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      Genome-wide analysis reveals a switch in the translational program upon oocyte meiotic resumption

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          Abstract

          During oocyte maturation, changes in gene expression depend exclusively on translation and degradation of maternal mRNAs rather than transcription. Execution of this translation program is essential for assembling the molecular machinery required for meiotic progression, fertilization, and embryo development. With the present study, we used a RiboTag/RNA-Seq approach to explore the timing of maternal mRNA translation in quiescent oocytes as well as in oocytes progressing through the first meiotic division. This genome-wide analysis reveals a global switch in maternal mRNA translation coinciding with oocyte re-entry into the meiotic cell cycle. Messenger RNAs whose translation is highly active in quiescent oocytes invariably become repressed during meiotic re-entry, whereas transcripts repressed in quiescent oocytes become activated. Experimentally, we have defined the exact timing of the switch and the repressive function of CPE elements, and identified a novel role for CPEB1 in maintaining constitutive translation of a large group of maternal mRNAs during maturation.

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          Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells.

          R Desrosiers, K Friderici, F Rottman (1974)
          The poly(A) tract found in eukaryotic mRNA was used to study methylation in mRNA obtained from Novikoff hepatoma cells. Methyl labeling of RNA was achieved with L-[methyl-(3)H]methionine under conditions that suppress radioactive incorporation into the purine ring. RNA that contains a poly(A) segment was obtained from polysomal RNA by chromatography on oligo(dT)-cellulose. Sucrose density gradient centrifugation of this RNA revealed a pattern expected for mRNA. The composition of the methyl-labeled nucleosides in the RNA was analyzed after complete enzymatic degradation to nucleosides. By use of DEAE-cellulose (borate) chromatography, which separates 2'-O-methylnucleosides from normal and base-methylated nucleosides, about 50% of the radioactivity was recovered in the 2'-O-methylnucleoside fraction and 50% in the base-methylnucleoside fraction. High-speed liquid chromatography (Aminex A-5) of the 2'-O-methylnucleoside fraction produced four peaks coincident with the four 2'-O-methylnucleoside standards. Analysis of the base-methylnucleoside fraction revealed a unique pattern. While ribosomal RNA and tRNA possessed complex base-methylnucleoside patterns, the distribution in mRNA was quite simple, consisting predominantly of N(6)-methyladenosine. These results demonstrate a unique distribution of methylated nucleosides in mRNA. By analogy to ribosomal RNA synthesis, the presence of methylnucleosides in mRNA may reflect a cellular mechanism for the selective processing of certain mRNA sequences.
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            Poly(A)-tail profiling reveals an embryonic switch in translational control

            Alexander Subtelny, Stephen Eichhorn, Grace R. Chen … (2014)
            Poly(A) tails enhance the stability and translation of most eukaryotic mRNAs, but difficulties in globally measuring poly(A)-tail lengths have impeded greater understanding of poly(A)-tail function. Here, we describe poly(A)-tail length profiling by sequencing (PAL-seq) and apply it to measure tail lengths of millions of individual RNAs isolated from yeasts, cell lines, Arabidopsis leaves, mouse liver, and zebrafish and frog embryos. Poly(A)-tail lengths were conserved between orthologous mRNAs, with mRNAs encoding ribosomal proteins and other “housekeeping” proteins tending to have shorter tails. As expected, tail lengths were coupled to translational efficiency in early zebrafish and frog embryos. However, this strong coupling diminished at gastrulation and was absent in non-embryonic samples, indicating a rapid developmental switch in the nature of translational control. This switch complements an earlier switch to zygotic transcriptional control and explains why the predominant effect of microRNA-mediated deadenylation concurrently shifts from translational repression to mRNA destabilization.
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              Modified nucleosides and bizarre 5'-termini in mouse myeloma mRNA.

              J. Adams, Jenny Cory (1975)
              Messenger RNAs from mouse myeloma cells contain N-6-methyl adenosine and novel 5' termini having 7-methy-guanosine in a 5', 5' triphosphate linkage with ribose-methylated nucleosides. Ten common 5'-terminal sequences of the forms m-7-G-5'-PPP-5'-NmpNp and m-7-G-5'-ppp-5'-NmpNmpNp are reported. Structures like this may be a general feature of mRNA in eukaryotes.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Nucleic Acids Res
                Journal ID (iso-abbrev): Nucleic Acids Res
                Journal ID (publisher-id): nar
                Title: Nucleic Acids Research
                Publisher: Oxford University Press
                ISSN (Print): 0305-1048
                ISSN (Electronic): 1362-4962
                Publication date (Print): 06 April 2020
                Publication date (Electronic): 23 January 2020
                Publication date PMC-release: 23 January 2020
                Volume: 48
                Issue: 6
                Pages: 3257-3276
                Affiliations
                [1 ] Center for Reproductive Sciences, University of California , San Francisco, CA 94143, USA
                [2 ] Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California , San Francisco, CA 94143, USA
                [3 ]Department of Obstetrics and Gynecology and Reproductive Sciences, University of California , San Francisco, CA 94143, USA
                Author notes
                To whom correspondence should be addressed. Tel: +1 415 476 9214; Fax: +1 415 502 7866; Email: marco.conti@ 123456ucsf.edu

                The authors wish it to be known that, in their opinion, the first two authors should be regarded as Joint First Authors.

                Author information
                http://orcid.org/0000-0003-0600-8778
                Article
                Publisher ID: gkaa010
                DOI: 10.1093/nar/gkaa010
                PMC ID: 7102970
                PubMed ID: 31970406
                SO-VID: 64425205-455b-429a-a103-98ac8f97fb3d
                Copyright © © The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                Date accepted : 03 January 2020
                Date revision received : 27 December 2019
                Date received : 07 August 2019
                Page count
                Pages: 20
                Funding
                Funded by: National Institutes of Health, DOI 10.13039/100000002;
                Award ID: R01 GM116926
                Award ID: P50 HD055764
                Funded by: Lalor Foundation, DOI 10.13039/100012756;
                Categories
                Subject: AcademicSubjects/SCI00010
                Subject: RNA and RNA-protein complexes

                ScienceOpen disciplines: Genetics
                Data availability:
                ScienceOpen disciplines: Genetics

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