Literature DB >> 27578178

Cyclin CYB-3 controls both S-phase and mitosis and is asymmetrically distributed in the early C. elegans embryo.

W Matthew Michael1.   

Abstract

In early C. elegans embryos the timing of cell division is both invariant and developmentally regulated, yet how the cell cycle is controlled in the embryo and how cell cycle timing impacts early development remain important, unanswered questions. Here, I focus on the cyclin B3 ortholog CYB-3, and show that this cyclin has the unusual property of controlling both the timely progression through S-phase and mitotic entry, suggesting that CYB-3 is both an S-phase-promoting and mitosis-promoting factor. Furthermore, I find that CYB-3 is asymmetrically distributed in the two-cell embryo, such that the somatic precursor AB cell contains ∼2.5-fold more CYB-3 than its sister cell, the germline progenitor P1 CYB-3 is not only physically limited in P1 but also functionally limited, and this asymmetry is controlled by the par polarity network. These findings highlight the importance of the CYB-3 B3-type cyclin in cell cycle regulation in the early embryo and suggest that CYB-3 asymmetry helps establish the well-documented cell cycle asynchrony that occurs during cell division within the P-lineage.
© 2016. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Asynchrony; CYB-3 cyclin; Caenorhabditis elegans; Cell cycle; DNA replication; Early embryo

Mesh:

Substances:

Year:  2016        PMID: 27578178      PMCID: PMC5047676          DOI: 10.1242/dev.141226

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  47 in total

1.  Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans.

Authors:  B Sönnichsen; L B Koski; A Walsh; P Marschall; B Neumann; M Brehm; A-M Alleaume; J Artelt; P Bettencourt; E Cassin; M Hewitson; C Holz; M Khan; S Lazik; C Martin; B Nitzsche; M Ruer; J Stamford; M Winzi; R Heinkel; M Röder; J Finell; H Häntsch; S J M Jones; M Jones; F Piano; K C Gunsalus; K Oegema; P Gönczy; A Coulson; A A Hyman; C J Echeverri
Journal:  Nature       Date:  2005-03-24       Impact factor: 49.962

2.  Evolution of cyclin B3 shows an abrupt three-fold size increase, due to the extension of a single exon in placental mammals, allowing for new protein-protein interactions.

Authors:  Jean-Claude Lozano; Valérie Vergé; Philippe Schatt; Jennifer L Juengel; Gérard Peaucellier
Journal:  Mol Biol Evol       Date:  2012-07-23       Impact factor: 16.240

3.  Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans.

Authors:  Karen L McNally; Francis J McNally
Journal:  Dev Biol       Date:  2005-06-01       Impact factor: 3.582

4.  LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1.

Authors:  Jose M Lizcano; Olga Göransson; Rachel Toth; Maria Deak; Nick A Morrice; Jérôme Boudeau; Simon A Hawley; Lina Udd; Tomi P Mäkelä; D Grahame Hardie; Dario R Alessi
Journal:  EMBO J       Date:  2004-02-19       Impact factor: 11.598

Review 5.  Cell cycle timing regulation during asynchronous divisions of the early C. elegans embryo.

Authors:  N Tavernier; J C Labbé; L Pintard
Journal:  Exp Cell Res       Date:  2015-07-23       Impact factor: 3.905

6.  Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B.

Authors:  H W Jacobs; J A Knoblich; C F Lehner
Journal:  Genes Dev       Date:  1998-12-01       Impact factor: 11.361

7.  PLK-1 asymmetry contributes to asynchronous cell division of C. elegans embryos.

Authors:  Yemima Budirahardja; Pierre Gönczy
Journal:  Development       Date:  2008-02-27       Impact factor: 6.868

8.  HECT-E3 ligase ETC-1 regulates securin and cyclin B1 cytoplasmic abundance to promote timely anaphase during meiosis in C. elegans.

Authors:  Ruishan Wang; Zeenia Kaul; Charuta Ambardekar; Takaharu G Yamamoto; Kanisha Kavdia; Kiran Kodali; Anthony A High; Risa Kitagawa
Journal:  Development       Date:  2013-04-11       Impact factor: 6.868

9.  Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins.

Authors:  P Gallant; E A Nigg
Journal:  EMBO J       Date:  1994-02-01       Impact factor: 11.598

10.  Early transcription in Caenorhabditis elegans embryos.

Authors:  L G Edgar; N Wolf; W B Wood
Journal:  Development       Date:  1994-02       Impact factor: 6.868

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  10 in total

1.  Asymmetric distribution of cyb-3 in 4-cell stage embryos.

Authors:  W Matthew Michael
Journal:  MicroPubl Biol       Date:  2017-03-21

2.  Cycling through mammalian meiosis: B-type cyclins in oocytes.

Authors:  Nora Bouftas; Katja Wassmann
Journal:  Cell Cycle       Date:  2019-06-23       Impact factor: 4.534

Review 3.  Developmental Control of the Cell Cycle: Insights from Caenorhabditis elegans.

Authors:  Edward T Kipreos; Sander van den Heuvel
Journal:  Genetics       Date:  2019-03       Impact factor: 4.562

4.  RPA complexes in Caenorhabditis elegans meiosis; unique roles in replication, meiotic recombination and apoptosis.

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5.  Physically asymmetric division of the C. elegans zygote ensures invariably successful embryogenesis.

Authors:  Radek Jankele; Rob Jelier; Pierre Gönczy
Journal:  Elife       Date:  2021-02-23       Impact factor: 8.140

6.  Cell cycle control during early embryogenesis.

Authors:  Susanna E Brantley; Stefano Di Talia
Journal:  Development       Date:  2021-06-24       Impact factor: 6.862

Review 7.  PLK-1 Regulation of Asymmetric Cell Division in the Early C. elegans Embryo.

Authors:  Amelia J Kim; Erik E Griffin
Journal:  Front Cell Dev Biol       Date:  2021-01-21

8.  Dual RNAseq analyses at soma and germline levels reveal evolutionary innovations in the elephantiasis-agent Brugia malayi, and adaptation of its Wolbachia endosymbionts.

Authors:  Germain Chevignon; Vincent Foray; Mercedes Maria Pérez-Jiménez; Silvia Libro; Matthew Chung; Jeremy M Foster; Frédéric Landmann
Journal:  PLoS Negl Trop Dis       Date:  2021-01-06

9.  R-loop-induced irreparable DNA damage evades checkpoint detection in the C. elegans germline.

Authors:  Tara Hicks; Emily Koury; Caleb McCabe; Cameron Williams; Caroline Crahan; Sarit Smolikove
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10.  Specialization of CDK1 and cyclin B paralog functions in a coenocystic mode of oogenic meiosis.

Authors:  Haiyang Feng; Eric M Thompson
Journal:  Cell Cycle       Date:  2018-07-23       Impact factor: 4.534

  10 in total

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