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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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X. Qin, B. T. Guo, B. Wan, L. Fang, L. Lu, L. Wu, Y. Q. Zang, and J. Z. Zhang (2010)
J. Immunol. 185, 1855-1863
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Cytokine Requirements for the Differentiation and Expansion of IL-17A- and IL-22-Producing Human V{gamma}2V{delta}2 T Cells.
K. J. Ness-Schwickerath, C. Jin, and C. T. Morita (2010)
J. Immunol. 184, 7268-7280
   Abstract »    Full Text »    PDF »
Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax.
S. K. Datta, M. Sabet, K. P. L. Nguyen, P. A. Valdez, J. M. Gonzalez-Navajas, S. Islam, I. Mihajlov, J. Fierer, P. A. Insel, N. J. Webster, et al. (2010)
PNAS 107, 10638-10643
   Abstract »    Full Text »    PDF »
Desiccating Stress Promotion of Th17 Differentiation by Ocular Surface Tissues through a Dendritic Cell-Mediated Pathway.
X. Zheng, C. S. de Paiva, D. Q. Li, W. J. Farley, and S. C. Pflugfelder (2010)
Invest. Ophthalmol. Vis. Sci. 51, 3083-3091
   Abstract »    Full Text »    PDF »
Cellular and molecular basis for the regulation of inflammation by TGF-{beta}.
A. Yoshimura, Y. Wakabayashi, and T. Mori (2010)
J. Biochem. 147, 781-792
   Abstract »    Full Text »    PDF »
In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction.
N. R. Blatner, A. Bonertz, P. Beckhove, E. C. Cheon, S. B. Krantz, M. Strouch, J. Weitz, M. Koch, A. L. Halverson, D. J. Bentrem, et al. (2010)
PNAS 107, 6430-6435
   Abstract »    Full Text »    PDF »
Pharmacologic Inhibition of MEK-ERK Signaling Enhances Th17 Differentiation.
A. H.-M. Tan and K.-P. Lam (2010)
J. Immunol. 184, 1849-1857
   Abstract »    Full Text »    PDF »
STAT3 Signaling in CD4+ T Cells Is Critical for the Pathogenesis of Chronic Sclerodermatous Graft-Versus-Host Disease in a Murine Model.
V. Radojcic, M. A. Pletneva, H.-R. Yen, S. Ivcevic, A. Panoskaltsis-Mortari, A. C. Gilliam, C. G. Drake, B. R. Blazar, and L. Luznik (2010)
J. Immunol. 184, 764-774
   Abstract »    Full Text »    PDF »
Tc17 CD8 T Cells: Functional Plasticity and Subset Diversity.
H.-R. Yen, T. J. Harris, S. Wada, J. F. Grosso, D. Getnet, M. V. Goldberg, K.-L. Liang, T. C. Bruno, K. J. Pyle, S.-L. Chan, et al. (2009)
J. Immunol. 183, 7161-7168
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Natural Occurring IL-17 Producing T Cells Regulate the Initial Phase of Neutrophil Mediated Airway Responses.
S. Tanaka, T. Yoshimoto, T. Naka, S. Nakae, Y.-i. Iwakura, D. Cua, and M. Kubo (2009)
J. Immunol. 183, 7523-7530
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Transforming growth factor {beta} is dispensable for the molecular orchestration of Th17 cell differentiation.
J. Das, G. Ren, L. Zhang, A. I. Roberts, X. Zhao, A. L.M. Bothwell, L. Van Kaer, Y. Shi, and G. Das (2009)
J. Exp. Med. 206, 2407-2416
   Abstract »    Full Text »    PDF »
Differential Effect of IL-27 on Developing versus Committed Th17 Cells.
M. El-behi, B. Ciric, S. Yu, G.-X. Zhang, D. C. Fitzgerald, and A. Rostami (2009)
J. Immunol. 183, 4957-4967
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Berberine Differentially Modulates the Activities of ERK, p38 MAPK, and JNK to Suppress Th17 and Th1 T Cell Differentiation in Type 1 Diabetic Mice.
G. Cui, X. Qin, Y. Zhang, Z. Gong, B. Ge, and Y. Q. Zang (2009)
J. Biol. Chem. 284, 28420-28429
   Abstract »    Full Text »    PDF »

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