Regulation of FoxP3+ regulatory T cells and Th17 cells by retinoids

Clinical and Developmental Immunology

Volumn 2008, Issue , 2008, Pages

  Kim, Chang H ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; RECEPTOR; RETINOID; RETINOL; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

BIOLOGICAL ACTIVITY; CELL LINE; EFFECTOR CELL; ENZYME REGULATION; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SYNTHESIS; ANIMAL; BIOSYNTHESIS; DRUG EFFECT; HELPER CELL; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-17; MICE; RETINOIDS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 42949091388     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2008/416910     Document Type: Review

References (155)

1. Murphy K. M., Ouyang W., Farrar J. D., Signaling and transcription in T helper development Annual Review of Immunology 2000 18 451 494
2. Szabo S. J.
3. Stockinger B.
4. Weaver C. T.
5. Harrington L. E., Mangan P. R., Weaver C. T.
6. Fontenot J. D.
7. Sakaguchi S.
8. Thompson C., Powrie F., Regulatory T cells Current Opinion in Pharmacology 2004 4 4 408 414
9. Ziegler S. F.
10. Shevach E. M., Piccirillo C. A., Thornton A. M., McHugh R. S., Control of T cell activation by CD 4 + CD 25 + suppressor T cells Generation and Effector Functions of Regulatory Lymphocytes 2003 252 New York, NY, USA John Wiley & Sons 24 44 Novartis Foundation Symposia
11. Kim C. H.
12. Wildin R. S., Ramsdell F., Peake J., X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy Nature Genetics 2001 27 1 18 20
13. Bennett C. L., Christie J., Ramsdell F., The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FoxP3 Nature Genetics 2001 27 1 20 21
14. Patel D. D., Escape from tolerance in the human X-linked autoimmunity-allergic disregulation syndrome and the Scurfy mouse Journal of Clinical Investigation 2001 107 2 155 157
15. Brunkow M. E., Jeffery E. W., Hjerrild K. A., Disruption of a new forkhead/winged-helix protein, Scurfin, results in the fatal lymphoproliferative disorder of the Scurfy mouse Nature Genetics 2001 27 1 68 73
16. Khattri R., Cox T., Yasayko S.-A., Ramsdell F.
17. Kim C. H.
18. Wei S., Kryczek I., Zou W.
19. Siewert C., Menning A., Dudda J., Induction of organ-selective CD 4 + regulatory T cell homing European Journal of Immunology 2007 37 4 978 989
20. Mucida D., Park Y., Kim G., Reciprocal Th17 and regulatory T cell differentiation mediated by retinoic acid Science 2007 317 5835 256 260
21. Benson M. J., Pino-Lagos K., Rosemblatt M., Noelle R. J.
22. Sun C.-M., Hall J. A., Blank R. B., Small intestine lamina propria dendritic cells promote de novo generation of FoxP3 T reg cells via retinoic acid Journal of Experimental Medicine 2007 204 8 1775 1785
23. Coombes J. L., Siddiqui K. R. R., Arancibia-Cárcamo C. V., A functionally specialized population of mucosal CD 103 + DCs induces FoxP 3 + regulatory T cells via a TGF- β and retinoic acid-dependent mechanism Journal of Experimental Medicine 2007 204 8 1757 1764
24. Kang S. G., Lim H. W., Andrisani O. M., Broxmeyer H. E., Kim C. H., Vitamin A metabolites induce gut-homing FoxP 3 + regulatory T cells Journal of Immunology 2007 179 6 3724 3733
25. Schambach F., Schupp M., Lazar M. A., Reiner S. L.
26. Elias K. M., Laurence A., Davidson T. S., Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway Blood 2008 111 3 1013 1020
27. Napoli J. L., Retinoic acid biosynthesis and metabolism The FASEB Journal 1996 10 9 993 1001
28. Stephensen C. B., Vitamin A, infection, and immune function Annual Review of Nutrition 2001 21 167 192
29. Mark M., Ghyselinck N. B., Chambon P.
30. Chambon P., A decade of molecular biology of retinoic acid receptors The FASEB Journal 1996 10 9 940 954
31. Altucci L., Leibowitz M. D., Ogilvie K. M., de Lera A. R., Gronemeyer H., RAR and RXR modulation in cancer and metabolic disease Nature Reviews Drug Discovery 2007 6 10 793 810
32. Napoli J. L., Biochemical pathways of retinoid transport, metabolism, and signal transduction Clinical Immunology and Immunopathology 1996 80 3 S52 S62
