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J. Biol. Chem., Vol. 279, Issue 22, 23123-23133, May 28, 2004

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CD28 Costimulation Controls Histone Hyperacetylation of the Interleukin 5 Gene Locus in Developing Th2 Cells^*

Masamichi Inami, Masakatsu Yamashita, Yoshiyuki Tenda, Akihiro Hasegawa, Motoko Kimura, Kahoko Hashimoto, Nobuo Seki¶, Masaru Taniguchi||, and Toshinori Nakayama**

From the Department of Immunology, Graduate School of Medicine, Chiba University, 1-8-1 Inohana Chuo-ku, Chiba 260-8670, Department of Life and Environmental Sciences and High Technology Research Center, Chiba Institute of Technology, Narashino, Tsudanuma, Chiba 275-0016, ^¶Exploratory Research Laboratories, Department of Bioscience, Fujisawa Pharmaceutical Co. Ltd., 5-2-3, Tokodai, Tsukuba, Ibaraki 300-2698, and ^||Laboratory for Immune Regulation, RIKEN Research Center for Allergy and Immunology, Yokohama 230-0045, Japan

Interleukin 5 (IL-5) plays a unique role in allergic inflammatory responses, and the understanding of molecular mechanisms underlying the generation of IL-5-producing cells is crucial for the regulation of allergic disorders. Differentiation of naive CD4 T cells into type-2 helper (Th2) cells is accompanied by chromatin remodeling including hyperacetylation of histones H3 and H4 in the nucleosomes associated with the IL-4, IL-13, and IL-5 genes. Histone hyperacetylation of the IL-5 gene displayed a delayed kinetics compared with that of the IL-4 and IL-13 genes, suggesting a distinct remodeling mechanism for the IL-5-gene locus. Here we studied the role of CD28 costimulation in the generation of IL-5-producing cells and the histone hyperacetylation of the IL-5 gene locus. CD28-costimulation selectively enhanced histone hyperacetylation of the IL-5 gene locus that appeared to be mediated through NF-B activation and subsequent up-regulation of GATA3. The CD28 costimulation-sensitive histone hyperacetylation spanned almost the entire intergenic region between the IL-5 and RAD50 accompanied with intergenic transcript. Thus, this is the first demonstration that CD28 costimulation controls a chromatin-remodeling process during Th2 cell differentiation.

Received for publication, February 4, 2004 , and in revised form, March 22, 2004.

^* This work was supported by grants from the Ministry of Education, Culture, Sports, Science, and Technology of (Japan) (Grants-in-aid for Scientific Research, Priority Areas Research 13218016 and 12051203 and Scientific Research B 14370107, Advanced and Innovational Research Program in Life Science, and Special Coordination Funds), the Ministry of Health, Labor, and Welfare (Japan) (a grant-in-aid for research on Advanced Medical Technology), the Program for Promotion of Fundamental Studies in Health Science of the Organization for Pharmaceutical Safety and Research (Japan), Human Frontier Science Program Research Grant RG00168/2000-M206, the Hamaguchi Foundation, and the Uehara Memorial Foundation. 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.

^** To whom correspondence should be addressed: Dept. of Immunology, Graduate School of Medicine, Chiba University, 1-8-1 Inohana Chuo-ku, Chiba 260-8670, Japan. Tel.: 81-43-226-2200; Fax: 81-43-227-1498; E-mail: tnakayama{at}faculty.chiba-u.jp.

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