Intestinal dendritic cells specialize to activate transforming growth factor-β and induce Foxp3+ regulatory T cells via integrin αvβ8

Gastroenterology

Volumn 141, Issue 5, 2011, Pages 1802-1812

  Worthington, John J ^a   Czajkowska, Beata I ^a   Melton, Andrew C ^b   Travis, Mark A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Immune Response; Inflammatory Response; Self Tolerance; Signaling; T Cell Regulation

Indexed keywords

CD51 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; IMMUNITY; IN VITRO STUDY; INTESTINE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; UPREGULATION;

EID: 80054866424     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.06.057     Document Type: Article

References (38)

1. Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science 2001;292:1115-1118. (Pubitemid 32440925)
2. Barnes MJ, Powrie F. Regulatory T cells reinforce intestinal homeostasis. Immunity 2009;31:401-411.
3. de Lafaille MAC, Lafaille JJ. Natural and adaptive Foxp3(+) regulatory T Cells: More of the same or a division of labor? Immunity 2009;30:626-635.
4. Chen WJ, Jin WW, Hardegen N, et al. Conversion of peripheral CD4(+)CD25(-) naive T cells to CD4(+)CD25(+) regulatory T cells by TGF-β induction of transcription factor Foxp3. J Exp Med 2003;198:1875-1886. (Pubitemid 38032120)
5. Belkaid Y, Oldenhove G. Tuning microenvironments: Induction of regulatory T cells by dendritic cells. Immunity 2008;29:362-371.
6. Coombes JL, Siddiqui KRR, Arancibia-Carcamo CV, et al. A functionally specialized population of mucosal CD103(+) DCs induces Foxp3(+) regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J Exp Med 2007;204:1757-1764. (Pubitemid 47236314)
7. Sun CM, Hall JA, Blank RB, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007;204:1775-1785. (Pubitemid 47236316)
8. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFβactivation. J Cell Sci 2003;116:217-224.
9. Travis MA, Reizis B, Melton AC, et al. Loss of integrin αvβ8 on dendritic cells causes autoimmunity and colitis in mice. Nature 2007;449:361-365. (Pubitemid 47443473)
10. Fontenot JD, Rasmussen JP, Williams LM, et al. Regulatory T cell lineage specification by the forkhead transcription factor FoxP3. Immunity 2005;22:329-341. (Pubitemid 40387475)
11. Weigmann B, Tubbe I, Seidel D, et al. Isolation and subsequent analysis of murine lamina propria mononuclear cells from colonic tissue. Nature Protocols 2007;2:2307-2311.
12. Abe M, Harpel JG, Metz CN, et al. An assay for transforming growth factor-β using cells transfected with a plasminogen-activator inhibitor-1 promoter luciferase construct. Anal Biochem 1994; 216:276-284. (Pubitemid 24076008)
13. Worthington JJ, Klementowicz JE, Travis MA. TGFβ: a sleeping giant awoken by integrins. Trends Biochem Sci 2011;36:47-54.
14. Robinson PW, Green SJ, Carter C, et al. Studies on transcriptional regulation of the mucosal T-cell integrin αEβ7 (CD103). Immunology 2001;103:146-154. (Pubitemid 32521343)
15. Persson EK, Jaensson E, Agace WW. The diverse ontogeny and function of murine small intestinal dendritic cell/macrophage subsets. Immunobiology 2010;215:692-697.
16. Letterio JJ, Roberts AB. Regulation of immune responses by TGFβ. Ann Rev Immun 1998;16:137-161.
17. Yang ZW, Mu ZY, Dabovic B, et al. Absence of integrin-mediated TGFβ1 activation in vivo recapitulates the phenotype of TGFβ1-null mice. J Cell Biol 2007;176:787-793. (Pubitemid 46425539)
18. Parks WC, Shapiro SD. Matrix metalloproteinases in lung biology. Resp Res 2001;2:10-19. (Pubitemid 34187902)