33. Iwata M.
34. Duester G.
35. Vicari A. P., Figueroa D. J., Hedrick J. A., TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development Immunity 1997 7 2 291 301
36. Hamann A., Andrew D. P., Jablonski-Westrich D., Holzmann B., Butcher E. C., Role of α 4-integrins in lymphocyte homing to mucosal tissues in vivo Journal of Immunology 1994 152 7 3282 3293
37. Berlin C., Berg E. L., Briskin M. J., α 4 β 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1 Cell 1993 74 1 185 195
38. Collins M. D.
39. McCullough F. S., Northrop-Clewes C. A., Thurnham D. I., The effect of vitamin A on epithelial integrity Proceedings of the Nutrition Society 1999 58 2 289 293
40. Soprano D. R., Qin P., Soprano K. J., Retinoic acid receptors and cancers Annual Review of Nutrition 2004 24 201 221
41. Okuno M., Kojima S., Matsushima-Nishiwaki R., Retinoids in cancer chemoprevention Current Cancer Drug Targets 2004 4 3 285 298
42. Szondy Z.
43. Bourguet W.
44. Clarke N.
45. Shibata H., Spencer T. E., Oñate S. A., Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action Recent Progress in Hormone Research 1997 52 141 164
46. Cantorna M. T., Nashold F. E., Hayes C. E., In vitamin A deficiency multiple mechanisms establish a regulatory T helper cell imbalance with excess Th1 and insufficient Th2 function Journal of Immunology 1994 152 4 1515 1522
47. Racke M. K., Burnett D., Pak S.-H., Retinoid treatment of experimental allergic encephalomyelitis: IL-4 production correlates with improved disease course Journal of Immunology 1995 154 1 450 458
48. Hoag K. A.
49. Stephensen C. B., Rasooly R., Jiang X., Vitamin A enhances in vitro Th2 development via retinoid X receptor pathway Journal of Immunology 2002 168 9 4495 4503
50. Iwata M.
51. Tokuyama Y., Tokuyama H., Retinoids as Ig isotype-switch modulators the role of retinoids in directing isotype switching to IgA and IgG1 (IgE) in association with IL-4 and IL-5 Cellular Immunology 1996 170 2 230 234
52. Du X., Tabeta K., Mann N., Crozat K., Mudd S., Beutler B.
53. Mora J. R., Bono M. R., Manjunath N., Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells Nature 2003 424 6944 88 93
54. Stenstad H., Ericsson A., Johansson-Lindbom B., Gut-associated lymphoid tissue-primed CD 4 + T cells display CCR9-dependent and -independent homing to the small intestine Blood 2006 107 9 3447 3454
55. Mora J. R.
56. Pasatiempo A. M. G., Kinoshita M., Taylor C. E., Ross A. C., Antibody production in vitamin A-depleted rats is impaired after immunization with bacterial polysaccharide or protein antigens The FASEB Journal 1990 4 8 2518 2527
57. Smith S. M., Hayes C. E., Contrasting impairments in IgM and IgG responses of vitamin A-deficient mice Proceedings of the National Academy of Sciences of the United States of America 1987 84 16 5878 5882
58. Sirisinha S., Darip M. D., Moongkarndi P., Impaired local immune response in vitamin A-deficient rats Clinical and Experimental Immunology 1980 40 1 127 135
59. Yang Y., Vacchio M. S., Ashwell J. D., 9-cis-retinoic acid inhibits activation-driven T-cell apoptosis: implications for retinoid X receptor involvement in thymocyte development Proceedings of the National Academy of Sciences of the United States of America 1993 90 13 6170 6174
60. Iwata M., Mukai M., Nakai Y., Iseki R., Retinoic acids inhibit activation-induced apoptosis in T cell hybridomas and thymocytes Journal of Immunology 1992 149 10 3302 3308
61. Wiedermann A., Tarkowski U., Bremell T., Hanson L. Å., Kahu H., Dahlgren U. I., Vitamin A deficiency predisposes to Staphylococcus aureus infection Infection and Immunity 1996 64 1 209 214
