From the diet to the nucleus: Vitamin A and TGF-β join efforts at the mucosal interface of the intestine

Seminars in Immunology

Volumn 21, Issue 1, 2009, Pages 14-21

  Mucida, Daniel ^a   Park, Yunji ^a   Cheroutre, Hilde ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Foxp3; Gut tropism; Nuclear receptors; TH17; Vitamin A

Indexed keywords

CELL NUCLEUS RECEPTOR; INTERLEUKIN 17; ISOTRETINOIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOL; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

CELL DIFFERENTIATION; CELL NUCLEUS; DIET; HELPER CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INTESTINE MUCOSA; METABOLITE; PLEIOTROPY; REGULATORY T LYMPHOCYTE; REVIEW;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTINEOPLASTIC AGENTS; CELL NUCLEUS; DIET; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-17; INTESTINAL MUCOSA; RECEPTORS, RETINOIC ACID; T-LYMPHOCYTES, HELPER-INDUCER; TRANSFORMING GROWTH FACTOR BETA; TRETINOIN; VITAMIN A;

EID: 56249143761     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2008.08.001     Document Type: Review

References (83)

1. Burnet M.F. The clonal selection theory of immunity. 1st ed. (1959), The Vanderbilt and Cambridge University Presses, Nashville/London
2. Sakaguchi S., Takahashi T., and Nishizuka Y. Study on cellular events in post-thymectomy autoimmune oophoritis in mice. II. Requirement of Lyt-1 cells in normal female mice for the prevention of oophoritis. J Exp Med 156 6 (1982) 1577-1586
3. Sakaguchi S., Fukuma K., Kuribayashi K., and Masuda T. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med 161 1 (1985) 72-87
4. Sakaguchi S., Takahashi T., and Nishizuka Y. Study on cellular events in postthymectomy autoimmune oophoritis in mice. I. Requirement of Lyt-1 effector cells for oocytes damage after adoptive transfer. J Exp Med 156 6 (1982) 1565-1576
5. Taguchi O., Kontani K., Ikeda H., Kezuka T., Takeuchi M., Takahashi T., et al. Tissue-specific suppressor T cells involved in self-tolerance are activated extrathymically by self-antigens. Immunology 82 3 (1994) 365-369
6. Lafaille J.J., Nagashima K., Katsuki M., and Tonegawa S. High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 78 3 (1994) 399-408
7. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., and Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155 3 (1995) 1151-1164
8. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4(+)CD25(+) regulatory T cells. Nat Immunol 4 4 (2003) 330-336
9. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299 5609 (2003) 1057-1061
10. Brunkow M.E., Jeffery E.W., Hjerrild K.A., Paeper B., Clark L.B., Yasayko S.A., et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 27 1 (2001) 68-73
11. Bennett C.L., Christie J., Ramsdell F., Brunkow M.E., Ferguson P.J., Whitesell L., et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 27 1 (2001) 20-21
12. Cheroutre H. Starting at the beginning: new perspectives on the biology of mucosal T cells. Annu Rev Immunol 22 (2004) 217-246
13. Faria A.M., and Weiner H.L. Oral tolerance. Immunol Rev 206 1 (2005) 232-259
14. Vaz N.M. Immunological tolerance and dogma. Med Hypotheses 5 9 (1979) 1037-1043
15. Vaz N.M., Faria A.M., Verdolin B.A., Silva Neto A.F., Menezes J.S., and Carvalho C.R. The conservative physiology of the immune system. Braz J Med Biol Res 36 1 (2003) 13-22
16. Izcue A., Coombes J.L., and Powrie F. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol Rev 212 (2006) 256-271
17. + regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198 12 (2003) 1875-1886
18. - T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 172 9 (2004) 5149-5153
19. Apostolou I., and Von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med 199 10 (2004) 1401-1408
20. + regulatory T Cells by peripheral expansion. J Immunol 173 12 (2004)
21. Mucida D., Kutchukhidze N., Erazo A., Russo M., Lafaille J.J., and Curotto de Lafaille M.A. Oral tolerance in the absence of naturally occurring Tregs. J Clin Invest 115 7 (2005) 1923-1933
22. + regulatory T cell-dependent and -independent control of allergic inflammation. Immunity 29 1 (2008) 114-126
23. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317 5835 (2007) 256-260
24. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204 8 (2007) 1757-1764
25. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 204 8 (2007) 1775-1785
26. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2 4 (2001) 361-367
27. Jang M.H., Sougawa N., Tanaka T., Hirata T., Hiroi T., Tohya K., et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol 176 2 (2006) 803-810
