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

Caroline A. Spike, Donna Coetzee, Yuichi Nishi, Tugba Guven-Ozkan, Marieke Oldenbroek, Ikuko Yamamoto, Rueyling Lin, David Greenstein

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)1513-1533
Number of pages21
JournalGenetics
Volume198
Issue number4
DOIs
StatePublished - Dec 1 2014

Fingerprint

Ribonucleoproteins
Caenorhabditis elegans
Oocytes
Growth
Messenger RNA
Proteins
Meiotic Prophase I
Two-Hybrid System Techniques
RNA-Binding Proteins
Meiosis
Protein Biosynthesis
3' Untranslated Regions
Mental Competency
Spermatozoa
Mass Spectrometry
Genome
Hormones

ASJC Scopus subject areas

  • Genetics

Cite this

Spike, C. A., Coetzee, D., Nishi, Y., Guven-Ozkan, T., Oldenbroek, M., Yamamoto, I., ... Greenstein, D. (2014). Translational control of the oogenic program by components of OMA ribonucleoprotein particles in caenorhabditis elegans. Genetics, 198(4), 1513-1533. https://doi.org/10.1534/genetics.114.168823

Translational control of the oogenic program by components of OMA ribonucleoprotein particles in caenorhabditis elegans. / Spike, Caroline A.; Coetzee, Donna; Nishi, Yuichi; Guven-Ozkan, Tugba; Oldenbroek, Marieke; Yamamoto, Ikuko; Lin, Rueyling; Greenstein, David.

In: Genetics, Vol. 198, No. 4, 01.12.2014, p. 1513-1533.

Research output: Contribution to journalArticle

Spike, CA, Coetzee, D, Nishi, Y, Guven-Ozkan, T, Oldenbroek, M, Yamamoto, I, Lin, R & Greenstein, D 2014, 'Translational control of the oogenic program by components of OMA ribonucleoprotein particles in caenorhabditis elegans', Genetics, vol. 198, no. 4, pp. 1513-1533. https://doi.org/10.1534/genetics.114.168823
Spike, Caroline A. ; Coetzee, Donna ; Nishi, Yuichi ; Guven-Ozkan, Tugba ; Oldenbroek, Marieke ; Yamamoto, Ikuko ; Lin, Rueyling ; Greenstein, David. / Translational control of the oogenic program by components of OMA ribonucleoprotein particles in caenorhabditis elegans. In: Genetics. 2014 ; Vol. 198, No. 4. pp. 1513-1533.
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