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Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs
Kouji Hirota1,2,4, Tomoichiro Miyoshi2, Kazuto Kugou1,2, Charles S. Hoffman3, Takehiko Shibata1 & Kunihiro Ohta1,2
1 Cellular & Molecular Biology Laboratory, RIKEN Advanced Science Institute, Wako-shi, Saitama 351-0198, Japan
2 Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan
3 Biology Department, Boston College, Chestnut Hill, Massachusetts 02467, USA
4 Present address: Department of Radiation Genetics, Kyoto University Graduate School of Medicine, Yoshida Konoe, Sakyo-ku, Kyoto 606-8501, Japan.
Recent transcriptome analyses using high-density tiling arrays1, 2, 3 and data from large-scale analyses of full-length complementary DNA libraries by the FANTOM3 consortium4, 5 demonstrate that many transcripts are non-coding RNAs (ncRNAs). These transcriptome analyses indicate that many of the non-coding regions, previously thought to be functionally inert, are actually transcriptionally active regions with various features. Furthermore, most relatively large (several kilobases) polyadenylated messenger RNA transcripts are transcribed from regions harbouring little coding potential. However, the function of such ncRNAs is mostly unknown and has been a matter of debate2. Here we show that RNA polymerase II (RNAPII) transcription of ncRNAs is required for chromatin remodelling at the fission yeast Schizosaccharomyces pombe fbp1 + locus during transcriptional activation. The chromatin at fbp1 + is progressively converted to an open configuration, as several species of ncRNAs are transcribed through fbp1 +. This is coupled with the translocation of RNAPII through the region upstream of the eventual fbp1 + transcriptional start site. Insertion of a transcription terminator into this upstream region abolishes both the cascade of transcription of ncRNAs and the progressive chromatin alteration. Our results demonstrate that transcription through the promoter region is required to make DNA sequences accessible to transcriptional activators and to RNAPII.
