRESENTING CELL; AUTOIMMUNE DIABETES; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CYTOKINE RELEASE; GENE ACTIVATION; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; GENE TARGETING; HELPER CELL; HUMAN; HYPERGAMMAGLOBULINEMIA; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOGENESIS; LUPUS LIKE SYNDROME; LYMPHOCYTE DIFFERENTIATION; MOLECULAR GENETICS; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA BINDING; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE TOLERANCE; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, KNOCKOUT; MOLECULAR TARGETED THERAPY; MUTATION; OX40 LIGAND; REPRESSOR PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER; TRANS-ACTIVATORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84875777618     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12056     Document Type: Review

References (72)

1. Vinuesa CG, et al. A RING-type ubiquitin ligase family member required to repress Tfh cells and autoimmunity. Nature 2005;435:452-458.
2. Tafuri A, et al. ICOS is essential for effective T-helper-cell responses. Nature 2001;409:105-109.
3. Dong C, Temann UA, Flavell RA. Cutting edge: critical role of inducible costimulator in germinal center reactions. J Immunol 2001;166:3659-3662.
4. Bossaller L, et al. ICOS deficiency is associated with a severe reduction of CXCR5+CD4 germinal center Th cells. J Immunol 2006;177:4927-4932.
5. Yu D, et al. Roquin represses autoimmunity by limiting inducible T-cell co-stimulator messenger RNA. Nature 2007;450:299-303.
6. Bertossi A, et al. Loss of Roquin induces early death and immune deregulation but not autoimmunity. J Exp Med 2011;208:1749-1756.
7. Vogel KU, et al. Combined loss of Rc3h1 and Rc3h2 derepresses Icos and Ox40 target mRNAs and imposes Tfh differentiation on CD4 (+) T cells. Immunity 2013; in press.
8. Siess DC, et al. A human gene coding for a membrane-associated nucleic acid-binding protein. J Biol Chem 2000;275:33655-33662.
9. Schaefer JS, Montufar-Solis D, Vigneswaran N, Klein JR. Selective upregulation of microRNA expression in peripheral blood leukocytes in IL-10-/- mice precedes expression in the colon. J Immunol 2011;187:5834-5841.
10. Athanasopoulos V, et al. The ROQUIN family of proteins localizes to stress granules via the ROQ domain and binds target mRNAs. FEBS J 2010;277:2109-2127.
11. Glasmacher E, et al. Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression. Nat Immunol 2010;11:725-733.
12. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 1999;19:4311-4323.
13. Li W, Gao B, Lee SM, Bennett K, Fang D. RLE-1, an E3 ubiquitin ligase, regulates C. elegans aging by catalyzing DAF-16 polyubiquitination. Dev Cell 2007;12:235-246.
14. Laroia G, Sarkar B, Schneider RJ. Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc Natl Acad Sci USA 2002;99:1842-1846.
15. Cano F, et al. The RNA-binding E3 ubiquitin ligase MEX-3C links ubiquitination with MHC-I mRNA degradation. EMBO J 2012;31:3596-3606.
16. Linterman MA, et al. Tfh cells are required for systemic autoimmunity. J Exp Med 2009;206:561-576.
17. Silva DG, et al. Anti-islet autoantibodies trigger autoimmune diabetes in the presence of an increased frequency of islet-reactive CD4 T cells. Diabetes 2011;60:2102-2111.
18. Goodnow CC. Multistep pathogenesis of autoimmune disease. Cell 2007;130:25-35.
19. Ellyard JI, et al. Heterozygosity for Roquinsan leads to angioimmunoblastic T-cell lymphoma-like tumors in mice. Blood 2012;120:812-821.
20. Burmeister Y, et al. ICOS controls the pool size of effector-memory and regulatory T cells. J Immunol 2008;180:774-782.
21. Yoshinaga SK, et al. T-cell co-stimulation through B7RP-1 and ICOS. Nature 1999;402:827-832.
22. Rudd CE, Schneider H. Unifying concepts in CD28, ICOS and CTLA4 co-receptor signalling. Nat Rev Immunol 2003;3:544-556.
