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Symmetry breaking of tissue mechanics in wound induced hair follicle regeneration of laboratory and spiny mice

Harn, Hans I-Chen, Wang, Sheng-Pei, Lai, Yung-Chih, Handel, Ben Van, Liang, Ya-Chen, Tsai, Stephanie, Schiessl, Ina Maria, Sarkar, Arijita, Xi, Haibin, Hughes, Michael, Stefan, Kaemmer, Ming-Jer, Tang, Janos, Peti-Peterdi, April D., Pyle, Woolley, Thomas E., Evseenko, Denis, Jiang, Ting-Xin and Chuong, Cheng-Ming 2021. Symmetry breaking of tissue mechanics in wound induced hair follicle regeneration of laboratory and spiny mice. Nature Communications 12 , 2595. 10.1038/s41467-021-22822-9

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Abstract

Tissue regeneration is a process that recapitulates and restores organ structure and function. Although previous studies have demonstrated wound-induced hair neogenesis (WIHN) in laboratory mice (Mus), the regeneration is limited to the center of the wound unlike those observed in African spiny (Acomys) mice. Tissue mechanics have been implicated as an integral part of tissue morphogenesis. Here we use the WIHN model to investigate the mechanical and molecular responses of laboratory and African spiny mice, and report these models demonstrate opposing trends in spatiotemporal morphogenetic field formation with association to wound stiffness landscapes. Transcriptome analysis and K14-Cre-Twist1 transgenic mice show the Twist1 pathway acts as a mediator for both epidermal-dermal interactions and a competence factor for periodic patterning, differing from those used in development. We propose a Turing model based on tissue stiffness which supports a two-scale tissue mechanics process: (1) establishing a morphogenetic field within the wound bed (mm scale) and (2) symmetry breaking of the epidermis and forming periodically arranged hair primordia within the morphogenetic field (μm scale). Thus, we delineate distinct chemo-mechanical events in building a Turing morphogenesis-competent field during WIHN of laboratory and African spiny mice and identify its evo-devo advantages with perspectives for regenerative medicine.

Item Type: Article
Date Type: Publication
Status: Published
Schools: Mathematics
Subjects: Q Science > Q Science (General)
Q Science > QA Mathematics
Q Science > QR Microbiology
Publisher: Nature Research
ISSN: 2041-1723
Date of First Compliant Deposit: 22 April 2021
Date of Acceptance: 25 March 2021
Last Modified: 13 May 2021 12:13
URI: http://orca-mwe.cf.ac.uk/id/eprint/140217

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