O-GlcNAcase Is an RNA Polymerase II Elongation Factor Coupled to Pausing Factors SPT5 and TIF1β

J Biol Chem. 2016 Oct 21;291(43):22703-22713. doi: 10.1074/jbc.M116.751420. Epub 2016 Sep 6.

Abstract

We describe here the identification and functional characterization of the enzyme O-GlcNAcase (OGA) as an RNA polymerase II elongation factor. Using in vitro transcription elongation assays, we show that OGA activity is required for elongation in a crude nuclear extract system, whereas in a purified system devoid of OGA the addition of rOGA inhibited elongation. Furthermore, OGA is physically associated with the known RNA polymerase II (pol II) pausing/elongation factors SPT5 and TRIM28-KAP1-TIF1β, and a purified OGA-SPT5-TIF1β complex has elongation properties. Lastly, ChIP-seq experiments show that OGA maps to the transcriptional start site/5' ends of genes, showing considerable overlap with RNA pol II, SPT5, TRIM28-KAP1-TIF1β, and O-GlcNAc itself. These data all point to OGA as a component of the RNA pol II elongation machinery regulating elongation genome-wide. Our results add a novel and unexpected dimension to the regulation of elongation by the insertion of O-GlcNAc cycling into the pol II elongation regulatory dynamics.

Keywords: O-GlcNAcylation; RNA polymerase II; metabolism; transcription; transcription elongation factor.

MeSH terms

  • Antigens, Neoplasm / chemistry*
  • Antigens, Neoplasm / metabolism
  • Histone Acetyltransferases / chemistry*
  • Histone Acetyltransferases / metabolism
  • Humans
  • Hyaluronoglucosaminidase / chemistry*
  • Hyaluronoglucosaminidase / metabolism
  • Nuclear Proteins / chemistry*
  • Nuclear Proteins / metabolism
  • RNA Polymerase II / chemistry*
  • RNA Polymerase II / metabolism
  • Repressor Proteins / chemistry*
  • Repressor Proteins / metabolism
  • Transcription Elongation, Genetic / physiology
  • Transcriptional Elongation Factors / chemistry*
  • Transcriptional Elongation Factors / metabolism
  • Tripartite Motif-Containing Protein 28

Substances

  • Antigens, Neoplasm
  • Nuclear Proteins
  • Repressor Proteins
  • SUPT5H protein, human
  • Transcriptional Elongation Factors
  • Histone Acetyltransferases
  • TRIM28 protein, human
  • Tripartite Motif-Containing Protein 28
  • RNA Polymerase II
  • OGA protein, human
  • Hyaluronoglucosaminidase