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

Hans I-Chen Harn, Sheng-Pei Wang, Yung-Chih Lai, Ben Van Handel, Ya-Chen Liang, Stephanie Tsai, Ina Maria Schiessl, Arijita Sarkar, Haibin Xi, Michael Hughes, Stefan Kaemmer, Ming-Jer Tang, Janos Peti-Peterdi, April D. Pyle, Thomas E. Woolley, Denis Evseenko, Ting-Xin Jiang and Cheng-Ming Chuong ()
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Hans I-Chen Harn: University of Southern California
Sheng-Pei Wang: University of Southern California
Yung-Chih Lai: China Medical University Hospital, China Medical University
Ben Van Handel: University of Southern California
Ya-Chen Liang: University of Southern California
Stephanie Tsai: University of Southern California
Ina Maria Schiessl: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California
Arijita Sarkar: University of Southern California
Haibin Xi: University of California Los Angeles
Michael Hughes: National Cheng Kung University
Stefan Kaemmer: Park Systems Inc.
Ming-Jer Tang: National Cheng Kung University
Janos Peti-Peterdi: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California
April D. Pyle: University of California Los Angeles
Thomas E. Woolley: Cardiff University
Denis Evseenko: University of Southern California
Ting-Xin Jiang: University of Southern California
Cheng-Ming Chuong: University of Southern California

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: 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 that 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.

Date: 2021
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DOI: 10.1038/s41467-021-22822-9

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