A network of interdependent molecular interactions describes a higher order Nrd1-Nab3 complex involved in yeast transcription termination

J Biol Chem. 2013 Nov 22;288(47):34158-34167. doi: 10.1074/jbc.M113.516765. Epub 2013 Oct 7.

Abstract

Nab3 and Nrd1 are yeast heterogeneous nuclear ribonucleoprotein (hnRNP)-like proteins that heterodimerize and bind RNA. Genetic and biochemical evidence reveals that they are integral to the termination of transcription of short non-coding RNAs by RNA polymerase II. Here we define a Nab3 mutation (nab3Δ134) that removes an essential part of the protein's C terminus but nevertheless can rescue, in trans, the phenotype resulting from a mutation in the RNA recognition motif of Nab3. This low complexity region of Nab3 appears intrinsically unstructured and can form a hydrogel in vitro. These data support a model in which multiple Nrd1-Nab3 heterodimers polymerize onto substrate RNA to effect termination, allowing complementation of one mutant Nab3 molecule by another lacking a different function. The self-association property of Nab3 adds to the previously documented interactions between these hnRNP-like proteins, RNA polymerase II, and the nascent transcript, leading to a network of nucleoprotein interactions that define a higher order Nrd1-Nab3 complex. This was underscored from the synthetic phenotypes of yeast strains with pairwise combinations of Nrd1 and Nab3 mutations known to affect their distinct biochemical activities. The mutations included a Nab3 self-association defect, a Nab3-Nrd1 heterodimerization defect, a Nrd1-polymerase II binding defect, and an Nab3-RNA recognition motif mutation. Although no single mutation was lethal, cells with any two mutations were not viable for four such pairings, and a fifth displayed a synthetic growth defect. These data strengthen the idea that a multiplicity of interactions is needed to assemble a higher order Nrd1-Nab3 complex that coats specific nascent RNAs in preparation for termination.

Keywords: Gene Regulation; Nab3; Nrd1; Polyglutamine; RNA; RNA Polymerase II; RNA-binding Protein; Transcription Elongation Factors; Transcription Termination.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Motifs
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*
  • Mutation
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Protein Multimerization / physiology
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • RNA, Fungal / biosynthesis*
  • RNA, Fungal / genetics
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Transcription Termination, Genetic / physiology*

Substances

  • Multiprotein Complexes
  • NAB3 protein, S cerevisiae
  • NRD1 protein, S cerevisiae
  • Nuclear Proteins
  • RNA, Fungal
  • RNA-Binding Proteins
  • Saccharomyces cerevisiae Proteins
  • RNA Polymerase II