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, Cheng Ming Chuong

Research output: Contribution to journalArticlepeer-review

1 Citation (Scopus)

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.

Original languageEnglish
Article number2595
JournalNature communications
Volume12
Issue number1
DOIs
Publication statusPublished - 2021 Dec

All Science Journal Classification (ASJC) codes

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

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