Literature DB >> 20875815

Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators.

Jessica R Harrell1, Bob Goldstein.   

Abstract

Understanding the links between developmental patterning mechanisms and force-producing cytoskeletal mechanisms is a central goal in studies of morphogenesis. Gastrulation is the first morphogenetic event in the development of many organisms. Gastrulation involves the internalization of surface cells, often driven by the contraction of actomyosin networks that are deployed with spatial precision-both in specific cells and in a polarized manner within each cell. These cytoskeletal mechanisms rely on different cell fate and cell polarity regulators in different organisms. Caenorhabditis elegans gastrulation presents an opportunity to examine the extent to which diverse mechanisms may be used by dozens of cells that are internalized at distinct times within a single organism. We identified 66 cells that are internalized in C. elegans gastrulation, many of which were not known previously to gastrulate. To gain mechanistic insights into how these cells internalize, we genetically manipulated cell fate, cell polarity and cytoskeletal regulators and determined the effects on cell internalization. We found that cells of distinct lineages depend on common actomyosin-based mechanisms to gastrulate, but different cell fate regulators, and, surprisingly, different cell polarity regulators. We conclude that diverse cell fate and cell polarity regulators control common mechanisms of morphogenesis in C. elegans. The results highlight the variety of developmental patterning mechanisms that can be associated with common cytoskeletal mechanisms in the morphogenesis of an animal embryo.
Copyright © 2010 Elsevier Inc. All rights reserved.

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Year:  2010        PMID: 20875815      PMCID: PMC3022094          DOI: 10.1016/j.ydbio.2010.09.012

Source DB:  PubMed          Journal:  Dev Biol        ISSN: 0012-1606            Impact factor:   3.582


  48 in total

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Journal:  Development       Date:  2003-01       Impact factor: 6.868

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Authors:  Saori L Haigo; Jeffrey D Hildebrand; Richard M Harland; John B Wallingford
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3.  C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation.

Authors:  Jeremy Nance; Edwin M Munro; James R Priess
Journal:  Development       Date:  2003-09-16       Impact factor: 6.868

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Journal:  Nat Cell Biol       Date:  2002-11       Impact factor: 28.824

5.  Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice.

Authors:  J D Hildebrand; P Soriano
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6.  Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner.

Authors:  Stephen L Rogers; Ursula Wiedemann; Udo Häcker; Chris Turck; Ronald D Vale
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Review 7.  Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase.

Authors:  Andrew P Somlyo; Avril V Somlyo
Journal:  Physiol Rev       Date:  2003-10       Impact factor: 37.312

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Authors:  L A Berkowitz; S Strome
Journal:  Development       Date:  2000-10       Impact factor: 6.868

Review 9.  The last common bilaterian ancestor.

Authors:  Douglas H Erwin; Eric H Davidson
Journal:  Development       Date:  2002-07       Impact factor: 6.868

10.  Cell polarity and gastrulation in C. elegans.

Authors:  Jeremy Nance; James R Priess
Journal:  Development       Date:  2002-01       Impact factor: 6.868

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  15 in total

Review 1.  Germ cell specification.

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Journal:  Adv Exp Med Biol       Date:  2013       Impact factor: 2.622

2.  Quantitative semi-automated analysis of morphogenesis with single-cell resolution in complex embryos.

Authors:  Claudiu A Giurumescu; Sukryool Kang; Thomas A Planchon; Eric Betzig; Joshua Bloomekatz; Deborah Yelon; Pamela Cosman; Andrew D Chisholm
Journal:  Development       Date:  2012-10-10       Impact factor: 6.868

Review 3.  Apical constriction: themes and variations on a cellular mechanism driving morphogenesis.

Authors:  Adam C Martin; Bob Goldstein
Journal:  Development       Date:  2014-05       Impact factor: 6.868

Review 4.  Caenorhabditis elegans Gastrulation: A Model for Understanding How Cells Polarize, Change Shape, and Journey Toward the Center of an Embryo.

Authors:  Bob Goldstein; Jeremy Nance
Journal:  Genetics       Date:  2020-02       Impact factor: 4.562

5.  Identifying Regulators of Morphogenesis Common to Vertebrate Neural Tube Closure and Caenorhabditis elegans Gastrulation.

Authors:  Jessica L Sullivan-Brown; Panna Tandon; Kim E Bird; Daniel J Dickinson; Sophia C Tintori; Jennifer K Heppert; Joy H Meserve; Kathryn P Trogden; Sara K Orlowski; Frank L Conlon; Bob Goldstein
Journal:  Genetics       Date:  2015-10-04       Impact factor: 4.562

6.  The RhoGEF protein Plekhg5 regulates apical constriction of bottle cells during gastrulation.

Authors:  Ivan K Popov; Heather J Ray; Paul Skoglund; Ray Keller; Chenbei Chang
Journal:  Development       Date:  2018-12-12       Impact factor: 6.868

7.  An E-cadherin-mediated hitchhiking mechanism for C. elegans germ cell internalization during gastrulation.

Authors:  Daisuke Chihara; Jeremy Nance
Journal:  Development       Date:  2012-06-06       Impact factor: 6.868

Review 8.  Basement Membranes in the Worm: A Dynamic Scaffolding that Instructs Cellular Behaviors and Shapes Tissues.

Authors:  Matthew R Clay; David R Sherwood
Journal:  Curr Top Membr       Date:  2015-09-12       Impact factor: 3.049

Review 9.  Epithelial morphogenesis, tubulogenesis and forces in organogenesis.

Authors:  Daniel D Shaye; Martha C Soto
Journal:  Curr Top Dev Biol       Date:  2021-02-08       Impact factor: 4.897

10.  Actomyosin-based self-organization of cell internalization during C. elegans gastrulation.

Authors:  Christian Pohl; Michael Tiongson; Julia L Moore; Anthony Santella; Zhirong Bao
Journal:  BMC Biol       Date:  2012-11-30       Impact factor: 7.431

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