62. Aukrust P.
63. Vladutiu A., Cringulescu N., Suppression of experimental allergic encephalomyelitis by vitamin A Experientia 1968 24 7 718 719
64. Massacesi L., Abbamondi A. L., Giorgi C., Sarlo F., Lolli F., Amaducci L., Suppression of experimental allergic encephalomyelitis by retinoic acid Journal of the Neurological Sciences 1987 80 1 55 64
65. Wang T., Niwa S., Bouda K., The effect of Am-80, one of retinoids derivatives on experimental allergic encephalomyelitis in rats Life Sciences 2000 67 15 1869 1879
66. Massacesi L., Castigli E., Vergelli M., Immunosuppressive activity of 13-cis-retinoic acid and prevention of experimental autoimmune encephalomyelitis in rats Journal of Clinical Investigation 1991 88 4 1331 1337
67. Sijtsma S. R., Rombout J. H. W. M., West C. E., van der Zijpp A. J., Vitamin A deficiency impairs cytotoxic T lymphocyte activity in Newcastle disease virus-infected chickens Veterinary Immunology and Immunopathology 1990 26 2 191 201
68. Smith S. M., Levy N. S., Hayes C. E., Impaired immunity in vitamin A-deficient mice Journal of Nutrition 1987 117 5 857 865
69. Wiedermann U., Chen X.-J., Enerbäck L., Hanson L. Å., Kahu H., Dahlgren U. I., Vitamin A deficiency increases inflammatory responses Scandinavian Journal of Immunology 1996 44 6 578 584
70. Carman J. A., Hayes C. E., Abnormal regulation of IFN- γ secretion in vitamin A deficiency Journal of Immunology 1991 147 4 1247 1252
71. Cantorna M. T., Nashold F. E., Hayes C. E., Vitamin A deficiency results in a priming environment conducive for Th1 cell development European Journal of Immunology 1995 25 6 1673 1679
72. Fontham E. T. H., Protective dietary factors and lung cancer International Journal of Epidemiology 1990 19, supplement 1 S32 S42
73. Albanes D., Heinonen O. P., Taylor P. R., α -tocopherol and β -carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: effects of base-line characteristics and study compliance Journal of the National Cancer Institute 1996 88 21 1560 1570
74. Kuenzli S., Saurat J.-H., Retinoids for the treatment of psoriasis: outlook for the future Current Opinion in Investigational Drugs 2001 2 5 625 630
75. Millikan L. E.
76. Fenaux P.
77. Krown S. E.
78. de Thé H., Lavau C., Marchio A., Chomienne C., Degos L., Dejean A., The PML-RAR α fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR Cell 1991 66 4 675 684
79. Kakizuka A., Miller W. H. Jr., Umesono K., Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RAR α with a novel putative transcription factor, PML Cell 1991 66 4 663 674
80. Breitman T. R., Selonick S. E., Collins S. J., Induction of differentiation of the human promyelocytic leukemia cell line (HL-60) by retinoic acid Proceedings of the National Academy of Sciences of the United States of America 1980 77 5 2936 2940
81. Breitman T. R., Collins S. J., Keene B. R., Terminal differentiation of human promyelocytic leukemic cells in primary culture in response to retinoic acid Blood 1981 57 6 1000 1004
82. Mucida D., Kutchukhidze N., Erazo A., Russo M., Lafaille J. J.
83. Sun J.-B.
84. Chen W.
85. Zheng S. G., Wang J. H., Gray J. D., Soucier H., Horwitz D. A.
86. Setoguchi R., Hori S., Takahashi T., Sakaguchi S.
87. Fontenot J. D., Rasmussen J. P., Gavin M. A., Rudensky A. Y., A function for interleukin 2 in FoxP3-expressing regulatory T cells Nature Immunology 2005 6 1142 1151
88. Knoechel B., Lohr J., Kahn E., Bluestone J. A., Abbas A. K., Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen Journal of Experimental Medicine 2005 202 10 1375 1386
89. Furtado G. C., Curotto de Lafaille M. A., Kutchukhidze N., Lafaille J. J., Interleukin 2 signaling is required for CD 4 + regulatory T cell function Journal of Experimental Medicine 2002 196 6 851 857
90. Verhasselt V., Vosters O., Beuneu C., Nicaise C., Stordeur P., Goldman M., Induction of FoxP3-expressing regulatory CD 4 pos T cells by human mature autologous dendritic cells European Journal of Immunology 2004 34 3 762 772
91. Moseman E. A., Liang X., Dawson A. J., Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD 4 + CD 25 + regulatory T cells Journal of Immunology 2004 173 7 4433 4442
