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      PRP-19, a conserved pre-mRNA processing factor and E3 ubiquitin ligase, inhibits the nuclear accumulation of GLP-1/Notch intracellular domain

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          ABSTRACT

          The Notch signalling pathway is a conserved and widespread signalling paradigm, and its misregulation has been implicated in numerous disorders, including cancer. The output of Notch signalling depends on the nuclear accumulation of the Notch receptor intracellular domain (ICD). Using the Caenorhabditis elegans germline, where GLP-1/Notch-mediated signalling is essential for maintaining stem cells, we monitored GLP-1 in vivo. We found that the nuclear enrichment of GLP-1 ICD is dynamic: while the ICD is enriched in germ cell nuclei during larval development, it is depleted from the nuclei in adult germlines. We found that this pattern depends on the ubiquitin proteolytic system and the splicing machinery and, identified the splicing factor PRP-19 as a candidate E3 ubiquitin ligase required for the nuclear depletion of GLP-1 ICD.

          Abstract

          Summary: GFP tagging of endogenous GLP-1/Notch revealed life stage-specific differences in the nuclear accumulation of GLP-1 intracellular domain, which are mediated by the ubiquitin-proteolytic system and the splicing factor/E3 ubiquitin ligase PRP-19.

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          Most cited references53

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          The SCF ubiquitin ligase: insights into a molecular machine.

          Ubiquitin ligases are well suited to regulate molecular networks that operate on a post-translational timescale. The F-box family of proteins - which are the substrate-recognition components of the Skp1-Cul1-F-box-protein (SCF) ubiquitin ligase - are important players in many mammalian functions. Here we explore a unifying and structurally detailed view of SCF-mediated proteolytic control of cellular processes that has been revealed by recent studies.
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            glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans.

            In the wild-type C. elegans germ line there are both mitotic and meiotic germ cells. Mutations in glp-1 cause germ cells that would normally divide mitotically to enter meiosis. This mutant phenotype mimics the effect of killing the distal tip cell, a somatic cell that interacts with the germ line to regulate the mitotic/meiotic decision. In addition, wild-type glp-1 product is required maternally for embryogenesis. Temperature-shift experiments indicate that the temporal requirement for glp-1 activity in the germ line is the same as that for distal tip cell regulation. Mosaic analyses suggest that glp-1 is produced in the germ line. We propose that glp-1 acts as part of the receiving mechanism in the interaction between the distal tip cell and germ line.
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              Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans.

              The Caenorhabditis elegans germ line provides an exceptional model for analysis of the molecular controls governing stem cell maintenance, the cell cycle transition from mitosis to meiosis, and the choice of sexual identity-sperm or oocyte. Germline stem cells are maintained in an undifferentiated state within a well-defined niche formed by a single somatic cell, the distal tip cell (DTC). In both sexes, the DTC employs GLP-1/Notch signaling and FBF/PUF RNA-binding proteins to maintain stem cells and promote mitotic divisions, three additional RNA regulators (GLD-1/quaking, GLD-2/poly(A) polymerase, and GLD-3/Bicaudal-C) control entry into meiosis, and FOG-1/CPEB and FOG-3/Tob proteins govern sperm specification. These key regulators are part of a robust regulatory network that controls germ cell proliferation, stem cell maintenance, and sex determination. Parallels with controls in other organisms include the use of PUF proteins for stem cell maintenance and the prominence of mRNA regulation for the control of germline development.
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                Author and article information

                Journal
                Biol Open
                Biol Open
                bio
                biolopen
                Biology Open
                The Company of Biologists Ltd
                2046-6390
                15 July 2018
                15 July 2018
                15 July 2018
                : 7
                : 7
                : bio034066
                Affiliations
                [1 ]Friedrich Miescher Institute for Biomedical Research , Maulbeerstrasse 66, 4058 Basel, Switzerland
                [2 ]University of Basel , Petersplatz 1, 4001 Basel, Switzerland
                [3 ]Cell Cycle and Development, Institut Jacques Monod, UMR7592 CNRS - Université Paris Diderot, Sorbonne Paris Cité , F-75013 Paris, France
                [4 ]Department of Biosciences, Faculty of Mathematics and Natural Sciences, University of Oslo , 0316 Oslo, Norway
                [5 ]Sorbonne Université, CNRS, Institut de Biologie Paris-Seine (IBPS) , Developmental Biology Laboratory, UMR 7622, F-75005 Paris, France
                [6 ]Institute of Bioorganic Chemistry, Polish Academy of Sciences , Noskowskiego 12/14, 61-704 Poznan, Poland
                Author notes
                Author information
                http://orcid.org/0000-0001-9873-9556
                http://orcid.org/0000-0002-1918-3527
                http://orcid.org/0000-0003-2234-6216
                Article
                BIO034066
                10.1242/bio.034066
                6078339
                30012553
                a6cac922-3481-479b-ada7-3d1760a846e8
                © 2018. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 8 March 2018
                : 15 June 2018
                Funding
                Funded by: European Cooperation in Science and Technology, http://dx.doi.org/10.13039/501100000921;
                Award ID: C15.0038
                Funded by: National Science Centre, http://dx.doi.org/10.13039/501100004442;
                Award ID: 2015/19/B/NZ3/02412
                Funded by: EMBO, http://dx.doi.org/10.13039/100004410;
                Funded by: Foundation for Polish Science, http://dx.doi.org/10.13039/501100001870;
                Award ID: TEAM/2016-2/11
                Funded by: Novartis Research Foundation;
                Funded by: Fondation pour la Recherche Médicale;
                Award ID: DEQ20140329538
                Funded by: Labex, http://dx.doi.org/10.13039/501100004100;
                Award ID: ANR-11-LABX-0071
                Funded by: French National Research Agency, http://dx.doi.org/10.13039/501100001665;
                Award ID: ANR-11-IDEX-0005-01
                Categories
                Research Article

                Life sciences
                caenorhabditis elegans,glp-1,notch,prp-19,splicing,ubiquitin ligase
                Life sciences
                caenorhabditis elegans, glp-1, notch, prp-19, splicing, ubiquitin ligase

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