Hierarchical patterning modes orchestrate hair follicle morphogenesis

  • Two theories address the origin of repeating patterns, such as hair follicles, limb digits, and intestinal villi, during development. The Turing reaction–diffusion system posits that interacting diffusible signals produced by static cells first define a prepattern that then induces cell rearrangements to produce an anatomical structure. The second theory, that of mesenchymal self-organisation, proposes that mobile cells can form periodic patterns of cell aggregates directly, without reference to any prepattern. Early hair follicle development is characterised by the rapid appearance of periodic arrangements of altered gene expression in the epidermis and prominent clustering of the adjacent dermal mesenchymal cells. We assess the contributions and interplay between reaction–diffusion and mesenchymal self-organisation processes in hair follicle patterning, identifying a network of fibroblast growth factor (FGF), wingless-related integration site (WNT), and bone morphogenetic protein (BMP) signalling interactions capable of spontaneously producing a periodic pattern. Using time-lapse imaging, we find that mesenchymal cell condensation at hair follicles is locally directed by an epidermal prepattern. However, imposing this prepattern’s condition of high FGF and low BMP activity across the entire skin reveals a latent dermal capacity to undergo spatially patterned self-organisation in the absence of epithelial direction. This mesenchymal self-organisation relies on restricted transforming growth factor (TGF) β signalling, which serves to drive chemotactic mesenchymal patterning when reaction–diffusion patterning is suppressed, but, in normal conditions, facilitates cell movement to locally prepatterned sources of FGF. This work illustrates a hierarchy of periodic patterning modes operating in organogenesis.
Metadaten
Author:James D. Glover, Kirsty L. Wells, Franziska Matthäus, Kevin J. Painter, William Ho, Jon Riddell, Jeanette A. Johansson, Matthew J. Ford, Colin A. B. Jahoda, Vaclav Klika, Richard L. Mort, Denis J. Headon
URN:urn:nbn:de:hebis:30:3-439919
DOI:https://doi.org/10.1371/journal.pbio.2002117
ISSN:1545-7885
ISSN:1544-9173
Pubmed Id:https://pubmed.ncbi.nlm.nih.gov/28700594
Parent Title (English):PLoS biology
Publisher:PLoS
Place of publication:Lawrence, KS
Contributor(s):Caroline Hill
Document Type:Article
Language:English
Date of Publication (online):2017/07/24
Date of first Publication:2017/07/11
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2017/07/24
Volume:15
Issue:(7): e2002117
Page Number:31
First Page:1
Last Page:31
Note:
Copyright: © 2017 Glover et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
HeBIS-PPN:421457252
Institutes:Biowissenschaften / Biowissenschaften
Wissenschaftliche Zentren und koordinierte Programme / Frankfurt Institute for Advanced Studies (FIAS)
Dewey Decimal Classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Sammlungen:Universitätspublikationen
Licence (German):License LogoCreative Commons - Namensnennung 4.0