Literature DB >> 22675206

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

Daisuke Chihara1, Jeremy Nance.   

Abstract

Gastrulation movements place endodermal precursors, mesodermal precursors and primordial germ cells (PGCs) into the interior of the embryo. Somatic cell gastrulation movements are regulated by transcription factors that also control cell fate, coupling cell identity and position. By contrast, PGCs in many species are transcriptionally quiescent, suggesting that they might use alternative gastrulation strategies. Here, we show that C. elegans PGCs internalize by attaching to internal endodermal cells, which undergo morphogenetic movements that pull the PGCs into the embryo. We show that PGCs enrich HMR-1/E-cadherin at their surfaces to stick to endoderm. HMR-1 expression in PGCs is necessary and sufficient to ensure internalization, suggesting that HMR-1 can promote PGC-endoderm adhesion through a mechanism other than homotypic trans interactions between the two cell groups. Finally, we demonstrate that the hmr-1 3' untranslated region promotes increased HMR-1 translation in PGCs. Our findings reveal that quiescent PGCs employ a post-transcriptionally regulated hitchhiking mechanism to internalize during gastrulation, and demonstrate a morphogenetic role for the conserved association of PGCs with the endoderm.

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Year:  2012        PMID: 22675206      PMCID: PMC3383229          DOI: 10.1242/dev.079863

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


  61 in total

1.  Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains.

Authors:  K J Reese; M A Dunn; J A Waddle; G Seydoux
Journal:  Mol Cell       Date:  2000-08       Impact factor: 17.970

2.  Quantitative studies of germ plasm and germ cells during early embryogenesis of Xenopus laevis.

Authors:  P M Whitington; K E Dixon
Journal:  J Embryol Exp Morphol       Date:  1975-02

3.  An evolutionary conserved region in the vasa 3'UTR targets RNA translation to the germ cells in the zebrafish.

Authors:  Holger Knaut; Herbert Steinbeisser; Heinz Schwarz; Christiane Nüsslein-Volhard
Journal:  Curr Biol       Date:  2002-03-19       Impact factor: 10.834

4.  Creation of low-copy integrated transgenic lines in Caenorhabditis elegans.

Authors:  V Praitis; E Casey; D Collar; J Austin
Journal:  Genetics       Date:  2001-03       Impact factor: 4.562

5.  The C. elegans hmr-1 gene can encode a neuronal classic cadherin involved in the regulation of axon fasciculation.

Authors:  Ian D Broadbent; Jonathan Pettitt
Journal:  Curr Biol       Date:  2002-01-08       Impact factor: 10.834

6.  FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak.

Authors:  B Ciruna; J Rossant
Journal:  Dev Cell       Date:  2001-07       Impact factor: 12.270

7.  Genes required for axon pathfinding and extension in the C. elegans nerve ring.

Authors:  J A Zallen; S A Kirch; C I Bargmann
Journal:  Development       Date:  1999-08       Impact factor: 6.868

8.  Cell polarity and gastrulation in C. elegans.

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

9.  nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans.

Authors:  K Subramaniam; G Seydoux
Journal:  Development       Date:  1999-11       Impact factor: 6.868

10.  LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling.

Authors:  L Chen; B Ong; V Bennett
Journal:  J Cell Biol       Date:  2001-08-13       Impact factor: 10.539

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  30 in total

1.  Jeremy Nance: Charting gastrulation's gyrations.

Authors:  Kendall Powell
Journal:  J Cell Biol       Date:  2016-01-18       Impact factor: 10.539

2.  Repurposing an endogenous degradation system for rapid and targeted depletion of C. elegans proteins.

Authors:  Stephen T Armenti; Lauren L Lohmer; David R Sherwood; Jeremy Nance
Journal:  Development       Date:  2014-11-05       Impact factor: 6.868

Review 3.  Biting Off What Can Be Chewed: Trogocytosis in Health, Infection, and Disease.

Authors:  Akhila Bettadapur; Hannah W Miller; Katherine S Ralston
Journal:  Infect Immun       Date:  2020-06-22       Impact factor: 3.441

Review 4.  Cadherin complexity: recent insights into cadherin superfamily function in C. elegans.

Authors:  Timothy Loveless; Jeff Hardin
Journal:  Curr Opin Cell Biol       Date:  2012-07-19       Impact factor: 8.382

Review 5.  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

6.  Niche Cell Wrapping Ensures Primordial Germ Cell Quiescence and Protection from Intercellular Cannibalism.

Authors:  Daniel C McIntyre; Jeremy Nance
Journal:  Curr Biol       Date:  2020-01-30       Impact factor: 10.834

Review 7.  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

Review 8.  The Caenorhabditis elegans Transgenic Toolbox.

Authors:  Jeremy Nance; Christian Frøkjær-Jensen
Journal:  Genetics       Date:  2019-08       Impact factor: 4.562

Review 9.  Cadherins and their partners in the nematode worm Caenorhabditis elegans.

Authors:  Jeff Hardin; Allison Lynch; Timothy Loveless; Jonathan Pettitt
Journal:  Prog Mol Biol Transl Sci       Date:  2013       Impact factor: 3.622

10.  MRCK-1 Drives Apical Constriction in C. elegans by Linking Developmental Patterning to Force Generation.

Authors:  Daniel J Marston; Christopher D Higgins; Kimberly A Peters; Timothy D Cupp; Daniel J Dickinson; Ariel M Pani; Regan P Moore; Amanda H Cox; Daniel P Kiehart; Bob Goldstein
Journal:  Curr Biol       Date:  2016-07-21       Impact factor: 10.834

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