Calcium oscillations coordinate feather mesenchymal cell movement by SHH dependent modulation of gap junction networks

Ang Li, Jung-Hwa Cho, Brian Reid, Chun-Chih Tseng, Lian He, Peng Tan, Chao-Yuan Yeh, Ping Wu, Yuwei Li, Randall B. Widelitz, Yubin Zhou, Min Zhao, Robert H. Chow () and Cheng-Ming Chuong ()
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Ang Li: USC Keck School of Medicine
Jung-Hwa Cho: USC Keck School of Medicine
Brian Reid: UC Davis School of Medicine
Chun-Chih Tseng: USC Keck School of Medicine
Lian He: College of Medicine, Texas A&M University
Peng Tan: College of Medicine, Texas A&M University
Chao-Yuan Yeh: USC Keck School of Medicine
Ping Wu: USC Keck School of Medicine
Yuwei Li: California Institute of Technology
Randall B. Widelitz: USC Keck School of Medicine
Yubin Zhou: College of Medicine, Texas A&M University
Min Zhao: UC Davis School of Medicine
Robert H. Chow: USC Keck School of Medicine
Cheng-Ming Chuong: USC Keck School of Medicine

Nature Communications, 2018, vol. 9, issue 1, 1-15

Abstract: Abstract Collective cell migration mediates multiple tissue morphogenesis processes. Yet how multi-dimensional mesenchymal cell movements are coordinated remains mostly unknown. Here we report that coordinated mesenchymal cell migration during chicken feather elongation is accompanied by dynamic changes of bioelectric currents. Transcriptome profiling and functional assays implicate contributions from functional voltage-gated Ca2+ channels (VGCCs), Connexin-43 based gap junctions, and Ca2+ release activated Ca2+ (CRAC) channels. 4-Dimensional Ca2+ imaging reveals that the Sonic hedgehog-responsive mesenchymal cells display synchronized Ca2+ oscillations, which expand progressively in area during feather elongation. Inhibiting VGCCs, gap junctions, or Sonic hedgehog signaling alters the mesenchymal Ca2+ landscape, cell movement patterns and feather bud elongation. Ca2+ oscillations induced by cyclic activation of opto-cCRAC channels enhance feather bud elongation. Functional disruption experiments and promoter analysis implicate synergistic Hedgehog and WNT/β-Catenin signaling in activating Connexin-43 expression, establishing gap junction networks synchronizing the Ca2+ profile among cells, thereby coordinating cell movement patterns.

Date: 2018
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DOI: 10.1038/s41467-018-07661-5

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