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J. Biol. Chem. 282 (13): 9358-9363

© 2007 by The American Society for Biochemistry and Molecular Biology, Inc.

STAT3 Regulates Cytokine-mediated Generation of Inflammatory Helper T Cells*

Xuexian O. Yang{ddagger}, Athanasia D. Panopoulos{ddagger}1, Roza Nurieva{ddagger}23, Seon Hee Chang{ddagger}3, Demin Wang§, Stephanie S. Watowich{ddagger}, , and Chen Dong{ddagger}4

{ddagger}Department of Immunology, M.D. Anderson Cancer Center, Houston, Texas 77030 and the §Blood Research Institute, Blood Center of Wisconsin, Milwaukee, Wisconsin 53226

Abstract: Interleukin-17 (IL-17)-producing helper T (TH) cells, named as THIL-17, TH17, or inflammatory TH (THi), have been recently identified as a novel effector lineage. However, how cytokine signals mediate THi differentiation is unclear. We found that IL-6 functioned to up-regulate IL-23R and that IL-23 synergized with IL-6 in promoting THi generation. STAT3, activated by both IL-6 and IL-23, plays a critical role in THi development. A hyperactive form of STAT3 promoted THi development, whereas this differentiation process was greatly impaired in STAT3-deficient T cells. Moreover, STAT3 regulated the expression of retinoic acid receptor-related orphan receptor {gamma}-T (ROR{gamma}t), a THi-specific transcriptional regulator; STAT3 deficiency impaired ROR{gamma}t expression and led to elevated expression of T-box expressed in T cells (T-bet) and Forkhead box P3 (Foxp3). Our data thus demonstrate a pathway whereby cytokines regulate THi differentiation through a selective STAT transcription factor that functions to regulate lineage-specific gene expression.

Received for publication December 28, 2006. Revision received January 16, 2007.

* This work was supported by research grants from the National Institutes of Health (to C. D. and D. W.), American Cancer Society (to D. W.), and M. D. Anderson Cancer Center (to S. S. W.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1 Supported by an National Institutes of Health training grant and an American Legion Auxiliary Award.

2 Recipient of a scientist development grant from the American Heart Association.

3 Recipients of postdoctoral fellowships from the Arthritis Foundation.

4 A Cancer Research Institute Investigator and an M. D. Anderson Cancer Center Trust Fellow. To whom correspondence should be addressed. Fax: 713-563-0604; E-mail: cdong{at}mdanderson.org.

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Regulation of Th17 cell differentiation and EAE induction by MAP3K NIK.
W. Jin, X.-F. Zhou, J. Yu, X. Cheng, and S.-C. Sun (2009)
Blood 113, 6603-6610
   Abstract »    Full Text »    PDF »
The T Cell STAT Signaling Network Is Reprogrammed within Hours of Bacteremia via Secondary Signals.
A. N. Hotson, J. W. Hardy, M. B. Hale, C. H. Contag, and G. P. Nolan (2009)
J. Immunol. 182, 7558-7568
   Abstract »    Full Text »    PDF »
Halofuginone Inhibits TH17 Cell Differentiation by Activating the Amino Acid Starvation Response.
M. S. Sundrud, S. B. Koralov, M. Feuerer, D. P. Calado, A. E. Kozhaya, A. Rhule-Smith, R. E. Lefebvre, D. Unutmaz, R. Mazitschek, H. Waldner, et al. (2009)
Science 324, 1334-1338
   Abstract »    Full Text »    PDF »
Decreased Levels of Both Stat1 and Stat3 in T Lymphocytes from Mice Bearing Mammary Tumors.
M. E. HANDEL-FERNANDEZ, D. ILKOVITCH, V. IRAGAVARAPU-CHARYULU, L. M. HERBERT, and D. M. LOPEZ (2009)
Anticancer Res 29, 2051-2058
   Abstract »    Full Text »    PDF »
Calcitriol Suppresses Antiretinal Autoimmunity through Inhibitory Effects on the Th17 Effector Response.
J. Tang, R. Zhou, D. Luger, W. Zhu, P. B. Silver, R. S. Grajewski, S.-B. Su, C.-C. Chan, L. Adorini, and R. R. Caspi (2009)
J. Immunol. 182, 4624-4632
   Abstract »    Full Text »    PDF »
Cutting Edge: In Vitro Generated Th17 Cells Maintain Their Cytokine Expression Program in Normal but Not Lymphopenic Hosts.
R. Nurieva, X. O. Yang, Y. Chung, and C. Dong (2009)
J. Immunol. 182, 2565-2568
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Defects in Jak-STAT-mediated cytokine signals cause hyper-IgE syndrome: lessons from a primary immunodeficiency.
Y. Minegishi and H. Karasuyama (2009)
Int. Immunol. 21, 105-112
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The induction of antibody production by IL-6 is indirectly mediated by IL-21 produced by CD4+ T cells.
O. Dienz, S. M. Eaton, J. P. Bond, W. Neveu, D. Moquin, R. Noubade, E. M. Briso, C. Charland, W. J. Leonard, G. Ciliberto, et al. (2009)
J. Exp. Med. 206, 69-78
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Insights into the Role of STAT3 in Human Lymphocyte Differentiation as Revealed by the Hyper-IgE Syndrome.
S. G. Tangye, M. C. Cook, and D. A. Fulcher (2009)
J. Immunol. 182, 21-28
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CCR6 Regulates the Migration of Inflammatory and Regulatory T Cells.
T. Yamazaki, X. O. Yang, Y. Chung, A. Fukunaga, R. Nurieva, B. Pappu, N. Martin-Orozco, H. S. Kang, L. Ma, A. D. Panopoulos, et al. (2008)
J. Immunol. 181, 8391-8401
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IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+ regulatory T cells.
T. Korn, M. Mitsdoerffer, A. L. Croxford, A. Awasthi, V. A. Dardalhon, G. Galileos, P. Vollmar, G. L. Stritesky, M. H. Kaplan, A. Waisman, et al. (2008)
PNAS 105, 18460-18465
   Abstract »    Full Text »    PDF »
Modulation of Acute Diarrheal Illness by Persistent Bacterial Infection.
M. E. McBee, P. Z. Zheng, A. B. Rogers, J. G. Fox, and D. B. Schauer (2008)
Infect. Immun. 76, 4851-4858
   Abstract »    Full Text »    PDF »
The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation.
F. Annunziato, L. Cosmi, F. Liotta, E. Maggi, and S. Romagnani (2008)
Int. Immunol. 20, 1361-1368
   Abstract »    Full Text »    PDF »

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