Visualizing mesoderm and neural crest cell dynamics during chick head morphogenesis

Mary Cathleen McKinney, Rebecca McLennan, Rasa Giniunaite, Ruth E. Baker, Philip K. Maini, Hans G. Othmer, Paul M. Kulesa

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Vertebrate head morphogenesis involves carefully-orchestrated tissue growth and cell movements of the mesoderm and neural crest to form the distinct craniofacial pattern. To better understand structural birth defects, it is important that we characterize the dynamics of these processes and learn how they rely on each other. Here we examine this question during chick head morphogenesis using time-lapse imaging, computational modeling, and experiments. We find that head mesodermal cells in culture move in random directions as individuals and move faster in the presence of neural crest cells. In vivo, mesodermal cells migrate in a directed manner and maintain neighbor relationships; neural crest cells travel through the mesoderm at a faster speed. The mesoderm grows with a non-uniform spatio-temporal profile determined by BrdU labeling during the period of faster and more-directed neural crest collective migration through this domain. We use computer simulations to probe the robustness of neural crest stream formation by varying the spatio-temporal growth profile of the mesoderm. We follow this with experimental manipulations that either stop mesoderm growth or prevent neural crest migration and observe changes in the non-manipulated cell population, implying a dynamic feedback between tissue growth and neural crest cell signaling to confer robustness to the system. Overall, we present a novel descriptive analysis of mesoderm and neural crest cell dynamics that reveals the coordination and co-dependence of these two cell populations during head morphogenesis.

Original languageEnglish (US)
Pages (from-to)184-196
Number of pages13
JournalDevelopmental Biology
Volume461
Issue number2
DOIs
StatePublished - May 15 2020

Bibliographical note

Funding Information:
This work was supported by the kind funding of The Stowers Institute for Medical Research. R.E.B. is a Royal Society Wolfson Research Merit Award holder. H.G.O. is supported by National Institutes of Health award RO1GM029123. R.G. gratefully acknowledges funding from the Engineering and Physical Sciences Research Council (EP/G03706X/1).PMK would like to acknowledge the kind and generous funding from the Stowers Institute for Medical Research. We would also like to thank David Huss, Rusty Lansford, and the Translational Imaging Center at the University of Southern California for use of the transgenic quail. In addition, we thank Dave Lei and Ashley Young for contributions to imaging and image analysis as part of the Stowers Summer Scholars Program.

Funding Information:
This work was supported by the kind funding of The Stowers Institute for Medical Research . R.E.B. is a Royal Society Wolfson Research Merit Award holder. H.G.O. is supported by National Institutes of Health award RO1GM029123 . R.G. gratefully acknowledges funding from the Engineering and Physical Sciences Research Council ( EP/G03706X/1 ).

Publisher Copyright:
© 2020 Elsevier Inc.

Keywords

  • Avian
  • Computer modeling
  • Mesoderm
  • Neural crest
  • Time-lapse
  • Tissue growth

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