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J. Biol. Chem., Vol. 279, Issue 41, 42850-42859, October 8, 2004

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Regulation of Swi6/HP1-dependent Heterochromatin Assembly by Cooperation of Components of the Mitogen-activated Protein Kinase Pathway and a Histone Deacetylase Clr6^*

Hyun Soo Kim, Eun Shik Choi, Jin A Shin, Yeun Kyu Jang, and Sang Dai Park¶||

From the Research Institute, National Cancer Center, Goyang, Gyeonggi 411-769 and ^¶School of Biological Sciences, Seoul National University, Seoul 151-742, Republic of Korea

A study of gene silencing within the mating-type region of fission yeast defines two distinct pathways responsible for the establishment of heterochromatin assembly. One is RNA interference-dependent and acts on centromere-homologous repeats (cenH). The other is a stochastic Swi6 (the fission yeast HP1 homolog)-dependent mechanism that is not fully understood. Here we find that activating transcription factor (Atf1) and Pcr1, the fission yeast bZIP transcription factors homologous to human ATF-2, are crucial for proper histone deacetylation of both H3 and H4. This deacetylation is a prerequisite for subsequent H3 lysine 9 methylation and Swi6-dependent heterochromatin assembly across the rest of the silent mating-type (mat) region lacking the RNA interference-dependent cenH repeat. Moreover, Atf1 and Pcr1 can form complexes with both a histone deacetylase, Clr6, and Swi6, and clr6 mutations affected the H3/H4 acetylation patterns, similar to the atf1 and pcr1 deletion mutant phenotypes at the endogenous mat loci and at the ctt1⁺ promoter region surrounding ATF/CRE-binding site. These data suggest that Atf1 and Pcr1 participate in an early step essential for heterochromatin assembly at the mat locus and silencing of transcriptional targets of Atf1. Furthermore, a phosphorylation event catalyzed by the conserved mitogen-activated protein kinase pathway is important for regulation of heterochromatin silencing by Atf1 and Pcr1. These findings suggest a role for the mitogen-activated protein kinase pathway and histone deacetylase in Swi6-based heterochromatin assembly.

Received for publication, June 29, 2004 , and in revised form, August 2, 2004.

^* This work was supported in part by National Cancer Center Research Grant 0210110 (to Y. K. J.). 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.

^|| Supported by Research Fellowship BK21 from the Korean Ministry of Education.

To whom correspondence should be addressed: National Cancer Center, 809 Madu-dong, Ilsan-gu, Goyang, Gyeonggi 411-769, Republic of Korea. Tel.: 82-31-920-2001; Fax: 82-31-920-2009; E-mail: ykjang{at}ncc.re.kr.

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