Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation

Genes Dev. 2006 Jan 15;20(2):199-209. doi: 10.1101/gad.1383106.

Abstract

CPEB is a sequence-specific RNA-binding protein that controls the polyadenylation-induced translation of mos and cyclin B1 mRNAs in maturing Xenopus oocytes. CPEB activity requires not only the phosphorylation of S174, but also the synthesis of a heretofore-unknown upstream effector molecule. We show that the synthesis of RINGO/Spy, an atypical activator of cyclin-dependent kinases (cdks), is necessary for CPEB-directed polyadenylation. Deletion analysis and mRNA reporter assays show that a cis element in the RINGO/Spy 3'UTR is necessary for translational repression in immature (G2-arrested) oocytes. The repression is mediated by 3'UTR Pumilio-Binding Elements (PBEs), and by its binding protein Pumilio 2 (Pum2). Pum2 also interacts with the Xenopus homolog of human Deleted for Azoospermia-like (DAZL) and the embryonic poly(A)-binding protein (ePAB). Following the induction of maturation, Pum2 dissociates not only from RINGO/Spy mRNA, but from XDAZL and ePAB as well; as a consequence, RINGO/Spy mRNA is translated. These results demonstrate that a reversible Pum2 interaction controls RINGO/Spy mRNA translation and, as a result, CPEB-mediated cytoplasmic polyadenylation.

Publication types

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

MeSH terms

  • 3' Untranslated Regions / genetics
  • 3' Untranslated Regions / metabolism
  • Animals
  • Base Sequence
  • Carrier Proteins / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Gene Expression Regulation, Developmental
  • Humans
  • Models, Biological
  • Molecular Sequence Data
  • Oocytes / drug effects
  • Oocytes / enzymology
  • Oocytes / metabolism
  • Poly(A)-Binding Proteins / metabolism
  • Polyadenylation
  • Progesterone / metabolism
  • Progesterone / pharmacology
  • Protein Binding / genetics
  • Protein Biosynthesis / genetics*
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / immunology
  • RNA-Binding Proteins / metabolism*
  • Transcription Factors / metabolism*
  • Xenopus
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism*
  • mRNA Cleavage and Polyadenylation Factors

Substances

  • 3' Untranslated Regions
  • Carrier Proteins
  • Cell Cycle Proteins
  • Cpeb1 protein, Xenopus
  • Dazl protein, Xenopus
  • PABPC4 protein, Xenopus
  • PUM1 protein, Xenopus
  • PUM2 protein, human
  • Poly(A)-Binding Proteins
  • Pum2 protein, Xenopus
  • RNA, Messenger
  • RNA-Binding Proteins
  • Transcription Factors
  • Xenopus Proteins
  • ls27 protein, Xenopus
  • mRNA Cleavage and Polyadenylation Factors
  • Progesterone