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In Vivo Quantitative Imaging Provides Insights into Trunk Neural Crest Migration

Li, Yuwei and Vieceli, Felipe M. and Gonzalez, Walter G. and Li, Ang and Tang, Weiyi and Lois, Carlos and Bronner, Marianne E. (2019) In Vivo Quantitative Imaging Provides Insights into Trunk Neural Crest Migration. Cell Reports, 26 (6). pp. 1489-1500. ISSN 2211-1247. PMCID PMC6449054. http://resolver.caltech.edu/CaltechAUTHORS:20190205-105428612

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Abstract

Neural crest (NC) cells undergo extensive migrations during development. Here, we couple in vivo live imaging at high resolution with custom software tools to reveal dynamic migratory behavior in chick embryos. Trunk NC cells migrate as individuals with both stochastic and biased features as they move dorsoventrally to form peripheral ganglia. Their leading edge displays a prominent fan-shaped lamellipodium that reorients upon cell-cell contact. Computational analysis reveals that when the lamellipodium of one cell touches the body of another, the two cells undergo “contact attraction,” often moving together and then separating via a pulling force exerted by lamellipodium. Targeted optical manipulation shows that cell interactions coupled with cell density generate a long-range biased random walk behavior, such that cells move from high to low density. In contrast to chain migration noted at other axial levels, the results show that individual trunk NC cells navigate the complex environment without tight coordination between neighbors.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.celrep.2019.01.039DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6449054PubMed CentralArticle
ORCID:
AuthorORCID
Li, Yuwei0000-0001-7753-4869
Vieceli, Felipe M.0000-0001-5142-8224
Lois, Carlos0000-0002-7305-2317
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2019 The Author(s). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 10 October 2018, Revised 29 December 2018, Accepted 10 January 2019, Available online 5 February 2019. We thank Dr. Vikas Trivedi (EMBL) for critically reading the manuscript and the Caltech Biological Imaging Center for sharing equipment. W.G.G. was supported by the Della Martin Foundation, the American Heart Association, and the Burroughs Wellcome Fund. This project was supported by DE024157 and DE027568 (to M.E.B.).] Author Contributions: Y.L. and M.E.B. conceived of the project with consultation from F.M.V. Y.L. designed the experiments, performed the molecular cloning, virus preparation, live imaging, laser ablation, and cell spot and surface segmentation. F.M.V. performed viral injections and slice cultures and provided helpful suggestions on experimental design. Y.L. and F.M.V. performed the immunofluorescence. W.G.G. developed the software tools for cell-surface segmentation and performed the cell morphological analysis. A.L. performed the cell trajectory analysis. W.G.G. and A.L. performed the statistical analysis. W.T. provided help on slice cultures and improving the titers of virus. C.L. provided helpful discussion. Y.L. and M.E.B. wrote the manuscript with consultation from W.G.G, A.L., and F.M.V. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Della Martin FoundationUNSPECIFIED
American Heart AssociationUNSPECIFIED
Burroughs Wellcome FundUNSPECIFIED
NIHDE024157
NIHDE027568
Subject Keywords:trunk neural crest; individual cell migration; contact-attraction; quantitative imaging
PubMed Central ID:PMC6449054
Record Number:CaltechAUTHORS:20190205-105428612
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190205-105428612
Official Citation:Yuwei Li, Felipe M. Vieceli, Walter G. Gonzalez, Ang Li, Weiyi Tang, Carlos Lois, Marianne E. Bronner, In Vivo Quantitative Imaging Provides Insights into Trunk Neural Crest Migration, Cell Reports, Volume 26, Issue 6, 2019, Pages 1489-1500.e3, ISSN 2211-1247, https://doi.org/10.1016/j.celrep.2019.01.039. (http://www.sciencedirect.com/science/article/pii/S2211124719300579)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:92666
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:05 Feb 2019 19:00
Last Modified:03 Jun 2019 23:14

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