title: Translational control of the oogenic program by components of OMA ribonucleoprotein particles in Caenorhabditis elegans.
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 zinc-finger 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.
authors.affiliation: Department of Genetics, Cell Biology and Development, University of Minnesota Minneapolis, Minnesota 55455.
authors.forename: Caroline A
authors.initials: CA
authors.lastname: Spike
authors.affiliation: Department of Genetics, Cell Biology and Development, University of Minnesota Minneapolis, Minnesota 55455.
authors.forename: Donna
authors.initials: D
authors.lastname: Coetzee
authors.affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390.
authors.forename: Yuichi
authors.initials: Y
authors.lastname: Nishi
authors.affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390.
authors.forename: Tugba
authors.initials: T
authors.lastname: Guven-Ozkan
authors.affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390.
authors.forename: Marieke
authors.initials: M
authors.lastname: Oldenbroek
authors.affiliation: Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee 37232.
authors.forename: Ikuko
authors.initials: I
authors.lastname: Yamamoto
authors.affiliation: Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, Texas 75390.
authors.forename: Rueyling
authors.initials: R
authors.lastname: Lin
authors.affiliation: Department of Genetics, Cell Biology and Development, University of Minnesota Minneapolis, Minnesota 55455 green959@umn.edu.
authors.forename: David
authors.identifier: http://orcid.org/0000-0001-8189-2087
authors.initials: D
authors.lastname: Greenstein
mesh_terms: D020413:3' Untranslated Regions; D000818:Animals; D001665:Binding Sites; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D002352:Carrier Proteins / Q000378:metabolism; D004527:Egg Proteins / Q000378:metabolism*; D005260:Female; D005786:Gene Expression Regulation; D008540:Meiosis; D009866:Oogenesis; D011485:Protein Binding; D014176:Protein Biosynthesis; D025941:Protein Interaction Mapping; D034622:RNA Interference; D012333:RNA, Messenger / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D012261:Ribonucleoproteins / Q000378:metabolism*
chemical_list: D020413:3' Untranslated Regions; D029742:Caenorhabditis elegans Proteins; D002352:Carrier Proteins; D004527:Egg Proteins; C440205:OMA-1 protein, C elegans; D012333:RNA, Messenger; D012261:Ribonucleoproteins; C473076:oma-2 protein, C elegans
keywords: RNA-binding proteins; oocyte growth; oocyte meiotic maturation; ribonucleoprotein particle purification; translational regulation