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J. Biol. Chem., Vol. 283, Issue 23, 15884-15892, June 6, 2008

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Histone Acetylation and Methylation at Sites Initiating Divergent Polycistronic Transcription in Trypanosoma cruzi^*

Patricia Respuela¹, Marcela Ferella, Alvaro Rada-Iglesias², and Lena Åslund³

From the Department of Genetics and Pathology, Rudbeck Laboratory, Uppsala University, SE-751 85 Uppsala, Sweden and the Program for Genomics and Bioinformatics, Department of Cell and Molecular Biology, Karolinska Institute, SE-171 77 Stockholm, Sweden

Trypanosomes are ancient eukaryotic parasites in which the protein-coding genes, organized in large polycistronic clusters on both strands, are transcribed from as yet unidentified promoters. In an effort to reveal transcriptional initiation sites, we examined the Trypanosoma cruzi genome for histone modification patterns shown to be linked to active genes in various organisms. Here, we show that acetylated and methylated histones were found to be enriched at strand switch regions of divergent gene arrays, not at convergent clusters or intra- and intergenic regions within clusters. The modified region showed a bimodular profile with two peaks centered over the 5'-regions of the gene pair flanking the strand switch region. This pattern, which demarcates polycistronic transcription units originating from bidirectional initiation sites, is likely to be common in kinetoplastid parasites as well as in other organisms with polycistronic transcription. In contrast, no acetylation was found at promoters of the highly expressed rRNA and spliced leader genes or satellite DNA or at tested retrotransposonal elements. These results reveal, for the first time, the presence of specific epigenetic marks in T. cruzi with potential implications for transcriptional regulation; they indicate that both histone modifications and bidirectional transcription are evolutionarily conserved.

Received for publication, March 17, 2008

^* This work was supported in part by grants from the Swedish International Development Cooperation Agency (SWE-2006-499 and SWE-2001-392), Indevelops U-landsfond Uppsala University, and the Gunvor and Josef Anér and Magn Bergwall Foundations (to L. Å.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S5–S12 and Tables S1–S3.

¹ Supported by a fellowship from the Swedish Institute (00514/2005210) and by Swedish International Development Cooperation Agency Grant SWE-2006-499.

² Current address: Linnaeus Centre for Bioinformatics, Uppsala University, SE-751 85 Uppsala, Sweden.

³ To whom correspondence should be addressed: Dept. of Genetics and Pathology, Rudbeck Laboratory, SE75185 Uppsala, Sweden. Fax: 46-18-4714808; E-mail: lena.aslund{at}genpat.uu.se.

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