28. Hanson D.G., Vaz N.M., Maia L.C., Hornbrook M.M., Lynch J.M., and Roy C.A. Inhibition of specific immune responses by feeding protein antigens. Int Arch Allergy Appl Immunol 55 1-6 (1977) 526-532
29. Worbs T., Bode U., Yan S., Hoffmann M.W., Hintzen G., Bernhardt G., et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203 3 (2006) 519-527
30. Li M.O., Wan Y.Y., Sanjabi S., Robertson A.K., and Flavell R.A. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24 (2006) 99-146
31. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 2 (2006) 179-189
32. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 7090 (2006) 235-238
33. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441 7090 (2006) 231-234
34. Kliewer S.A., Umesono K., Mangelsdorf D.J., and Evans R.M. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 355 6359 (1992) 446-449
35. Zhang X.K., Lehmann J., Hoffmann B., Dawson M.I., Cameron J., Graupner G., et al. Homodimer formation of retinoid X receptor induced by 9-cis retinoic acid. Nature 358 6387 (1992) 587-591
36. de Lera A.R., Bourguet W., Altucci L., and Gronemeyer H. Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat Rev Drug Discov 6 10 (2007) 811-820
37. Alroy I., Towers T.L., and Freedman L.P. Transcriptional repression of the interleukin-2 gene by vitamin D3: direct inhibition of NFATp/AP-1 complex formation by a nuclear hormone receptor. Mol Cell Biol 15 10 (1995) 5789-5799
38. Yu X.P., Bellido T., and Manolagas S.C. Down-regulation of NF-kappa B protein levels in activated human lymphocytes by 1,25-dihydroxyvitamin D3. Proc Natl Acad Sci USA 92 24 (1995) 10990-10994
39. Yanagisawa J., Yanagi Y., Masuhiro Y., Suzawa M., Watanabe M., Kashiwagi K., et al. Convergence of transforming growth factor-beta and vitamin D signaling pathways on SMAD transcriptional coactivators. Science 283 5406 (1999) 1317-1321
40. Barrat F.J., Cua D.J., Boonstra A., Richards D.F., Crain C., Savelkoul H.F., et al. In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J Exp Med 195 5 (2002) 603-616
41. Wang X., Allen C., and Ballow M. Retinoic acid enhances the production of IL-10 while reducing the synthesis of IL-12 and TNF-alpha from LPS-stimulated monocytes/macrophages. J Clin Immunol 27 2 (2007) 193-200
42. Sanchez-Martinez R., Zambrano A., Castillo A.I., and Aranda A. Vitamin D-dependent recruitment of corepressors to vitamin D/retinoid X receptor heterodimers. Mol Cell Biol 28 11 (2008) 3817-3829
43. Lee J.W., Bajwa P.J., Carson M.J., Jeske D.R., Cong Y., Elson C.O., et al. Fenofibrate represses interleukin-17 and interferon-gamma expression and improves colitis in interleukin-10-deficient mice. Gastroenterology 133 1 (2007) 108-123
44. Fensterl V., Grotheer D., Berk I., Schlemminger S., Vallbracht A., and Dotzauer A. Hepatitis A virus suppresses RIG-I-mediated IRF-3 activation to block induction of beta interferon. J Virol 79 17 (2005) 10968-10977
45. Chow E.K., Razani B., and Cheng G. Innate immune system regulation of nuclear hormone receptors in metabolic diseases. J Leukoc Biol 82 2 (2007) 187-195
46. Geissmann F., Revy P., Regnault A., Lepelletier Y., Dy M., Brousse N., et al. TGF-beta 1 prevents the noncognate maturation of human dendritic Langerhans cells. J Immunol 162 8 (1999) 4567-4575
47. Tridandapani S., Wardrop R., Baran C.P., Wang Y., Opalek J.M., Caligiuri M.A., et al. TGF-beta 1 suppresses [correction of supresses] myeloid Fc gamma receptor function by regulating the expression and function of the common gamma-subunit. J Immunol 170 9 (2003) 4572-4577
48. Nandan D., and Reiner N.E. TGF-beta attenuates the class II transactivator and reveals an accessory pathway of IFN-gamma action. J Immunol 158 3 (1997) 1095-1101
49. Bogdan C., Paik J., Vodovotz Y., and Nathan C. Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-beta and interleukin-10. J Biol Chem 267 32 (1992) 23301-23308
50. Aukrust P., Muller F., Ueland T., Svardal A.M., Berge R.K., and Froland S.S. Decreased vitamin A levels in common variable immunodeficiency: vitamin A supplementation in vivo enhances immunoglobulin production and downregulates inflammatory responses. Eur J Clin Invest 30 3 (2000) 252-259
51. McIntyre T.M., Kehry M.R., and Snapper C.M. Novel in vitro model for high-rate IgA class switching. J Immunol 154 7 (1995) 3156-3161
52. Borsutzky S., Cazac B.B., Roes J., and Guzman C.A. TGF-beta receptor signaling is critical for mucosal IgA responses. J Immunol 173 5 (2004) 3305-3309
53. Tokuyama H., and Tokuyama Y. Retinoids enhance IgA production by lipopolysaccharide-stimulated murine spleen cells. Cell Immunol 150 2 (1993) 353-363
54. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314 5802 (2006) 1157-1160