19. Crawford SE, Stellmach V, Murphy-Ullrich JE, et al. Thrombospondin-1 is a major activator of TGFβ1 in vivo. Cell 1998;93:1159-1170. (Pubitemid 28307421)
20. Carmeliet P, Schoonjans L, Kieckens L, et al. Physiological consequences of loss of plasminogen-activator gene-function in mice. Nature 1994;368:419-424. (Pubitemid 24115347)
21. Chen Y, Dabovic B, Colarossi C, et al. Growth retardation as well as spleen and thymus involution in latent TGFβ binding protein (Ltbp)-3 null mice. J Cell Physiol 2003;196:319-325. (Pubitemid 36775879)
22. Mu DZ, Cambier S, Fjellbirkeland L, et al. The integrin αvβ8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGFβ1. J Cell Biol 2002;157:493-507. (Pubitemid 34839812)
23. Li MO, Wan YSY, Flavell RA. T cell-produced transforming growth factor-β1 controls T cell tolerance and regulates Th1- and Th17- cell differentiation. Immunity 2007;26:579-591. (Pubitemid 46756347)
24. Benson MJ, Pino-Lagos K, Rosemblatt M, et al. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 2007;204:1765-1774. (Pubitemid 47236315)
25. Mucida D, Park Y, Kim G, et al. Reciprocal T(H)17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007; 317:256-260. (Pubitemid 47076203)
26. Elias KM, Laurence A, Davidson TS, et al. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat- 3/Stat-5 independent signaling pathway. Blood 2008;111:1013-1020. (Pubitemid 351213378)
27. Hill JA, Hall JA, Sun CM, et al. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4(+)CD44(hi) cells. Immunity 2008;29:758-770.
28. Kang SG, Lim HW, Andrisani OM, et al. Vitamin A metabolites induce gut-homing FoxP3(+) regulatory T cells. J Immunol 2007; 179:3724-3733.
29. Schambach F, Schupp M, Lazar MA, et al. Activation of retinoic acid receptor-alpha favours regulatory T cell induction at the expense of IL-17-secreting T helper cell differentiation. Eur J Immunol 2007;37:2396-2399. (Pubitemid 47423609)
30. Cha HR, Chang SY, Chang JH, et al. Downregulation of Th17 cells in the small intestine by disruption of gut Flora in the absence of retinoic acid. J Immunol 2010;184:6799-6806.
31. Li MO, Wan YY, Sanjabi S, et al. Transforming growth factor-β regulation of immune responses. Ann Rev Immunol 2006;24:99-146.
32. Acharya M, Mukhopadhyay S, Paidassi H, et al. αv Integrin expression by DCs is required for Th17 cell differentiation and development of experimental autoimmune encephalomyelitis in mice. J Clin Invest 2010;120:4445-4452.
33. Melton AC, Bailey-Bucktrout SL, Travis MA, et al. Expression of αvβ8 integrin on dendritic cells regulates Th17 cell development and experimental autoimmune encephalomyelitis in mice. J Clin Invest 2010;120:4436-4444.
34. Takaki H, Ichiyama K, Koga K, et al. STAT6 inhibits TGF-beta 1-mediated Foxp3 induction through direct binding to the Foxp3 promoter, which is reverted by retinoic acid receptor. J Biol Chem 2008;283:14955-14962.
35. Nolting J, Daniel C, Reuter S, et al. Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines. J Exp Med 2009;206:2131-2139.
36. Xiao S, Jin H, Korn T, et al. Retinoic acid increases Foxp3(+) regulatory T cells and inhibits development of Th17 cells by enhancing TGF-β-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J Immunol 2008;181:2277-2284.
37. Xu LL, Kitani A, Stuelten C, et al. Positive and negative transcriptional regulation of the Foxp3 gene is mediated by access and binding of the Smad3 protein to enhancer I. Immunity 2010;33:313-325.
38. Coombes JL, Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol 2008;8:435-446. (Pubitemid 351733420)