Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes

Nat Cell Biol. 2013 Dec;15(12):1415-23. doi: 10.1038/ncb2873. Epub 2013 Nov 24.

Abstract

Germ cells divide and differentiate in a unique local microenvironment under the control of somatic cells. Signals released in this niche instruct oocyte reentry into the meiotic cell cycle. Once initiated, the progression through meiosis and the associated programme of maternal messenger RNA translation are thought to be cell autonomous. Here we show that translation of a subset of maternal mRNAs critical for embryo development is under the control of somatic cell inputs. Translation of specific maternal transcripts increases in oocytes cultured in association with somatic cells and is sensitive to EGF-like growth factors that act only on the somatic compartment. In mice deficient in amphiregulin, decreased fecundity and oocyte developmental competence is associated with defective translation of a subset of maternal mRNAs. These somatic cell signals that affect translation require activation of the PI(3)K-AKT-mTOR pathway. Thus, mRNA translation depends on somatic cell cues that are essential to reprogramme the oocyte for embryo development.

Publication types

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

MeSH terms

  • Amphiregulin
  • Animals
  • Cell Cycle Proteins
  • Cells, Cultured
  • Cumulus Cells / physiology
  • EGF Family of Proteins
  • Female
  • Gene Expression Regulation*
  • Glycoproteins / genetics
  • Glycoproteins / metabolism
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Meiosis
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Microtubule-Associated Proteins
  • Nuclear Proteins
  • Oocytes / physiology*
  • Oogenesis
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Biosynthesis*
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger, Stored / genetics*
  • RNA, Messenger, Stored / metabolism
  • Signal Transduction
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Amphiregulin
  • Areg protein, mouse
  • Cell Cycle Proteins
  • EGF Family of Proteins
  • Glycoproteins
  • Intercellular Signaling Peptides and Proteins
  • Microtubule-Associated Proteins
  • Nuclear Proteins
  • RNA, Messenger, Stored
  • TPX2 protein, mouse
  • mTOR protein, mouse
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases