Literature DB >> 28705989

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

Amy E Shyer1, Alan R Rodrigues2,3, Grant G Schroeder2, Elena Kassianidou4, Sanjay Kumar4, Richard M Harland2.   

Abstract

The spacing of hair in mammals and feathers in birds is one of the most apparent morphological features of the skin. This pattern arises when uniform fields of progenitor cells diversify their molecular fate while adopting higher-order structure. Using the nascent skin of the developing chicken embryo as a model system, we find that morphological and molecular symmetries are simultaneously broken by an emergent process of cellular self-organization. The key initiators of heterogeneity are dermal progenitors, which spontaneously aggregate through contractility-driven cellular pulling. Concurrently, this dermal cell aggregation triggers the mechanosensitive activation of β-catenin in adjacent epidermal cells, initiating the follicle gene expression program. Taken together, this mechanism provides a means of integrating mechanical and molecular perspectives of organ formation.
Copyright © 2017 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.

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Year:  2017        PMID: 28705989      PMCID: PMC5605277          DOI: 10.1126/science.aai7868

Source DB:  PubMed          Journal:  Science        ISSN: 0036-8075            Impact factor:   47.728


  23 in total

Review 1.  The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin.

Authors:  Jack Lilien; Janne Balsamo
Journal:  Curr Opin Cell Biol       Date:  2005-10       Impact factor: 8.382

2.  BMP2 and BMP7 play antagonistic roles in feather induction.

Authors:  Frederic Michon; Loïc Forest; Elodie Collomb; Jacques Demongeot; Danielle Dhouailly
Journal:  Development       Date:  2008-07-17       Impact factor: 6.868

Review 3.  Turing's next steps: the mechanochemical basis of morphogenesis.

Authors:  Jonathon Howard; Stephan W Grill; Justin S Bois
Journal:  Nat Rev Mol Cell Biol       Date:  2011-06       Impact factor: 94.444

4.  Mechanical induction of the tumorigenic β-catenin pathway by tumour growth pressure.

Authors:  María Elena Fernández-Sánchez; Sandrine Barbier; Joanne Whitehead; Gaëlle Béalle; Aude Michel; Heldmuth Latorre-Ossa; Colette Rey; Laura Fouassier; Audrey Claperon; Laura Brullé; Elodie Girard; Nicolas Servant; Thomas Rio-Frio; Hélène Marie; Sylviane Lesieur; Chantal Housset; Jean-Luc Gennisson; Mickaël Tanter; Christine Ménager; Silvia Fre; Sylvie Robine; Emmanuel Farge
Journal:  Nature       Date:  2015-05-11       Impact factor: 49.962

5.  Generation of biological pattern and form.

Authors:  J D Murray; G F Oster
Journal:  IMA J Math Appl Med Biol       Date:  1984

6.  Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase.

Authors:  Karen A Beningo; Kozue Hamao; Micah Dembo; Yu-Li Wang; Hiroshi Hosoya
Journal:  Arch Biochem Biophys       Date:  2006-10-11       Impact factor: 4.013

7.  N-terminal specific conjugation of extracellular matrix proteins to 2-pyridinecarboxaldehyde functionalized polyacrylamide hydrogels.

Authors:  Jessica P Lee; Elena Kassianidou; James I MacDonald; Matthew B Francis; Sanjay Kumar
Journal:  Biomaterials       Date:  2016-06-15       Impact factor: 12.479

8.  A self-organized biomechanical network drives shape changes during tissue morphogenesis.

Authors:  Akankshi Munjal; Jean-Marc Philippe; Edwin Munro; Thomas Lecuit
Journal:  Nature       Date:  2015-07-27       Impact factor: 49.962

9.  BMPs mediate lateral inhibition at successive stages in feather tract development.

Authors:  S Noramly; B A Morgan
Journal:  Development       Date:  1998-10       Impact factor: 6.868

10.  β-catenin tyrosine 654 phosphorylation increases Wnt signalling and intestinal tumorigenesis.

Authors:  Wendy van Veelen; Ngoc H Le; Werner Helvensteijn; Lau Blonden; Myrte Theeuwes; Elvira R M Bakker; Patrick F Franken; Léon van Gurp; Frits Meijlink; Martin A van der Valk; Ernst J Kuipers; Riccardo Fodde; Ron Smits
Journal:  Gut       Date:  2011-02-09       Impact factor: 23.059

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  63 in total

Review 1.  Physical control of tissue morphogenesis across scales.

Authors:  Georgina A Stooke-Vaughan; Otger Campàs
Journal:  Curr Opin Genet Dev       Date:  2018-11-01       Impact factor: 5.578

2.  Coupled cycling programs multicellular self-organization of neural progenitors.

Authors:  Saba Rezaei-Lotfi; Neil Hunter; Ramin M Farahani
Journal:  Cell Cycle       Date:  2019-07-09       Impact factor: 4.534

3.  Self-assembly of biological networks via adaptive patterning revealed by avian intradermal muscle network formation.

Authors:  Xiao-Shan Wu; Chao-Yuan Yeh; Hans I-Chen Harn; Ting-Xing Jiang; Ping Wu; Randall B Widelitz; Ruth E Baker; Cheng-Ming Chuong
Journal:  Proc Natl Acad Sci U S A       Date:  2019-05-09       Impact factor: 11.205

Review 4.  Programmed and self-organized flow of information during morphogenesis.

Authors:  Claudio Collinet; Thomas Lecuit
Journal:  Nat Rev Mol Cell Biol       Date:  2021-01-22       Impact factor: 94.444

5.  Mechanics of development.

Authors:  Niamh C Nowlan; Philippa Francis-West; Celeste Nelson
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-09-24       Impact factor: 6.237

6.  How cancer invasion takes shape.

Authors:  Karolina Punovuori; Sara A Wickström
Journal:  Nature       Date:  2020-09       Impact factor: 49.962

Review 7.  Embryonic Chicken (Gallus gallus domesticus) as a Model of Cardiac Biology and Development.

Authors:  José G Vilches-Moure
Journal:  Comp Med       Date:  2019-06-10       Impact factor: 0.982

8.  Optimal Contractile Forces for a Mesenchymal Engine.

Authors:  Dennis E Discher; Lawrence J Dooling
Journal:  Dev Cell       Date:  2017-08-21       Impact factor: 12.270

Review 9.  Emergence of evolutionary driving forces in pattern-forming microbial populations.

Authors:  Jona Kayser; Carl F Schreck; QinQin Yu; Matti Gralka; Oskar Hallatschek
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-05-26       Impact factor: 6.237

Review 10.  Mechanical forces direct stem cell behaviour in development and regeneration.

Authors:  Kyle H Vining; David J Mooney
Journal:  Nat Rev Mol Cell Biol       Date:  2017-11-08       Impact factor: 94.444

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