55. Mora J.R., Bono M.R., Manjunath N., Weninger W., Cavanagh L.L., Rosemblatt M., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424 6944 (2003) 88-93
56. Papadakis K.A., Landers C., Prehn J., Kouroumalis E.A., Moreno S.T., Gutierrez-Ramos J.C., et al. CC chemokine receptor 9 expression defines a subset of peripheral blood lymphocytes with mucosal T cell phenotype and Th1 or T-regulatory 1 cytokine profile. J Immunol 171 1 (2003) 159-165
57. Svensson M., Marsal J., Ericsson A., Carramolino L., Broden T., Marquez G., et al. CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J Clin Invest 110 8 (2002) 1113-1121
58. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., and Song S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21 4 (2004) 527-538
59. Denning T.L., Granger S.W., Mucida D., Graddy R., Leclercq G., Zhang W., et al. Mouse TCRalphabeta+CD8alphaalpha intraepithelial lymphocytes express genes that down-regulate their antigen reactivity and suppress immune responses. J Immunol 178 7 (2007) 4230-4239
60. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., and Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8 10 (2007) 1086-1094
61. Barnard J.A., Beauchamp R.D., Coffey R.J., and Moses H.L. Expression of TGF-β1 by intestinal epithelial cells. Proc Natl Acad Sci USA 86 (1989) 1578-1583
62. Dignass A.U., Stow J.L., and Babyatsky M.W. Acute epithelial injury in the rat small intestine in vivo is associated with expanded expression of transforming growth factor alpha and beta. Gut 38 5 (1996) 687-693
63. + regulatory T cells. Nat Immunol 9 6 (2008) 632-640
64. Cantorna M.T., Nashold F.E., and Hayes C.E. In vitamin A deficiency multiple mechanisms establish a regulatory T helper cell imbalance with excess Th1 and insufficient Th2 function. J Immunol 152 4 (1994) 1515-1522
65. Iwata M., Eshima Y., and Kagechika H. Retinoic acids exert direct effects on T cells to suppress Th1 development and enhance Th2 development via retinoic acid receptors. Int Immunol 15 8 (2003) 1017-1025
66. Elias K.M., Laurence A., Davidson T.S., Stephens G., Kanno Y., Shevach E.M., et al. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway. Blood 111 3 (2008) 1013-1020
67. Takaki H., Ichiyama K., Koga K., Chinen T., Takaesu G., Sugiyama Y., 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 283 22 (2008) 14955-14962
68. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17(+) T helper cells. Cell 126 6 (2006) 1121-1133
69. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448 7152 (2007) 484-487
70. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 29 1 (2007) 44-56
71. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 8 9 (2007) 967-974
72. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishiyama M., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 9 7 (2008) 769-776
73. Kattah M.G., Wong M.T., Yocum M.D., and Utz P.J. Cytokines secreted in response to Toll-like receptor ligand stimulation modulate differentiation of human Th17 cells. Arthritis Rheum 58 6 (2008) 1619-1629
74. Saurer L., McCullough K.C., and Summerfield A. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J Immunol 179 6 (2007) 3504-3514
75. Laurence A., Tato C.M., Davidson T.S., Kanno Y., Chen Z., Yao Z., et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26 3 (2007) 371-381
76. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 282 13 (2007) 9358-9363
77. Winoto A., and Littman D.R. Nuclear hormone receptors in T lymphocytes. Cell 109 Suppl (2002) S57-S66
78. Si J., and Collins S.J. IL-3-induced enhancement of retinoic acid receptor activity is mediated through Stat5, which physically associates with retinoic acid receptors in an IL-3-dependent manner. Blood 100 13 (2002) 4401-4409
79. Nakajima H., Brindle P.K., Handa M., and Ihle J.N. Functional interaction of STAT5 and nuclear receptor co-repressor SMRT: implications in negative regulation of STAT5-dependent transcription. EMBO J 20 23 (2001) 6836-6844
80. Zhou L., Lopes J.E., Chong M.M., Ivanov I.I., Min R., Victora G.D., et al. TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453 7192 (2008) 236-240
81. Ichiyama K., Yoshida H., Wakabayashi Y., Chinen T., Saeki K., Nakaya M., et al. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat. J Biol Chem 283 25 (2008) 17003-17008
82. Yang X.O., Nurieva R., Martinez G.J., Kang H.S., Chung Y., Pappu B.P., et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29 1 (2008) 44-56
83. Yarmus M., Woolf E., Bernstein Y., Fainaru O., Negreanu V., Levanon D., et al. Groucho/transducin-like enhancer-of-split (TLE)-dependent and -independent transcriptional regulation by Runx3. Proc Natl Acad Sci USA 103 19 (2006) 7384-7389