Title

Translational control of the oogenic program by components of OMA ribonucleoprotein particles in caenorhabditis elegans

Document Type

Article

Source of Publication

Genetics

Publication Date

12-1-2014

Abstract

© 2014 by the Genetics Society of America. The oocytes of most sexually reproducing animals arrest in meiotic prophase I. Oocyte growth, which occurs during this period of arrest, enables oocytes to acquire the cytoplasmic components needed to produce healthy progeny and to gain competence to complete meiosis. In the nematode Caenorhabditis elegans, the major sperm protein hormone promotes meiotic resumption (also called meiotic maturation) and the cytoplasmic flows that drive oocyte growth. Prior work established that two related TIS11 zincfinger RNA-binding proteins, OMA-1 and OMA-2, are redundantly required for normal oocyte growth and meiotic maturation. We affinity purified OMA-1 and identified associated mRNAs and proteins using genome-wide expression data and mass spectrometry, respectively. As a class, mRNAs enriched in OMA-1 ribonucleoprotein particles (OMA RNPs) have reproductive functions. Several of these mRNAs were tested and found to be targets of OMA-1/2-mediated translational repression, dependent on sequences in their 3′-untranslated regions (3′-UTRs). Consistent with a major role for OMA-1 and OMA-2 in regulating translation, OMA-1-associated proteins include translational repressors and activators, and some of these proteins bind directly to OMA-1 in yeast two-hybrid assays, including OMA-2. We show that the highly conserved TRIM-NHL protein LIN-41 is an OMA-1-associated protein, which also represses the translation of several OMA-1/2 target mRNAs. In the accompanying article in this issue, we show that LIN-41 prevents meiotic maturation and promotes oocyte growth in opposition to OMA-1/2. Taken together, these data support a model in which the conserved regulators of mRNA translation LIN-41 and OMA-1/2 coordinately control oocyte growth and the proper spatial and temporal execution of the meiotic maturation decision.

ISSN

0016-6731

Publisher

Genetics Society of America

Volume

198

Issue

4

First Page

1513

Last Page

1533

Disciplines

Chemistry | Life Sciences

Keywords

butyrate response factor 1; LIN 41 protein; messenger RNA; OMA 1 ribonucleoprotein; OMA 2 ribonucleoprotein; ribonucleoprotein; RNA binding protein; unclassified drug; 3' untranslated region; Caenorhabditis elegans protein; carrier protein; egg protein; messenger RNA; OMA-1 protein, C elegans; oma-2 protein, C elegans; protein binding; ribonucleoprotein; 3' untranslated region; animal cell; animal tissue; Article; Caenorhabditis elegans; cell maturation; controlled study; embryo; female; gene repression; mass spectrometry; meiosis; nonhuman; nucleotide sequence; oocyte; oocyte development; protein analysis; protein expression; protein protein interaction; protein purification; reproduction; translation regulation; translational repression; two hybrid system; animal; binding site; Caenorhabditis elegans; chemistry; gene expression regulation; genetics; metabolism; protein synthesis; RNA interference; Caenorhabditis elegans; 3' Untranslated Regions; Animals; Binding Sites; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Carrier Proteins; Egg Proteins; Female; Gene Expression Regulation; Meiosis; Oogenesis; Protein Binding; Protein Biosynthesis; Protein Interaction Mapping; Ribonucleoproteins; RNA Interference; RNA, Messenger

Scopus ID

84915750475

Indexed in Scopus

yes

Open Access

yes

Open Access Type

Bronze: This publication is openly available on the publisher’s website but without an open license

Share

COinS