Literature DB >> 36215298

Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds.

Camille Curantz1,2,3, Richard Bailleul1,2,4, María Castro-Scherianz1, Magdalena Hidalgo1, Melina Durande5, François Graner5, Marie Manceau1.   

Abstract

Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling self-organized systems such that they achieve stable pattern outcomes remain unknown. Here, we described natural variation in the fidelity of self-organized arrays formed by feather follicle precursors in bird embryos. By surveying skin cells prior to and during tissue self-organization and performing species-specific ex vivo drug treatments and mechanical stress tests, we demonstrated that pattern fidelity depends on the initial amplitude of cell anisotropy in regions of the developing dermis competent to produce a pattern. Using live imaging, we showed that cell shape anisotropy is associated with a limited increase in cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which initial tissue properties ensure stability in self-organization and thus, reproducible pattern production.

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Year:  2022        PMID: 36215298      PMCID: PMC9584522          DOI: 10.1371/journal.pbio.3001807

Source DB:  PubMed          Journal:  PLoS Biol        ISSN: 1544-9173            Impact factor:   9.593


  43 in total

Review 1.  Pattern formation by local self-activation and lateral inhibition.

Authors:  H Meinhardt; A Gierer
Journal:  Bioessays       Date:  2000-08       Impact factor: 4.345

2.  WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism.

Authors:  Stefanie Sick; Stefan Reinker; Jens Timmer; Thomas Schlake
Journal:  Science       Date:  2006-11-02       Impact factor: 47.728

3.  Towards an integrated experimental-theoretical approach for assessing the mechanistic basis of hair and feather morphogenesis.

Authors:  K J Painter; G S Hunt; K L Wells; J A Johansson; D J Headon
Journal:  Interface Focus       Date:  2012-02-15       Impact factor: 3.906

Review 4.  Forces in tissue morphogenesis and patterning.

Authors:  Carl-Philipp Heisenberg; Yohanns Bellaïche
Journal:  Cell       Date:  2013-05-23       Impact factor: 41.582

Review 5.  Force generation, transmission, and integration during cell and tissue morphogenesis.

Authors:  Thomas Lecuit; Pierre-François Lenne; Edwin Munro
Journal:  Annu Rev Cell Dev Biol       Date:  2011-07-05       Impact factor: 13.827

6.  Inhibition of actin polymerization by latrunculin A.

Authors:  M Coué; S L Brenner; I Spector; E D Korn
Journal:  FEBS Lett       Date:  1987-03-23       Impact factor: 4.124

7.  Emergent cellular self-organization and mechanosensation initiate follicle pattern in the avian skin.

Authors:  Amy E Shyer; Alan R Rodrigues; Grant G Schroeder; Elena Kassianidou; Sanjay Kumar; Richard M Harland
Journal:  Science       Date:  2017-07-13       Impact factor: 47.728

Review 8.  Mechanical force sensing in tissues.

Authors:  Soline Chanet; Adam C Martin
Journal:  Prog Mol Biol Transl Sci       Date:  2014       Impact factor: 3.622

9.  A chemotaxis model of feather primordia pattern formation during avian development.

Authors:  Kevin J Painter; William Ho; Denis J Headon
Journal:  J Theor Biol       Date:  2017-10-31       Impact factor: 2.691

10.  Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate.

Authors:  Andrew D Economou; Atsushi Ohazama; Thantrira Porntaveetus; Paul T Sharpe; Shigeru Kondo; M Albert Basson; Amel Gritli-Linde; Martyn T Cobourne; Jeremy B A Green
Journal:  Nat Genet       Date:  2012-02-19       Impact factor: 38.330

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