Untwisting the Caenorhabditis elegans embryo

  1. Ryan Patrick Christensen  Is a corresponding author
  2. Alexandra Bokinsky
  3. Anthony Santella
  4. Yicong Wu
  5. Javier Marquina-Solis
  6. Min Guo
  7. Ismar Kovacevic
  8. Abhishek Kumar
  9. Peter W Winter
  10. Nicole Tashakkori
  11. Evan McCreedy
  12. Huafeng Liu
  13. Matthew McAuliffe
  14. William Mohler
  15. Daniel A Colon-Ramos
  16. Zhirong Bao
  17. Hari Shroff
  1. National Institutes of Health, United States
  2. Sloan-Kettering Institute, United States
  3. Yale University, United States
  4. Zhejiang University, China
  5. University of Connecticut Health Center, United States

Abstract

The nematode Caenorhabditis elegans possesses a simple embryonic nervous system comprising 222 neurons, a number small enough that the growth of each cell could be followed to provide a systems-level view of development. However, studies of single cell development have largely been conducted in fixed or pre-twitching live embryos, because of technical difficulties associated with embryo movement in late embryogenesis. We present open source untwisting and annotation software which allows the investigation of neurodevelopmental events in post-twitching embryos, and apply them to track the 3D positions of seam cells, neurons, and neurites in multiple elongating embryos. The detailed positional information we obtained enabled us to develop a composite model showing movement of these cells and neurites in an "average" worm embryo. The untwisting and cell tracking capability we demonstrate provides a foundation on which to catalog C. elegans neurodevelopment, allowing interrogation of developmental events in previously inaccessible periods of embryogenesis.

Article and author information

Author details

  1. Ryan Patrick Christensen

    National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
    For correspondence
    ryan.christensen@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexandra Bokinsky

    Center for Information Technology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Anthony Santella

    Developmental Biology Program, Sloan-Kettering Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yicong Wu

    National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Javier Marquina-Solis

    Program in Cellular Neuroscience, Neurodegeneration, and Repair, Department of Cell Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Min Guo

    State Key Laboratory of Modern Optical Instrumentation, College of Optical Science and Engineering, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Ismar Kovacevic

    Developmental Biology Program, Sloan-Kettering Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Abhishek Kumar

    Program in Cellular Neuroscience, Neurodegeneration, and Repair, Department of Cell Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Peter W Winter

    National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Nicole Tashakkori

    National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Evan McCreedy

    Center for Information Technology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Huafeng Liu

    State Key Laboratory of Modern Optical Instrumentation, College of Optical Science and Engineering, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  13. Matthew McAuliffe

    Center for Information Technology, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. William Mohler

    Department of Genetics and Developmental Biology, University of Connecticut Health Center, Farmington, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Daniel A Colon-Ramos

    Cell Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Zhirong Bao

    Developmental Biology Program, Sloan-Kettering Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Hari Shroff

    National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Oliver Hobert, Columbia University, United States

Version history

  1. Received: July 14, 2015
  2. Accepted: November 25, 2015
  3. Accepted Manuscript published: December 3, 2015 (version 1)
  4. Version of Record published: February 10, 2016 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Ryan Patrick Christensen
  2. Alexandra Bokinsky
  3. Anthony Santella
  4. Yicong Wu
  5. Javier Marquina-Solis
  6. Min Guo
  7. Ismar Kovacevic
  8. Abhishek Kumar
  9. Peter W Winter
  10. Nicole Tashakkori
  11. Evan McCreedy
  12. Huafeng Liu
  13. Matthew McAuliffe
  14. William Mohler
  15. Daniel A Colon-Ramos
  16. Zhirong Bao
  17. Hari Shroff
(2015)
Untwisting the Caenorhabditis elegans embryo
eLife 4:e10070.
https://doi.org/10.7554/eLife.10070

Share this article

https://doi.org/10.7554/eLife.10070

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