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J. Biol. Chem., Vol. 279, Issue 17, 18091-18097, April 23, 2004

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In Vivo Chromatin Remodeling Events Leading to Inflammatory Gene Transcription under Diabetic Conditions^*

Feng Miao, Irene Gaw Gonzalo, Linda Lanting, and Rama Natarajan

From the Gonda Diabetes Center, Beckman Research Institute of City of Hope, Duarte, California 91010

The transcription factor NF-B (NF-B) plays a pivotal role in regulating inflammatory gene expression. Its effects are optimized by various coactivators including histone acetyltransferases (HATs) such as CBP/p300 and p/CAF. Evidence shows that high glucose (HG) conditions mimicking diabetes can activate the transcription of NF-B-regulated inflammatory genes. However, the underlying in vivo transcription and nuclear chromatin remodeling events are unknown. We therefore carried out chromatin immunoprecipitation (ChIP) assays in monocytes to identify 1) chromatin factors bound to the promoters of tumor necrosis factor- (TNF-) and related NF-B-regulated genes under HG or diabetic conditions, 2) specific lysine (Lys (K)) residues on histone H3 (HH3) and HH4 acetylated in this process. HG treatment of THP-1 monocytes increased the transcriptional activity of NF-B p65, which was augmented by CBP/p300 and p/CAF. ChIP assays showed that HG increased the recruitment of NF-B p65, CPB, and p/CAF to the TNF- and COX-2 promoters. Interestingly, ChIP assays also demonstrated concomitant acetylation of HH3 at Lys⁹ and Lys¹⁴, and HH4 at Lys⁵, Lys⁸, and Lys¹² at the TNF- and COX-2 promoters. Overexpression of histone deacetylase (HDAC) isoforms inhibited p65-mediated TNF- transcription. In contrast, a HDAC inhibitor stimulated gene transcription and histone acetylation. Finally, we demonstrated increased HH3 acetylation at TNF- and COX-2 promoters in human blood monocytes from type 1 and type 2 diabetic subjects relative to nondiabetic. These results show for the first time that diabetic conditions can increase in vivo recruitment of NF-B and HATs, as well as histone acetylation at the promoters of inflammatory genes, leading to chromatin remodeling and transcription.

Received for publication, October 27, 2003 , and in revised form, February 4, 2004.

^* This work was supported by National Institutes of Health Grants RO1 DK065073 and PO1 HL55798, by Juvenile Diabetes Foundation International, and in part by General Clinical Research Center Grant MO1RR00043 (awarded to City of Hope) from the National Center for Research Resources. 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: Gonda Diabetes Center, Beckman Research Inst. of the City of Hope, 1500 East Duarte Rd., Duarte, CA 91010. Tel.: 626-359-8111 (ext. 62289); Fax: 626-301-8136; E-mail: rnatarajan{at}coh.org.

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