The Neuron-Restrictive Silencer Element-Neuron-Restrictive Silencer Factor System Regulates Basal and Endothelin 1-Inducible Atrial Natriuretic Peptide Gene Expression in Ventricular Myocytes

doi:10.1128/MCB.21.6.2085-2097.2001

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Molecular and Cellular Biology, March 2001, p. 2085-2097, Vol. 21, No. 6
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.6.2085-2097.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

The Neuron-Restrictive Silencer Element-Neuron-Restrictive Silencer Factor System Regulates Basal and Endothelin 1-Inducible Atrial Natriuretic Peptide Gene Expression in Ventricular Myocytes

Koichiro Kuwahara,¹ Yoshihiko Saito,¹^,^* Emiko Ogawa,¹ Nobuki Takahashi,¹ Yasuaki Nakagawa,¹ Yoshihisa Naruse,² Masaki Harada,¹ Ichiro Hamanaka,¹ Takehiko Izumi,¹ Yoshihiro Miyamoto,¹ Ichiro Kishimoto,¹ Rika Kawakami,¹ Michio Nakanishi,¹ Nozomu Mori,²^,³ and Kazuwa Nakao¹

Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, Kyoto 606-8397,¹ Department of Molecular Genetic Research, National Institute for Longevity Sciences, Oobu, Aichi 474-8522,² and CREST, Science and Technology Corporation of Japan (JST), Kawaguchi, Saitama 332-0012,³ Japan

Received 19 October 2000/Accepted 19 December 2000

Induction of the atrial natriuretic peptide (ANP) gene is a common feature of ventricular hypertrophy. A number of cis-actingenhancer elements for several transcriptional activators havebeen shown to play central roles in the regulation of ANP geneexpression, but much less is known about contributions made bytranscriptional repressors. The neuron-restrictive silencer element(NRSE), also known as repressor element 1, mediates repressionof neuronal gene expression in nonneuronal cells. We found thatNRSE, which is located in the 3' untranslated region of the ANPgene, mediated repression of ANP promoter activity in ventricularmyocytes and was also involved in the endothelin 1-induced increasein ANP gene transcription. The repression was conferred by a repressorprotein, neuron-restrictive silencer factor (NRSF). NRSF associatedwith the transcriptional corepressor mSin3 and formed a complexwith histone deacetylase (HDAC) in ventricular myocytes. TrichostatinA (TSA), a specific HDAC inhibitor, relieved NRSE-mediated repressionof ANP promoter activity, and chromatin immunoprecipitation assaysrevealed the involvement of histone deacetylation in NRSE-mediatedrepression of ANP gene expression. Furthermore, in myocytes infectedwith recombinant adenovirus expressing a dominant-negative formof NRSF, the basal level of endogenous ANP gene expression wasincreased and a TSA-induced increase in ANP gene expression wasapparently attenuated, compared with those in myocytes infectedwith control adenovirus. Our findings show that an NRSE-NRSF systemplays a key role in the regulation of ANP gene expression by HDACin ventricular myocytes and provide a new insight into the roleof the NRSE-NRSF system outside the nervoussystem.

^* Corresponding author. Mailing address: Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine,54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto 606, Japan. Phone: 81-75-751-4287.Fax: 81-75-771-9452. E-mail: yssaito{at}kuhp.kyoto-u.ac.jp.

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