title: The TRIM-NHL protein LIN-41 and the OMA RNA-binding proteins antagonistically control the prophase-to-metaphase transition and growth of Caenorhabditis elegans oocytes.
abstract: In many animals, oocytes enter meiosis early in their development but arrest in meiotic prophase I. Oocyte growth, which occurs during this arrest period, enables the acquisition of meiotic competence and the capacity to produce healthy progeny. Meiotic resumption, or meiotic maturation, involves the transition to metaphase I (M phase) and is regulated by intercellular signaling and cyclin-dependent kinase activation. Premature meiotic maturation would be predicted to diminish fertility as the timing of this event, which normally occurs after oocyte growth is complete, is crucial. In the accompanying article in this issue, we identify the highly conserved TRIM-NHL protein LIN-41 as a translational repressor that copurifies with OMA-1 and OMA-2, RNA-binding proteins redundantly required for normal oocyte growth and meiotic maturation. In this article, we show that LIN-41 enables the production of high-quality oocytes and plays an essential role in controlling and coordinating oocyte growth and meiotic maturation. lin-41 null mutants display a striking defect that is specific to oogenesis: pachytene-stage cells cellularize prematurely and fail to progress to diplotene. Instead, these cells activate CDK-1, enter M phase, assemble spindles, and attempt to segregate chromosomes. Translational derepression of the CDK-1 activator CDC-25.3 appears to contribute to premature M-phase entry in lin-41 mutant oocytes. Genetic and phenotypic analyses indicate that LIN-41 and OMA-1/2 exhibit an antagonistic relationship, and we suggest that translational regulation by these proteins could be important for controlling and coordinating oocyte growth and meiotic maturation.
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 Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, Minnesota 55455.
authors.forename: Carly
authors.initials: C
authors.lastname: Eichten
authors.affiliation: Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4.
authors.forename: Xin
authors.initials: X
authors.lastname: Wang
authors.affiliation: Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4.
authors.forename: Dave
authors.initials: D
authors.lastname: Hansen
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: D000818:Animals; D016203:CDC2 Protein Kinase / Q000378:metabolism; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002352:Carrier Proteins / Q000378:metabolism; D002453:Cell Cycle / Q000235:genetics; D005260:Female; D005298:Fertility / Q000235:genetics; D015870:Gene Expression; D005786:Gene Expression Regulation; D023061:Gene Order; D056426:Genetic Loci; D005838:Genotype; D008297:Male; D008540:Meiosis / Q000235:genetics; D008677:Metaphase / Q000235:genetics; D009154:Mutation; D009630:Nondisjunction, Genetic; D009865:Oocytes / Q000378:metabolism*; D009866:Oogenesis / Q000235:genetics; D011418:Prophase / Q000235:genetics; D054730:Protein Interaction Domains and Motifs; D012326:RNA Splicing; D016601:RNA-Binding Proteins / Q000378:metabolism*; D013091:Spermatogenesis / Q000235:genetics; D014157:Transcription Factors / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
chemical_list: D029742:Caenorhabditis elegans Proteins; D002352:Carrier Proteins; C410586:LIN-41 protein, C elegans; C440205:OMA-1 protein, C elegans; D016601:RNA-Binding Proteins; D014157:Transcription Factors; C473076:oma-2 protein, C elegans; D016203:CDC2 Protein Kinase
keywords: RNA-binding proteins; TRIM-NHL protein; oocyte growth; oocyte meiotic maturation; translational regulation