Literature DB >> 31178400

Organization of Embryonic Morphogenesis via Mechanical Information.

Dipjyoti Das1, Dörthe Jülich1, Jamie Schwendinger-Schreck1, Emilie Guillon1, Andrew K Lawton1, Nicolas Dray1, Thierry Emonet2, Corey S O'Hern3, Mark D Shattuck4, Scott A Holley5.   

Abstract

Embryonic organizers establish gradients of diffusible signaling molecules to pattern the surrounding cells. Here, we elucidate an additional mechanism of embryonic organizers that is a secondary consequence of morphogen signaling. Using pharmacological and localized transgenic perturbations, 4D imaging of the zebrafish embryo, systematic analysis of cell motion, and computational modeling, we find that the vertebrate tail organizer orchestrates morphogenesis over distances beyond the range of morphogen signaling. The organizer regulates the rate and coherence of cell motion in the elongating embryo using mechanical information that is transmitted via relay between neighboring cells. This mechanism is similar to a pressure front in granular media and other jammed systems, but in the embryo the mechanical information emerges from self-propelled cell movement and not force transfer between cells. The propagation likely relies upon local biochemical signaling that affects cell contractility, cell adhesion, and/or cell polarity but is independent of transcription and translation.
Copyright © 2019 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  BMP; biomechanics; cell migration; computational modeling; embryonic organizer; eve1; morphogen; morphogenesis; systems biology; tail organizer

Mesh:

Substances:

Year:  2019        PMID: 31178400      PMCID: PMC6590525          DOI: 10.1016/j.devcel.2019.05.014

Source DB:  PubMed          Journal:  Dev Cell        ISSN: 1534-5807            Impact factor:   12.270


  67 in total

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Review 2.  Stem cells, signals and vertebrate body axis extension.

Authors:  Valerie Wilson; Isabel Olivera-Martinez; Kate G Storey
Journal:  Development       Date:  2009-05       Impact factor: 6.868

3.  BMP and non-canonical Wnt signaling are required for inhibition of secondary tail formation in zebrafish.

Authors:  Yi Yang; Chris Thorpe
Journal:  Development       Date:  2011-06       Impact factor: 6.868

4.  In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors.

Authors:  Jijun Hao; Joshua N Ho; Jana A Lewis; Kaleh A Karim; R Nathan Daniels; Patrick R Gentry; Corey R Hopkins; Craig W Lindsley; Charles C Hong
Journal:  ACS Chem Biol       Date:  2010-02-19       Impact factor: 5.100

5.  BMP signaling and spadetail regulate exit of muscle precursors from the zebrafish tailbud.

Authors:  Katelyn O'Neill; Chris Thorpe
Journal:  Dev Biol       Date:  2012-12-12       Impact factor: 3.582

6.  Tbx16 and Msgn1 are required to establish directional cell migration of zebrafish mesodermal progenitors.

Authors:  Alyssa J Manning; David Kimelman
Journal:  Dev Biol       Date:  2015-09-12       Impact factor: 3.582

7.  Widespread expression of the eve1 gene in zebrafish embryos affects the anterior-posterior axis pattern.

Authors:  O Barro; S Vriz; J S Joly; C Joly; H Condamine; H Boulekbache
Journal:  Dev Genet       Date:  1995

8.  Crosstalk between Fgf and Wnt signaling in the zebrafish tailbud.

Authors:  Michael J Stulberg; Aiping Lin; Hongyu Zhao; Scott A Holley
Journal:  Dev Biol       Date:  2012-07-14       Impact factor: 3.582

9.  Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains.

Authors:  Catherine A Wilson; Samantha K High; Braedan M McCluskey; Angel Amores; Yi-lin Yan; Tom A Titus; Jennifer L Anderson; Peter Batzel; Michael J Carvan; Manfred Schartl; John H Postlethwait
Journal:  Genetics       Date:  2014-09-18       Impact factor: 4.562

10.  Mechanical Coupling between Endoderm Invagination and Axis Extension in Drosophila.

Authors:  Claire M Lye; Guy B Blanchard; Huw W Naylor; Leila Muresan; Jan Huisken; Richard J Adams; Bénédicte Sanson
Journal:  PLoS Biol       Date:  2015-11-06       Impact factor: 8.029

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  9 in total

1.  Mechanical Coupling Coordinates the Co-elongation of Axial and Paraxial Tissues in Avian Embryos.

Authors:  Fengzhu Xiong; Wenzhe Ma; Bertrand Bénazéraf; L Mahadevan; Olivier Pourquié
Journal:  Dev Cell       Date:  2020-09-11       Impact factor: 12.270

2.  Mechanics as a Means of Information Propagation in Development.

Authors:  Miriam A Genuth; Scott A Holley
Journal:  Bioessays       Date:  2020-09-03       Impact factor: 4.345

Review 3.  Forced to communicate: Integration of mechanical and biochemical signaling in morphogenesis.

Authors:  Abigail Kindberg; Jimmy K Hu; Jeffrey O Bush
Journal:  Curr Opin Cell Biol       Date:  2020-06-20       Impact factor: 8.382

Review 4.  The unappreciated generative role of cell movements in pattern formation.

Authors:  Timothy Fulton; Berta Verd; Benjamin Steventon
Journal:  R Soc Open Sci       Date:  2022-04-27       Impact factor: 3.653

Review 5.  Mechanics of Development.

Authors:  Katharine Goodwin; Celeste M Nelson
Journal:  Dev Cell       Date:  2020-12-14       Impact factor: 12.270

6.  Shaping the zebrafish myotome by intertissue friction and active stress.

Authors:  S Tlili; J Yin; J-F Rupprecht; M A Mendieta-Serrano; G Weissbart; N Verma; X Teng; Y Toyama; J Prost; T E Saunders
Journal:  Proc Natl Acad Sci U S A       Date:  2019-11-26       Impact factor: 11.205

7.  Epithelial-Mesenchymal Transition Drives Three-Dimensional Morphogenesis in Mammalian Early Development.

Authors:  Galym Ismagulov; Sofiane Hamidi; Guojun Sheng
Journal:  Front Cell Dev Biol       Date:  2021-02-11

8.  Anterior expansion and posterior addition to the notochord mechanically coordinate zebrafish embryo axis elongation.

Authors:  Susannah B P McLaren; Benjamin J Steventon
Journal:  Development       Date:  2021-07-21       Impact factor: 6.868

9.  Hox13 genes are required for mesoderm formation and axis elongation during early zebrafish development.

Authors:  Zhi Ye; David Kimelman
Journal:  Development       Date:  2020-11-27       Impact factor: 6.862

  9 in total

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