92. Verginis P., Li H. S., Carayanniotis G., Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin-specific CD 4 + CD 25 + T cells Journal of Immunology 2005 174 11 7433 7439
93. Ghiringhelli F., Puig P. E., Roux S., Tumor cells convert immature myeloid dendritic cells into TGF- β -secreting cells inducing CD 4 + CD 25 + regulatory T cell proliferation Journal of Experimental Medicine 2005 202 7 919 929
94. Belkaid Y., Piccirillo C. A., Mendez S., Shevach E. M., Sacks D. L., CD 4 + CD 25 + regulatory T cells control Leishmania major persistence and immunity Nature 2002 420 6915 502 507
95. Kullberg M. C., Jankovic D., Gorelick P. L., Bacteria-triggered CD 4 + T regulatory cells suppress Helicobacter hepaticus -induced colitis Journal of Experimental Medicine 2002 196 4 505 515
96. Caramalho I., Lopes-Carvalho T., Ostler D., Zelenay S., Haury M., Demengeot J., Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide Journal of Experimental Medicine 2003 197 4 403 411
97. Pasare C., Medzhitov R., Toll pathway-dependent blockade of CD 4 + CD 25 + T cell-mediated suppression by dendritic cells Science 2003 299 5609 1033 1036
98. Fehérvári Z., Sakaguchi S., Control of FoxP 3 + CD 25 + CD 4 + regulatory cell activation and function by dendritic cells International Immunology 2004 16 12 1769 1780
99. Lyons R. M., Keski-Oja J., Moses H. L., Proteolytic activation of latent transforming growth factor- β from fibroblast-conditioned medium Journal of Cell Biology 1988 106 5 1659 1665
100. Penttinen C., Saharinen J., Weikkolainen K., Hyytiainen M., Keski-Oja J., Secretion of human latent TGF- β -binding protein-3 (LTBP-3) is dependent on co-expression of TGF- β Journal of Cell Science 2002 115 17 3457 3468
101. Annes J. P., Munger J. S., Rifkin D. B., Making sense of latent TGF- β activation Journal of Cell Science 2003 116 2 217 224
102. Denning T. L., Wang Y.-C., Patel S. R., Williams I. R., Pulendran B., Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses Nature Immunology 2007 8 10 1086 1094
103. Walker M. R., Kasprowicz D. J., Gersuk V. H., Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD 4 + CD 25-T cells Journal Clinical Investigation 2003 112 9 1437 1443
104. Mantel P.-Y., Ouaked N., Rückert B., Molecular mechanisms underlying FoxP3 induction in human T cells Journal of Immunology 2006 176 6 3593 3602
105. Wang J., Ioan-Facsinay A., van der Voort E. I. H., Huizinga T. W. J., Toes R. E. M.
106. Allan S. E., Passarini L., Bacchetta R., The role of 2 FoxP3 isoforms in the generation of human CD4 + Tregs Journal of Clinical Investigation 2005 115 11 3276 3284
107. Fontenot J. D., Gavin M. A., Rudensky A. Y.
108. Hori S., Nomura T., Sakaguchi S.
109. Kehrl J. H., Wakefield L. M., Roberts A. B., Production of transforming growth factor β by human T lymphocytes and its potential role in the regulation of T cell growth Journal of Experimental Medicine 1986 163 5 1037 1050
110. McGrane M. M.
111. Kang S. G., Piniecki R. J., Hogenesch H., Identification of a chemokine network that recruits FoxP 3 + regulatory T cells into chronically inflamed intestine Gastroenterology 2007 132 3 966 981
112. Lin J.-X., Leonard W. J., The role of Stat5a and Stat5b in signaling by IL-2 family cytokines Oncogene 2000 19 21 2566 2576
113. Yao Z., Kanno Y., Kerenyi M., Nonredundant roles for Stat5a/b in directly regulating FoxP3 Blood 2007 109 10 4368 4375
114. Dong S., Tweardy D. J., Interactions of STAT5b-RAR α, a novel acute promyelocytic leukemia fusion protein, with retinoic acid receptor and STAT3 signaling pathways Blood 2002 99 8 2637 2646
115. von Boehmer H.
116. Gondek D. C., Lu L.-F., Quezada S. A., Sakaguchi S., Noelle R. J.
117. Grossman W. J., Verbsky J. W., Barchet W., Colonna M., Atkinson J. P., Ley T. J.
118. Pearson C. I., McDevitt H. O., Redirecting Th1 and Th2 responses in autoimmune disease Current Topics in Microbiology and Immunology 1999 238 79 122
119. Willenborg D. O.
120. Ferber I. A., Brocke S., Taylor-Edwards C., Mice with a disrupted IFN- γ gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE) Journal of Immunology 1996 156 1 5 7
