The inner nuclear membrane proteins Man1 and Ima1 link to two different types of chromatin at the nuclear periphery in S. pombe

Nucleus. Jan-Feb 2012;3(1):77-87. doi: 10.4161/nucl.18825.

Abstract

Metazoan chromatin at the nuclear periphery is generally characterized by lowly expressed genes and repressive chromatin marks and presents a sub-compartment with properties distinct from the nuclear interior. To test whether the S. pombe nuclear periphery behaves similarly, we used DNA adenine methyltransferase identification (DamID) to map the target loci of two inner nuclear membrane proteins, Ima1 and Man1. We found that peripheral chromatin shows low levels of RNA-Polymerase II and nucleosome occupancy, both characteristic of repressed chromatin regions. Consistently, lowly expressed genes preferentially associate with the periphery and highly expressed genes are depleted from it. When looking at peripheral intergenic regions (IGRs), we found that divergent IGRs are enriched compared with convergent IGRs, indicating that transcription preferentially points away from the periphery rather than toward it. Interestingly, we found that Ima1 and Man1 have common, but also separate target regions in the genome. Ima1-interacting loci were enriched for the RNAi components Dcr1 and Rdp1. This agrees with previous findings that Dcr1 is localized at the nuclear periphery. In contrast, Man1 target loci were bound by the heterochromatin protein Swi6, especially at subtelomeric regions. Subtelomeric chromatin was shown to form a unique chromatin type lacking both repressive and active chromatin features and containing low levels of the histone variant H2A.Z. Thus, we find that the fission yeast nuclear periphery shows similar properties to those of metazoan cells, despite the absence of a nuclear lamina. Our results point to a role of nuclear membrane proteins in organizing chromatin domains and loops.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Chromatin / genetics*
  • Chromatin / metabolism
  • Genetic Loci / genetics
  • Genome, Fungal / genetics
  • Membrane Proteins / chemistry
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Molecular Sequence Data
  • Nuclear Envelope / genetics*
  • Nuclear Envelope / metabolism
  • Nuclear Proteins / chemistry
  • Nuclear Proteins / deficiency
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • RNA Interference
  • Schizosaccharomyces / cytology*
  • Schizosaccharomyces / genetics*
  • Schizosaccharomyces / metabolism
  • Schizosaccharomyces pombe Proteins / chemistry
  • Schizosaccharomyces pombe Proteins / genetics*
  • Schizosaccharomyces pombe Proteins / metabolism
  • Site-Specific DNA-Methyltransferase (Adenine-Specific) / metabolism
  • Telomere / genetics
  • Telomere / metabolism

Substances

  • Chromatin
  • Ima1 protein, S pombe
  • Man1 protein, S pombe
  • Membrane Proteins
  • Nuclear Proteins
  • Schizosaccharomyces pombe Proteins
  • Site-Specific DNA-Methyltransferase (Adenine-Specific)