1. Cell Biology
  2. Developmental Biology
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Single-cell transcriptome analysis of avian neural crest migration reveals signatures of invasion and molecular transitions

  1. Jason A Morrison
  2. Rebecca McLennan
  3. Lauren A Wolfe
  4. Madelaine M Gogol
  5. Samuel Meier
  6. Mary C McKinney
  7. Jessica M Teddy
  8. Laura Holmes
  9. Craig L Semerad
  10. Andrew C Box
  11. Hua Li
  12. Kathryn E Hall
  13. Anoja G Perera
  14. Paul M Kulesa  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
  2. University of Nebraska Medical Center, United States
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Cite this article as: eLife 2017;6:e28415 doi: 10.7554/eLife.28415

Abstract

Neural crest cells migrate throughout the embryo, but how cells move in a directed and collective manner has remained unclear. Here, we perform the first single-cell transcriptome analysis of cranial neural crest cell migration at three progressive stages in chick and identify and establish hierarchical relationships between cell position and time-specific transcriptional signatures. We determine a novel transcriptional signature of the most invasive neural crest Trailblazer cells that is consistent during migration and enriched for approximately 900 genes. Knockdown of several Trailblazer genes shows significant but modest changes to total distance migrated. However, in vivo expression analysis by RNAscope and immunohistochemistry reveals some salt and pepper patterns that include strong individual Trailblazer gene expression in cells within other subregions of the migratory stream. These data provide new insights into the molecular diversity and dynamics within a neural crest cell migratory stream that underlie complex directed and collective cell behaviors.

Article and author information

Author details

  1. Jason A Morrison

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebecca McLennan

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Lauren A Wolfe

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Madelaine M Gogol

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8738-0995
  5. Samuel Meier

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mary C McKinney

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jessica M Teddy

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Laura Holmes

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Craig L Semerad

    University of Nebraska Medical Center, Omaha, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Andrew C Box

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Hua Li

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Kathryn E Hall

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Anoja G Perera

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Paul M Kulesa

    Stowers Institute for Medical Research, Kansas City, United States
    For correspondence
    pmk@stowers.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6354-9904

Funding

Stowers Institute for Medical Research

  • Paul M Kulesa

National Institute of Neurological Disorders and Stroke (R21NS092001)

  • Paul M Kulesa

The funders had no role in data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were performed according to institutional (IBC-2003-23-pmk) and federal ethical standards.

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Publication history

  1. Received: May 5, 2017
  2. Accepted: December 2, 2017
  3. Accepted Manuscript published: December 4, 2017 (version 1)
  4. Version of Record published: December 13, 2017 (version 2)

Copyright

© 2017, Morrison et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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