Transmembrane TNF-TNFR2 impairs Th17 differentiation by promoting Il2 expression

Journal of Immunology

Volumn 195, Issue 6, 2015, Pages 2633-2647

  Miller, Patrick G ^a   Bonn, Michael B ^a   McKarns, Susan C ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 2; MESSENGER RNA; STAT3 PROTEIN; STAT5 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; ETANERCEPT; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; IMMUNOSUPPRESSIVE AGENT; STAT3 PROTEIN, MOUSE; TNFRSF1A PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FOXP3 GENE; GENE; GENE EXPRESSION; GFP GENE; HOST RESISTANCE; IL2 GENE; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LOSS OF FUNCTION MUTATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY T LYMPHOCYTE; RNA STABILITY; TH17 CELL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; AUTOIMMUNITY; CELL DIFFERENTIATION; ETANERCEPT; FORKHEAD TRANSCRIPTION FACTORS; GREEN FLUORESCENT PROTEINS; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-17; INTERLEUKIN-2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TH17 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84941778190     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500286     Document Type: Article

References (76)

1. Boyman, O., and J. Sprent. 2012. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12: 180-190.
2. Sadlack, B., H. Merz, H. Schorle, A. Schimpl, A. C. Feller, and I. Horak. 1993. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell 75: 253-261.
3. Suzuki, H., T. M. Kündig, C. Furlonger, A. Wakeham, E. Timms, T. Matsuyama, R. Schmits, J. J. Simard, P. S. Ohashi, H. Griesser, et al. 1995. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor beta. Science 268: 1472-1476.
4. Liao, W., J. X. Lin, and W. J. Leonard. 2011. IL-2 family cytokines: new insights into the complex roles of IL-2 as a broad regulator of T helper cell differentiation. Curr. Opin. Immunol. 23: 598-604.
5. Cheng, G., A. Yu, and T. R. Malek. 2011. T-cell tolerance and the multi-functional role of IL-2R signaling in T-regulatory cells. Immunol. Rev. 241: 63-76.
6. Shevach, E. M. 2009. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30: 636-645.
7. Pipkin, M. E., J. A. Sacks, F. Cruz-Guilloty, M. G. Lichtenheld, M. J. Bevan, and A. Rao. 2010. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32: 79-90.
8. Liao, W., J.-X. Lin, and W. J. Leonard. 2013. Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 38: 13-25.
9. Ballesteros-Tato, A., B. León, B. A. Graf, A. Moquin, P. S. Adams, F. E. Lund, and T. D. Randall. 2012. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity 36: 847-856.
10. Wells, A. D. 2009. New insights into the molecular basis of T cell anergy: anergy factors, avoidance sensors, and epigenetic imprinting. J. Immunol. 182: 7331-7341.
11. Malek, T. R., and I. Castro. 2010. Interleukin-2 receptor signaling: at the interface between tolerance and immunity. Immunity 33: 153-165.
12. McKarns, S. C., and R. H. Schwartz. 2008. Biphasic regulation of Il2 transcription in CD4+ T cells: roles for TNF-alpha receptor signaling and chromatin structure. J. Immunol. 181: 1272-1281.
13. Kim, E. Y., and H. S. Teh. 2004. Critical role of TNF receptor type-2 (p75) as a costimulator for IL-2 induction and T cell survival: a functional link to CD28. J. Immunol. 173: 4500-4509.
14. Kim, E. Y., and H. S. Teh. 2001. TNF type 2 receptor (p75) lowers the threshold of T cell activation. J. Immunol. 167: 6812-6820.
15. Black, R. A., C. T. Rauch, C. J. Kozlosky, J. J. Peschon, J. L. Slack, M. F. Wolfson, B. J. Castner, K. L. Stocking, P. Reddy, S. Srinivasan, et al. 1997. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385: 729-733.
16. Grell, M. 1995-1996. Tumor necrosis factor (TNF) receptors in cellular signaling of soluble and membrane-expressed TNF. J. Inflamm. 47: 8-17.
17. Grell, M., E. Douni, H. Wajant, M. Löhden, M. Clauss, B. Maxeiner, S. Georgopoulos, W. Lesslauer, G. Kollias, K. Pfizenmaier, and P. Scheurich. 1995. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 83: 793-802.
18. Micheau, O., and J. Tschopp. 2003. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114: 181-190.
19. Häcker, H., P. H. Tseng, and M. Karin. 2011. Expanding TRAF function: TRAF3 as a tri-faced immune regulator. Nat. Rev. Immunol. 11: 457-468.
20. Höfer, T., O. Krichevsky, and G. Altan-Bonnet. 2012. Competition for IL-2 between Regulatory and Effector T Cells to Chisel Immune Responses. Front. Immunol. 3: 268.