23. Walker LS, et al. Compromised Ox40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J Exp Med 1999;190:1115-1122.
24. Ferguson SE, Han S, Kelsoe G, Thompson CB. CD28 is required for germinal center formation. J Immunol 1996;156:4576-4581.
25. Shahinian A, et al. Differential T cell costimulatory requirements in CD28-deficient mice. Science 1993;261:609-612.
26. Crotty S, Kersh EN, Cannons J, Schwartzberg PL, Ahmed R. SAP is required for generating long-term humoral immunity. Nature 2003;421:282-287.
27. Aversa G, et al. SLAM and its role in T cell activation and Th cell responses. Immunol Cell Biol 1997;75:202-205.
28. Sayos J, et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 1998;395:462-469.
29. Akiba H, et al. The role of ICOS in the CXCR5 + follicular B helper T cell maintenance in vivo. J Immunol 2005;175:2340-2348.
30. Bauquet AT, et al. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat Immunol 2009;10:167-175.
31. Yusuf I, et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J Immunol 2010;185:190-202.
32. Linterman MA, et al. Roquin differentiates the specialized functions of duplicated T cell costimulatory receptor genes CD28 and ICOS. Immunity 2009;30:228-241.
33. Lee SK, et al. Interferon-gamma Excess Leads to Pathogenic Accumulation of Tfh Cells and Germinal Centers. Immunity 2012;37:880-892.
34. Herman AE, Freeman GJ, Mathis D, Benoist C. CD4 + CD25 + T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J Exp Med 2004;199:1479-1489.
35. Whitmire JK, Tan JT, Whitton JL. Interferon-gamma acts directly on CD8 + T cells to increase their abundance during virus infection. J Exp Med 2005;201:1053-1059.
36. Bhatnagar A, Wig JD, Majumdar S. Expression of activation, adhesion molecules and intracellular cytokines in acute pancreatitis. Immunol Lett 2001;77:133-141.
37. Bisping G, et al. Patients with inflammatory bowel disease (IBD) reveal increased induction capacity of intracellular interferon-gamma (IFN-gamma) in peripheral CD8 + lymphocytes co-cultured with intestinal epithelial cells. Clin Exp Immunol 2001;123:15-22.
38. Blanco P, Pitard V, Viallard JF, Taupin JL, Pellegrin JL, Moreau JF. Increase in activated CD8 + T lymphocytes expressing perforin and granzyme B correlates with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 2005;52:201-211.
39. Suzuki T, et al. Cytotoxic molecules expressed by intraepithelial lymphocytes may be involved in the pathogenesis of acute gastric mucosal lesions. J Gastroenterol 2003;38:216-221.
40. Chang PP, et al. Breakdown in repression of IFN-gamma mRNA leads to accumulation of self-reactive effector CD8 + T cells. J Immunol 2012;189:701-710.
41. Mestas J, Crampton SP, Hori T, Hughes CC. Endothelial cell co-stimulation through Ox40 augments and prolongs T cell cytokine synthesis by stabilization of cytokine mRNA. Int Immunol 2005;17:737-747.
42. Grumont RJ, Gerondakis S. Rel induces interferon regulatory factor 4 (IRF-4) expression in lymphocytes: modulation of interferon-regulated gene expression by rel/nuclear factor kappaB. J Exp Med 2000;191:1281-1292.
43. Bollig N, et al. Transcription factor IRF4 determines germinal center formation through follicular T-helper cell differentiation. Proc Natl Acad Sci USA 2012;109:8664-8669.
44. Kwon H, et al. Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity 2009;31:941-952.
45. Klein U, et al. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol 2006;7:773-882.
46. Mittrucker HW, et al. Requirement for the transcription factor LSIRF/IRF4 for mature B and T lymphocyte function. Science 1997;275:540-543.
