Lin-41 and oma ribonucleoprotein complexes mediate a translational repression-to-activation switch controlling oocyte meiotic maturation and the oocyte-to-embryo transition in caenorhabditis elegans

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Abstract

An extended meiotic prophase is a hallmark of oogenesis. Hormonal signaling activates the CDK1/cyclin B kinase to promote oocyte meiotic maturation, which involves nuclear and cytoplasmic events. Nuclear maturation encompasses nuclear envelope breakdown, meiotic spindle assembly, and chromosome segregation. Cytoplasmic maturation involves major changes in oocyte protein translation and cytoplasmic organelles and is poorly understood. In the nematode Caenorhabditis elegans, sperm release the major sperm protein (MSP) hormone to promote oocyte growth and meiotic maturation. Large translational regulatory ribonucleoprotein (RNP) complexes containing the RNA-binding proteins OMA-1, OMA-2, and LIN-41 regulate meiotic maturation downstream of MSP signaling. To understand the control of translation during meiotic maturation, we purified LIN-41-containing RNPs and characterized their protein and RNA components. Protein constituents of LIN-41 RNPs include essential RNA-binding proteins, the GLD-2 cytoplasmic poly(A) polymerase, the CCR4-NOT deadenylase complex, and translation initiation factors. RNA sequencing defined messenger RNAs (mRNAs) associated with both LIN-41 and OMA-1, as well as sets of mRNAs associated with either LIN-41 or OMA-1. Genetic and genomic evidence suggests that GLD-2, which is a component of LIN-41 RNPs, stimulates the efficient translation of many LIN-41-associated transcripts. We analyzed the translational regulation of two transcripts specifically associated with LIN-41 which encode the RNA regulators SPN-4 and MEG-1. We found that LIN-41 represses translation of spn-4 and meg-1, whereas OMA-1 and OMA-2 promote their expression. Upon their synthesis, SPN-4 and MEG-1 assemble into LIN-41 RNPs prior to their functions in the embryo. This study defines a translational repression-to-activation switch as a key element of cytoplasmic maturation.

Original languageEnglish (US)
Pages (from-to)2007-2039
Number of pages33
JournalGenetics
Volume206
Issue number4
DOIs
StatePublished - 2017

Bibliographical note

Funding Information:
We would like to thank Adele Barugahare and the Monash Bioinformatics Platform for contributing to the GLD-2 poly (A) length analysis. We are grateful to Joshua Arribere, Daniel Dickinson, Andrew Fire, Bob Goldstein, Kelly Liu, and Dustin Updike for providing strains or reagents. We thank Daniel Schmidt for guidance using Chimera and Sean Conner, Lorene Lanier, and Gant Luxton for the use of equipment. Swathi Arur, Ann Rougvie, Tim Schedl, Todd Starich, Dustin Updike, and Mariana Wolfner provided helpful suggestions for the manuscript. Some strains were provided by the Caenorhabditis Genetics Center, which is funded by grant P40 OD010440 from the National Institutes of Health Office of Research Infrastructure Programs. We also thank WormBase for sequences and annotations. The monoclonal anti-GFP antibodies developed by the Developmental Studies Hybridoma Bank (DSHB) were obtained from the DSHB created by the National Institute of Child Health and Human Development of the National Institutes of Health and maintained at Department of Biology, The University of Iowa. We thank the University of Minnesota Genomics Center for high-throughput sequencing and the Taplin Mass Spectrometry Facility at Harvard University for generating the spectra used in this study. This work was supported by National Institutes of Health grant GM57173 (to D.G.) and National Health and Medical Research Council of Australia grants APP606575 (to P.R.B.), APP1042848 (to P.R.B. and T.H.B.), and APP1042851 (to T.H.B). T.H.B. is supported by a Monash Biomedicine Discovery Fellowship.

Keywords

  • Cytoplasmic polyadenylation
  • Oocyte meiotic maturation
  • RNA-binding proteins
  • Ribonucleoprotein particle purification
  • Translational regulation

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