21. Wang, X., Y. Zhang, X. O. Yang, R. I. Nurieva, S. H. Chang, S. S. Ojeda, H. S. Kang, K. S. Schluns, J. Gui, A. M. Jetten, and C. Dong. 2012. Transcription of Il17 and Il17f is controlled by conserved noncoding sequence 2. Immunity 36: 23-31.
22. Pappu, B. P., A. Borodovsky, T. S. Zheng, X. Yang, P. Wu, X. Dong, S. Weng, B. Browning, M. L. Scott, L.Ma, et al. 2008. TL1A-DR3 interaction regulates Th17 cell function and Th17-mediated autoimmune disease. J. Exp. Med. 205: 1049-1062.
23. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
24. Seder, R. A., W. E. Paul, M. M. Davis, and B. Fazekas de St Groth. 1992. The presence of interleukin 4 during in vitro priming determines the lymphokineproducing potential of CD4+ T cells from T cell receptor transgenic mice. J. Exp. Med. 176: 1091-1098.
25. Naramura, M., R. J. Hu, and H. Gu. 1998. Mice with a fluorescent marker for interleukin 2 gene activation. Immunity 9: 209-216.
26. Peschon, J. J., D. S. Torrance, K. L. Stocking, M. B. Glaccum, C. Otten, C. R. Willis, K. Charrier, P. J. Morrissey, C. B. Ware, and K. M. Mohler. 1998. TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J. Immunol. 160: 943-952.
27. Alexopoulou, L., K. Kranidioti, S. Xanthoulea, M. Denis, A. Kotanidou, E. Douni, P. J. Blackshear, D. L. Kontoyiannis, and G. Kollias. 2006. Transmembrane TNF protects mutant mice against intracellular bacterial infections, chronic inflammation and autoimmunity. Eur. J. Immunol. 36: 2768-2780.
28. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
29. Steed, P. M., M. G. Tansey, J. Zalevsky, E. A. Zhukovsky, J. R. Desjarlais, D. E. Szymkowski, C. Abbott, D. Carmichael, C. Chan, L. Cherry, et al. 2003. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants. Science 301: 1895-1898.
30. Zalevsky, J., T. Secher, S. A. Ezhevsky, L. Janot, P. M. Steed, C. O'Brien, A. Eivazi, J. Kung, D. H. Nguyen, S. K. Doberstein, et al. 2007. Dominantnegative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J. Immunol. 179: 1872-1883.
31. Goffe, B., and J. C. Cather. 2003. Etanercept: An overview. J. Am. Acad. Dermatol. 49(2, Suppl.) S105-S111.
32. Victoratos, P., and G. Kollias. 2009. Induction of autoantibody-mediated spontaneous arthritis critically depends on follicular dendritic cells. Immunity 30: 130-142.
33. Murray, K. M., and S. L. Dahl. 1997. Recombinant human tumor necrosis factor receptor (p75) Fc fusion protein (TNFR:Fc) in rheumatoid arthritis. Ann. Pharmacother. 31: 1335-1338.
34. Pang, L., L. Wang, T. Suo, H. Hao, X. Fang, J. Jia, F. Huang, and J. Tang. 2008. Tumor necrosis factor-alpha blockade leads to decreased peripheral T cell reactivity and increased dendritic cell number in peripheral blood of patients with ankylosing spondylitis. J. Rheumatol. 35: 2220-2228.
35. Cowley, S. C., J. D. Sedgwick, and K. L. Elkins. 2007. Differential requirements by CD4+ and CD8+ T cells for soluble and membrane TNF in control of Francisella tularensis live vaccine strain intramacrophage growth. J. Immunol. 179: 7709-7719.
36. Green, L. C., D. A. Wagner, J. Glogowski, P. L. Skipper, J. S. Wishnok, and S. R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126: 131-138.
37. Pandiyan, P., H. R. Conti, L. Zheng, A. C. Peterson, D. R. Mathern, N. Hernández-Santos, M. Edgerton, S. L. Gaffen, and M. J. Lenardo. 2011. CD4(+)CD25(+)Foxp3(+) regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity 34: 422-434.
38. Sanchez-Lockhart, M., and J. Miller. 2006. Engagement of CD28 outside of the immunological synapse results in up-regulation of IL-2 mRNA stability but not IL-2 transcription. J. Immunol. 176: 4778-4784.
39. Umlauf, S. W., B. Beverly, O. Lantz, and R. H. Schwartz. 1995. Regulation of interleukin 2 gene expression by CD28 costimulation in mouse T-cell clones: both nuclear and cytoplasmic RNAs are regulated with complex kinetics. Mol. Cell. Biol. 15: 3197-3205.