47. Zheng Y, et al. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 2009;458:351-356.
48. Fanzo JC, et al. Loss of IRF-4-binding protein leads to the spontaneous development of systemic autoimmunity. J Clin Invest 2006;116:703-714.
49. Chen Q, et al. IRF-4-binding protein inhibits interleukin-17 and interleukin-21 production by controlling the activity of IRF-4 transcription factor. Immunity 2008;29:899-911.
50. Croft M. Control of immunity by the TNFR-related molecule Ox40 (CD134). Annu Rev Immunol 2010;28:57-78.
51. Bansal-Pakala P, Jember AG, Croft M. Signaling through Ox40 (CD134) breaks peripheral T-cell tolerance. Nat Med 2001;7:907-912.
52. Gaspal F, et al. Abrogation of CD30 and Ox40 signals prevents autoimmune disease in FoxP3-deficient mice. J Exp Med 2011;208:1579-1584.
53. Brocker T, Gulbranson-Judge A, Flynn S, Riedinger M, Raykundalia C, Lane P. CD4 T cell traffic control: in vivo evidence that ligation of Ox40 on CD4 T cells by Ox40-ligand expressed on dendritic cells leads to the accumulation of CD4 T cells in B follicles. Eur J Immunol 1999;29:1610-1616.
54. Flynn S, Toellner KM, Raykundalia C, Goodall M, Lane P. CD4 T cell cytokine differentiation: the B cell activation molecule, Ox40 ligand, instructs CD4 T cells to express interleukin 4 and upregulates expression of the chemokine receptor, Blr-1. J Exp Med 1998;188:297-304.
55. Choi YS, et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 2011;34:932-946.
56. Simpson TR, Quezada SA, Allison JP. Regulation of CD4 T cell activation and effector function by inducible costimulator (ICOS). Curr Opin Immunol 2010;22:326-332.
57. Weinberg AD. The role of Ox40 (CD134) in T-cell memory generation. Adv Exp Med Biol 2010;684:57-68.
58. Murata K, Nose M, Ndhlovu LC, Sato T, Sugamura K, Ishii N. Constitutive Ox40/Ox40 ligand interaction induces autoimmune-like diseases. J Immunol 2002;169:4628-4636.
59. Gigoux M, et al. Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase. Proc Natl Acad Sci USA 2009;106:20371-20376.
60. Murray SE, et al. NF-kappaB-inducing kinase plays an essential T cell-intrinsic role in graft-versus-host disease and lethal autoimmunity in mice. J Clin Invest 2011;121:4775-4786.
61. So T, Choi H, Croft M. Ox40 complexes with phosphoinositide 3-kinase and protein kinase B (PKB) to augment TCR-dependent PKB signaling. J Immunol 2011;186:3547-3555.
62. Rolf J, et al. Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J Immunol 2010;185:4042-4052.
63. Nakayamada S, et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011;35:919-931.
64. Lu KT, et al. Functional and epigenetic studies reveal multistep differentiation and plasticity of in vitro-generated and in vivo-derived follicular T helper cells. Immunity 2011;35:622-632.
65. Parker R, Song H. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 2004;11:121-127.
66. Tharun S, He W, Mayes AE, Lennertz P, Beggs JD, Parker R. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 2000;404:515-518.
67. Song MG, Kiledjian M. 3′ Terminal oligo U-tract-mediated stimulation of decapping. RNA 2007;13:2356-2365.
68. Hoefig KP, et al. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to inducereplication-dependent decay. Nat Struct Mol Biol 2013;20:73-81.
69. Mullen TE, Marzluff WF. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′′. Genes Dev 2008;22:50-65.
70. Coller J, Parker R. General translational repression by activators of mRNA decapping. Cell 2005;122:875-886.
71. Macian F, Garcia-Cozar F, Im SH, Horton HF, Byrne MC, Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002;109:719-731.
72. Heissmeyer V, et al. Calcineurin imposes T cell unresponsiveness through targeted proteolysis of signaling proteins. Nat Immunol 2004;5:255-265.