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

Jing Chen; Simona Torcia; Fang Xie; Chih-Jen Lin; Hakan Cakmak; Federica Franciosi; Kathleen Horner; Courtney Onodera; Jun S Song; Marcelle I Cedars; Miguel Ramalho-Santos; Marco Conti

doi:10.1038/ncb2873

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.

Authors

Jing Chen¹, Simona Torcia, Fang Xie, Chih-Jen Lin, Hakan Cakmak, Federica Franciosi, Kathleen Horner, Courtney Onodera, Jun S Song, Marcelle I Cedars, Miguel Ramalho-Santos, Marco Conti

Affiliation

¹ 1] Center for Reproductive Sciences, University of California, San Francisco, California 94143, USA [2] Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California, San Francisco, California 94143, USA [3] Department of Obstetrics and Gynecology and Reproductive Sciences, University of California, San Francisco, California 94143, USA.

PMID: 24270888
PMCID: PMC4066669
DOI: 10.1038/ncb2873

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

Abstract

Publication types

MeSH terms

Substances

Grants and funding