40. Chen, C. Y., F. Del Gatto-Konczak, Z. Wu, and M. Karin. 1998. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280: 1945-1949.
41. Chen, D., and E. V. Rothenberg. 1994. Interleukin 2 transcription factors as molecular targets of cAMP inhibition: delayed inhibition kinetics and combinatorial transcription roles. J. Exp. Med. 179: 931-942.
42. Emmel, E. A., C. L. Verweij, D. B. Durand, K. M. Higgins, E. Lacy, and G. R. Crabtree. 1989. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science 246: 1617-1620.
43. Ragheb, J. A., M. Deen, and R. H. Schwartz. 1999. CD28-Mediated regulation of mRNA stability requires sequences within the coding region of the IL-2 mRNA. J. Immunol. 163: 120-129.
44. Xu, L., J. Yang, Y. Huang, P. H. van der Meide, M. Levi, B. Wahren, H. Link, and B. Xiao. 2000. Limitation of nitric oxide production: cells from lymph node and spleen exhibit distinct difference in nitric oxide production. Immunol. Lett. 71: 177-184.
45. Shibata, H., Y. Abe, Y. Yoshioka, T. Nomura, M. Sato, H. Kayamuro, T. Kawara, S. Arita, T. Furuya, K. Nagano, et al. 2010. Generation of mouse macrophages expressing membrane-bound TNF variants with selectivity for TNFR1 or TNFR2. Cytokine 50: 75-83.
46. Umlauf, S. W., B. Beverly, S. M. Kang, K. Brorson, A. C. Tran, and R. H. Schwartz. 1993. Molecular regulation of the IL-2 gene: rheostatic control of the immune system. Immunol. Rev. 133: 177-197.
47. Trevejo, J. M., M. W. Marino, N. Philpott, R. Josien, E. C. Richards, K. B. Elkon, and E. Falck-Pedersen. 2001. TNF-alpha-dependent maturation of local dendritic cells is critical for activating the adaptive immune response to virus infection. Proc. Natl. Acad. Sci. USA 98: 12162-12167.
48. Maney, N. J., G. Reynolds, A. Krippner-Heidenreich, and C. M. Hilkens. 2014. Dendritic cell maturation and survival are differentially regulated by TNFR1 and TNFR2. J. Immunol. 193: 4914-4923.
49. Tang, W., Y. Lu, Q. Y. Tian, Y. Zhang, F. J. Guo, G. Y. Liu, N. M. Syed, Y. Lai, E. A. Lin, L. Kong, et al. 2011. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 332: 478-484.
50. Schwartz, R. H. 1997. T cell clonal anergy. Curr. Opin. Immunol. 9: 351-357.
51. Rothenberg, E. V., and S. B. Ward. 1996. A dynamic assembly of diverse transcription factors integrates activation and cell-type information for interleukin 2 gene regulation. Proc. Natl. Acad. Sci. USA 93: 9358-9365.
52. Rao, S., S. Gerondakis, D. Woltring, and M. F. Shannon. 2003. c-Rel is required for chromatin remodeling across the IL-2 gene promoter. J. Immunol. 170: 3724-3731.
53. Chen, C. Y., R. Gherzi, J. S. Andersen, G. Gaietta, K. Jürchott, H. D. Royer, M. Mann, and M. Karin. 2000. Nucleolin and YB-1 are required for JNKmediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14: 1236-1248.
54. McKarns, S. C., R. H. Schwartz, and N. E. Kaminski. 2004. Smad3 is essential for TGF-beta 1 to suppress IL-2 production and TCR-induced proliferation, but not IL-2-induced proliferation. J. Immunol. 172: 4275-4284.
55. Verrecchia, F., M. Pessah, A. Atfi, and A. Mauviel. 2000. Tumor necrosis factor-alpha inhibits transforming growth factor-beta/Smad signaling in human dermal fibroblasts via AP-1 activation. J. Biol. Chem. 275: 30226-30231.
56. Laurence, A., C. M. Tato, T. S. Davidson, Y. Kanno, Z. Chen, Z. Yao, R. B. Blank, F. Meylan, R. Siegel, L. Hennighausen, et al. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26: 371-381.
57. Chen, X., J. J. Subleski, H. Kopf, O. M. Howard, D. N. Männel, and J. J. Oppenheim. 2008. Cutting edge: expression of TNFR2 defines a maximally suppressive subset of mouse CD4+CD25+FoxP3+ T regulatory cells: applicability to tumor-infiltrating T regulatory cells. J. Immunol. 180: 6467-6471.
58. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
59. Quintana, F. J., A. S. Basso, A. H. Iglesias, T. Korn, M. F. Farez, E. Bettelli, M. Caccamo, M. Oukka, and H. L. Weiner. 2008. Control of T(reg) and T(H) 17 cell differentiation by the aryl hydrocarbon receptor. Nature 453: 65-71.
60. Liao, W., J. X. Lin, L. Wang, P. Li, and W. J. Leonard. 2011. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12: 551-559.
61. Yang, X. P., K. Ghoreschi, S. M. Steward-Tharp, J. Rodriguez-Canales, J. Zhu, J. R. Grainger, K. Hirahara, H. W. Sun, L. Wei, G. Vahedi, et al. 2011. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12: 247-254.
62. Basu, R., S. K. Whitley, S. Bhaumik, C. L. Zindl, T. R. Schoeb, E. N. Benveniste, W. S. Pear, R. D. Hatton, and C. T. Weaver. 2015. IL-1 signaling modulates activation of STAT transcription factors to antagonize retinoic acid signaling and control the TH17 cell-iTreg cell balance. Nat. Immunol. 16: 286-295.
63. The Lenercept Multiple Sclerosis Study Group and The University of British Columbia MS/MRI Analysis Group. 1999. TNF neutralization in MS: results of a randomized, placebo-controlled multicenter study. Neurology 53: 457-465.
64. Okubo, Y., T. Mera, L. Wang, and D. L. Faustman. 2013. Homogeneous expansion of human T-regulatory cells via tumor necrosis factor receptor 2. Sci. Rep. 3: 3153.
65. Chen, X., X.Wu, Q. Zhou, O.M. Howard, M. G. Netea, and J. J. Oppenheim. 2013. TNFR2 is critical for the stabilization of the CD4+Foxp3+ regulatory T. cell phenotype in the inflammatory environment. J. Immunol. 190: 1076-1084.
66. Sacca, R., C. A. Cuff, W. Lesslauer, and N. H. Ruddle. 1998. Differential activities of secreted lymphotoxin-alpha3 and membrane lymphotoxinalpha1beta2 in lymphotoxin-induced inflammation: critical role of TNF receptor 1 signaling. J. Immunol. 160: 485-491.
67. Zhu, M., N. K. Brown, and Y. X. Fu. 2010. Direct and indirect roles of the LTbetaR pathway in central tolerance induction. Trends Immunol. 31: 325-331.
68. Crowe, P. D., T. L. VanArsdale, B. N. Walter, C. F. Ware, C. Hession, B. Ehrenfels, J. L. Browning, W. S. Din, R. G. Goodwin, and C. A. Smith. 1994. A lymphotoxin-beta-specific receptor. Science 264: 707-710.
69. Wu, H., and R. M. Siegel. 2011. Medicine. Progranulin resolves inflammation. Science 332: 427-428.
70. Caamano, J., and C. A. Hunter. 2002. NF-kappaB family of transcription factors: central regulators of innate and adaptive immune functions. Clin. Microbiol. Rev. 15: 414-429.
71. Banerjee, D., H. C. Liou, and R. Sen. 2005. c-Rel-dependent priming of naive T cells by inflammatory cytokines. Immunity 23: 445-458.
72. Zhou, X. Y., Y. Yashiro-Ohtani, M. Nakahira, W. R. Park, R. Abe, T. Hamaoka, M. Naramura, H. Gu, and H. Fujiwara. 2002. Molecular mechanisms underlying differential contribution of CD28 versus non-CD28 costimulatory molecules to IL-2 promoter activation. J. Immunol. 168: 3847-3854.
73. Gramaglia, I., A. Jember, S. D. Pippig, A. D. Weinberg, N. Killeen, and M. Croft. 2000. The OX40 costimulatory receptor determines the development of CD4 memory by regulating primary clonal expansion. J. Immunol. 165: 3043-3050.
74. Ruddle, N. H., and E. M. Akirav. 2009. Secondary lymphoid organs: responding to genetic and environmental cues in ontogeny and the immune response. J. Immunol. 183: 2205-2212.
75. Tumanov, A. V., S. I. Grivennikov, A. A. Kruglov, Y. V. Shebzukhov, E. P. Koroleva, Y. Piao, C. Y. Cui, D. V. Kuprash, and S. A. Nedospasov. 2010. Cellular source and molecular form of TNF specify its distinct functions in organization of secondary lymphoid organs. Blood 116: 3456-3464.
76. Green, D. M., J. Trial, and H. H. Birdsall. 1998. TNF-a released by comigrating monocytes promotes transendothelial migration of activated lymphocytes. J. Immunol. 161: 2481-2489.