The Fun30 chromatin remodeler Fft3 controls nuclear organization and chromatin structure of insulators and subtelomeres in fission yeast

PLoS Genet. 2015 Mar 23;11(3):e1005101. doi: 10.1371/journal.pgen.1005101. eCollection 2015 Mar.

Abstract

In eukaryotic cells, local chromatin structure and chromatin organization in the nucleus both influence transcriptional regulation. At the local level, the Fun30 chromatin remodeler Fft3 is essential for maintaining proper chromatin structure at centromeres and subtelomeres in fission yeast. Using genome-wide mapping and live cell imaging, we show that this role is linked to controlling nuclear organization of its targets. In fft3∆ cells, subtelomeres lose their association with the LEM domain protein Man1 at the nuclear periphery and move to the interior of the nucleus. Furthermore, genes in these domains are upregulated and active chromatin marks increase. Fft3 is also enriched at retrotransposon-derived long terminal repeat (LTR) elements and at tRNA genes. In cells lacking Fft3, these sites lose their peripheral positioning and show reduced nucleosome occupancy. We propose that Fft3 has a global role in mediating association between specific chromatin domains and the nuclear envelope.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Nucleus / genetics
  • Chromatin / genetics*
  • Chromatin Assembly and Disassembly / genetics*
  • Chromosomal Proteins, Non-Histone / biosynthesis
  • Chromosomal Proteins, Non-Histone / genetics*
  • Gene Expression Regulation, Fungal
  • Insulator Elements / genetics
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / genetics
  • Nuclear Proteins / biosynthesis
  • Nuclear Proteins / genetics
  • Nucleosomes / genetics
  • RNA, Transfer / genetics
  • Schizosaccharomyces
  • Schizosaccharomyces pombe Proteins / biosynthesis
  • Schizosaccharomyces pombe Proteins / genetics*
  • Telomere / genetics*
  • Terminal Repeat Sequences / genetics
  • Transcription, Genetic*

Substances

  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • Fft3 protein, S pombe
  • Man1 protein, S pombe
  • Membrane Proteins
  • Nuclear Proteins
  • Nucleosomes
  • Schizosaccharomyces pombe Proteins
  • RNA, Transfer

Associated data

  • GEO/GSE58013

Grants and funding

This study was in part performed at the Live Cell Imaging unit/Nikon Center of Excellence, Department of Biosciences and Nutrition, Karolinska Institutet, Huddinge, Sweden, supported by grants from the Knut and Alice Wallenberg Foundation, the Swedish Research Council, the Centre for Innovative Medicine and the Jonasson donation to the School of Technology and Health, Kungliga Tekniska Högskolan, Huddinge, Sweden. Research in the Ekwall laboratory is supported by grants from the Swedish Cancer Society (CAN 2012/238) and the Swedish Research Council (grant numbers VR-M 2579 and VR-NT 4448). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.