Inhibition of gap junctions stimulates Turing-type periodic feather pattern formation during chick skin development

Tseng, Chun-Chih, Woolley, Thomas ORCID: https://orcid.org/0000-0001-6225-5365, Jiang, Ting-Xin, Wu, Ping, Maini, Philip, Widelitz, Randall and Chuong, Cheng-Ming 2024. Inhibition of gap junctions stimulates Turing-type periodic feather pattern formation during chick skin development. PLoS Biology

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Abstract

Periodic patterning requires coordinated cell-cell interactions at the tissue level. Turing showed, using mathematical modeling, how spatial patterns could arise from the reactions of a diffusive activator-inhibitor pair in an initially homogenous two-dimensional field. Most activators and inhibitors studied in biological systems are proteins, and the roles of cell-cell interaction, ions, bioelectricity, etc. are only now being identified. Gap junctions (GJs) mediate direct exchanges of ions or small molecules between cells, enabling rapid long-distance communications in a cell collective. They are therefore good candidates for propagating non-protein-based patterning signals that may act according to the Turing principles. Here, we explore the possible roles of GJs in Turing-type patterning using feather pattern formation as a model. We found seven of the twelve investigated GJ isoforms are highly dynamically expressed in the developing chicken skin. In ovo functional perturbations of the GJ isoform, connexin 30, by siRNA and the dominant-negative mutant applied before placode development led to disrupted primary feather bud formation. Interestingly, inhibition of gap junctional intercellular communication (GJIC) in the ex vivo skin explant culture allowed the sequential emergence of new feather buds at specific spatial locations relative to the existing primary buds. The results suggest that GJIC may facilitate the propagation of long-distance inhibitory signals. Thus, the removal of GJ activity would enable the emergence of new feather buds if the local environment were competent and the threshold to form buds was reached. We propose Turing-based computational simulations that can predict the sequential appearance of these ectopic buds. Our models demonstrate how a Turing activator-inhibitor system can continue to generate patterns in the competent morphogenetic field when the level of intercellular communication at the tissue scale is modulated.

Item Type:	Article
Status:	In Press
Schools:	Mathematics
Subjects:	Q Science > Q Science (General) Q Science > QA Mathematics Q Science > QR Microbiology
Publisher:	Public Library of Science
ISSN:	1544-9173
Date of First Compliant Deposit:	2 April 2024
Date of Acceptance:	23 March 2024
Last Modified:	21 Jun 2024 19:23
URI:	https://orca.cardiff.ac.uk/id/eprint/167641

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