Literature DB >> 35477753

Left-right symmetry of zebrafish embryos requires somite surface tension.

Sundar R Naganathan1, Marko Popović2,3,4, Andrew C Oates5.   

Abstract

The body axis of vertebrate embryos is periodically segmented into bilaterally symmetric pairs of somites1,2. The anteroposterior length of somites, their position and left-right symmetry are thought to be molecularly determined before somite morphogenesis3,4. Here we show that, in zebrafish embryos, initial somite anteroposterior lengths and positions are imprecise and, consequently, many somite pairs form left-right asymmetrically. Notably, these imprecisions are not left unchecked and we find that anteroposterior lengths adjust within an hour after somite formation, thereby increasing morphological symmetry. We find that anteroposterior length adjustments result entirely from changes in somite shape without change in somite volume, with changes in anteroposterior length being compensated by corresponding changes in mediolateral length. The anteroposterior adjustment mechanism is facilitated by somite surface tension, which we show by comparing in vivo experiments and in vitro single-somite explant cultures using a mechanical model. Length adjustment is inhibited by perturbation of molecules involved in surface tension, such as integrin and fibronectin. By contrast, the adjustment mechanism is unaffected by perturbations to the segmentation clock, therefore revealing a distinct process that influences morphological segment lengths. We propose that tissue surface tension provides a general mechanism to adjust shapes and ensure precision and symmetry of tissues in developing embryos.
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

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Year:  2022        PMID: 35477753     DOI: 10.1038/s41586-022-04646-9

Source DB:  PubMed          Journal:  Nature        ISSN: 0028-0836            Impact factor:   69.504


  40 in total

Review 1.  Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock.

Authors:  Andrew C Oates; Luis G Morelli; Saúl Ares
Journal:  Development       Date:  2012-02       Impact factor: 6.868

Review 2.  Top theories for the etiopathogenesis of adolescent idiopathic scoliosis.

Authors:  Wei Jun Wang; Hiu Yan Yeung; Winne Chiu-Wing Chu; Nelson Leung-Sang Tang; Kwong Man Lee; Yong Qiu; Richard Geoffrey Burwell; Jack Chun Yiu Cheng
Journal:  J Pediatr Orthop       Date:  2011 Jan-Feb       Impact factor: 2.324

3.  Scoliosis and developmental theory: adolescent idiopathic scoliosis.

Authors:  C J Goldberg; E E Fogarty; D P Moore; F E Dowling
Journal:  Spine (Phila Pa 1976)       Date:  1997-10-01       Impact factor: 3.468

Review 4.  Balancing segmentation and laterality during vertebrate development.

Authors:  Tim Brend; Scott A Holley
Journal:  Semin Cell Dev Biol       Date:  2008-11-25       Impact factor: 7.727

5.  Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis.

Authors:  I Palmeirim; D Henrique; D Ish-Horowicz; O Pourquié
Journal:  Cell       Date:  1997-11-28       Impact factor: 41.582

6.  A clock and wavefront model for control of the number of repeated structures during animal morphogenesis.

Authors:  J Cooke; E C Zeeman
Journal:  J Theor Biol       Date:  1976-05-21       Impact factor: 2.691

Review 7.  Patterning and mechanics of somite boundaries in zebrafish embryos.

Authors:  S R Naganathan; A C Oates
Journal:  Semin Cell Dev Biol       Date:  2020-05-19       Impact factor: 7.727

8.  Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos.

Authors:  Julien Vermot; Olivier Pourquié
Journal:  Nature       Date:  2005-05-12       Impact factor: 49.962

9.  Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo.

Authors:  Julien Vermot; Jabier Gallego Llamas; Valérie Fraulob; Karen Niederreither; Pierre Chambon; Pascal Dollé
Journal:  Science       Date:  2005-02-24       Impact factor: 47.728

Review 10.  Vertebrate segmentation: from cyclic gene networks to scoliosis.

Authors:  Olivier Pourquié
Journal:  Cell       Date:  2011-05-27       Impact factor: 41.582

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  2 in total

1.  Cell-Fibronectin Interactions and Actomyosin Contractility Regulate the Segmentation Clock and Spatio-Temporal Somite Cleft Formation during Chick Embryo Somitogenesis.

Authors:  Patrícia Gomes de Almeida; Pedro Rifes; Ana P Martins-Jesus; Gonçalo G Pinheiro; Raquel P Andrade; Sólveig Thorsteinsdóttir
Journal:  Cells       Date:  2022-06-22       Impact factor: 7.666

2.  A Dilp8-dependent time window ensures tissue size adjustment in Drosophila.

Authors:  D Blanco-Obregon; K El Marzkioui; F Brutscher; V Kapoor; L Valzania; D S Andersen; J Colombani; S Narasimha; D McCusker; P Léopold; L Boulan
Journal:  Nat Commun       Date:  2022-09-26       Impact factor: 17.694

  2 in total

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