121. Vermeire K., Heremans H., Vandeputte M., Huang S., Billiau A., Matthys P.
122. Sonderegger I., Röhn T. A., Kurrer M. O., Neutralization of IL-17 by active vaccination inhibits of IL-23-dependent autoimmune myocarditis European Journal of Immunology 2006 36 11 2849 2856
123. Komiyama Y., Nakae S., Matsuki T., IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis Journal of Immunology 2006 177 1 566 573
124. Chen Y., Langrish C. L., McKenzie B., Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis Journal of Clinical Investigation 2006 116 5 1317 1326
125. Belladonna M. L.
126. Hofstetter H. H., Ibrahim S. M., Koczan D., Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis Cellular Immunology 2005 237 2 123 130
127. Hirota K., Hashimoto M., Yoshitomi H., T cell self-reactivity forms a cytokine milieu for spontaneous development of IL- 17 + Th cells that cause autoimmune arthritis Journal of Experimental Medicine 2007 204 1 41 47
128. Aggarwal S., Ghilardi N., Xie M.-H., de Sauvage F. J., Gurney A. L.
129. Wei L.
130. Liang S. C., Tan X.-Y., Luxenberg D. P., Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides Journal of Experimental Medicine 2006 203 10 2271 2279
131. Fossiez F., Djossou O., Chomarat P., T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines Journal of Experimental Medicine 1996 183 6 2593 2603
132. Kawaguchi M., Kokubu F., Odaka M., Induction of granulocyte-macrophage colony-stimulating factor by a new cytokine, ML-1 (IL-17F), via Raf I-MEK-ERK pathway Journal of Allergy and Clinical Immunology 2004 114 2 444 450
133. Henness S., Johnson C. K., Ge Q., Armour C. L., Hughes J. M., Ammit A. J.
134. Korn T., Bettelli E., Gao W., IL-21 initiates an alternative pathway to induce proinflammatory Th17 cells Nature 2007 448 7152 484 487
135. Nurieva R.
136. Wolk K., Witte E., Wallace E., IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes: a potential role in psoriasis European Journal of Immunology 2006 36 5 1309 1323
137. Nagalakshmi M. L., Rascle A., Zurawski S., Menon S., de Waal Malefyt R.
138. Radaeva S., Sun R., Pan H.-N., Hong F., Gao B.
139. Wolk K., Witte E., Hoffmann U., IL-22 induces lipopolysaccharide-binding protein in hepatocytes: a potential systemic role of IL-22 in Crohn's disease Journal of Immunology 2007 178 9 5973 5981
140. Veldhoen M., Hocking R. J., Atkins C. J., Locksley R. M., Stockinger B.
141. Bettelli E., Carrier Y., Gao W., Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells Nature 2006 441 7090 235 238
142. Acosta-Rodriguez E. V., Napolitani G., Lanzavecchia A., Sallusto F., Interleukins 1 β and 6 but not transforming growth factor- β are essential for the differentiation of interleukin 17-producing human T helper cells Nature Immunology 2007 8 9 942 949
143. Kimura A., Naka T., Kishimoto T.
144. Zhou L., Ivanov I. I., Spolski R., IL-6 programs Th17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways Nature Immunology 2007 8 9 967 974
145. Nishihara M., Ogura H., Ueda N., IL-6-gp130-STAT3 in T cells directs the development of IL-1 + T h 7 with a minimum effect on that of Treg in the steady state International Immunology 2007 19 6 695 702
146. Mathur A. N., Chang H.-C., Zisoulis D. G., Stat3 and Stat4 direct development of IL-17-secreting Th cells Journal of Immunology 2007 178 8 4901 4907
147. Ivanov I. I., McKenzie B. S., Zhou L., The orphan nuclear receptor ROR γ t directs the differentiation program of proinflammatory IL- 17 + T helper cells Cell 2006 126 6 1121 1133
148. Yang X. O., Pappu B. P., Nurieva R., T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR α and ROR γ Immunity 2008 28 1 29 39
149. Eberl G.
150. Kurebayashi S., Ueda E., Sakaue M., Retinoid-related orphan receptor γ (ROR γ) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis Proceedings of the National Academy of Sciences of the United States of America 2000 97 18 10132 10137
151. Sun Z., Unutmaz D., Zou Y.-R., Requirement for ROR γ in thymocyte survival and lymphoid organ development Science 2000 288 5475 2369 2373
152. Batten M., Li J., Yi S., Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells Nature Immunology 2006 7 9 929 936
153. Stumhofer J. S., Laurence A., Wilson E. H., Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system Nature Immunology 2006 7 9 937 945
154. Laurence A., Tato C. M.
155. Amadi-Obi A., Yu C.-R., Liu X., Th17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1 Nature Medicine 2007 13 6 711 718