Neuroendocrine modulation sustains the C. elegans forward motor state

  1. Maria Lim  Is a corresponding author
  2. Jyothsna Chitturi
  3. Valeriya Laskova
  4. Jun Meng
  5. Daniel Findeis
  6. Anne Wiekenberg
  7. Ben Mulcahy
  8. Linjiao Luo
  9. Yan Li
  10. Yangning Lu
  11. Wesley Hung
  12. Yixin Qu
  13. Chiyip Ho
  14. Douglas Holmyard
  15. Ni Ji
  16. Rebecca D McWhirter
  17. Aravinthan DT Samuel
  18. David M Miller III
  19. Ralf Schnabel
  20. John A Calarco  Is a corresponding author
  21. Mei Zhen  Is a corresponding author
  1. Mount Sinai Hospital, Canada
  2. Technische Universität Braunschweig Carolo Wilhelmina, Germany
  3. Ministry of Education, China
  4. Harvard University, United States
  5. Vanderbilt University, United States

Abstract

Neuromodulators shape neural circuit dynamics. Combining electron microscopy, genetics, transcriptome profiling, calcium imaging, and optogenetics, we discovered a peptidergic neuron that modulates C. elegans motor circuit dynamics. The Six/SO-family homeobox transcription factor UNC-39 governs lineage-specific neurogenesis to give rise to a neuron RID. RID bears the anatomic hallmarks of a specialized endocrine neuron: it harbors near-exclusive dense core vesicles that cluster periodically along the axon, and expresses multiple neuropeptides, including the FMRF-amide-related FLP-14. RID activity increases during forward movement. Ablating RID reduces the sustainability of forward movement, a phenotype partially recapitulated by removing FLP-14. Optogenetic depolarization of RID prolongs forward movement, an effect reduced in the absence of FLP-14. Together, these results establish the role of a neuroendocrine cell RID in sustaining a specific behavioral state in C. elegans.

Article and author information

Author details

  1. Maria Lim

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    For correspondence
    maria.a.lim@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Jyothsna Chitturi

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Valeriya Laskova

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Jun Meng

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel Findeis

    Institut für Genetik, Technische Universität Braunschweig Carolo Wilhelmina, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Anne Wiekenberg

    Institut für Genetik, Technische Universität Braunschweig Carolo Wilhelmina, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Ben Mulcahy

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Linjiao Luo

    Key Laboratory of Modern Acoustics, Ministry of Education, Nanjing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Yan Li

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  10. Yangning Lu

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. Wesley Hung

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  12. Yixin Qu

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  13. Chiyip Ho

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  14. Douglas Holmyard

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  15. Ni Ji

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Rebecca D McWhirter

    Department of Cell and Developmental Biology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Aravinthan DT Samuel

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. David M Miller III

    Department of Cell and Developmental Biology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9048-873X
  19. Ralf Schnabel

    Institut für Genetik, Technische Universität Braunschweig Carolo Wilhelmina, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  20. John A Calarco

    FAS Center for Systems Biology, Harvard University, Cambridge, United States
    For correspondence
    jcalarco@fas.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
  21. Mei Zhen

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    For correspondence
    zhen@lunenfeld.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0086-9622

Funding

Canadian Institutes of Health Research (CIHR MOP to Mei Zhen)

  • Mei Zhen

National Institutes of Health (NIH award to John Calarco)

  • John A Calarco

National Institutes of Health (NIH award to Aravinthan Samuel)

  • Aravinthan DT Samuel

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

Reviewing Editor

  1. Eve Marder, Brandeis University, United States

Publication history

  1. Received: July 21, 2016
  2. Accepted: November 14, 2016
  3. Accepted Manuscript published: November 18, 2016 (version 1)
  4. Version of Record published: November 23, 2016 (version 2)
  5. Version of Record updated: January 19, 2017 (version 3)
  6. Version of Record updated: March 8, 2017 (version 4)

Copyright

© 2016, Lim 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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  1. Maria Lim
  2. Jyothsna Chitturi
  3. Valeriya Laskova
  4. Jun Meng
  5. Daniel Findeis
  6. Anne Wiekenberg
  7. Ben Mulcahy
  8. Linjiao Luo
  9. Yan Li
  10. Yangning Lu
  11. Wesley Hung
  12. Yixin Qu
  13. Chiyip Ho
  14. Douglas Holmyard
  15. Ni Ji
  16. Rebecca D McWhirter
  17. Aravinthan DT Samuel
  18. David M Miller III
  19. Ralf Schnabel
  20. John A Calarco
  21. Mei Zhen
(2016)
Neuroendocrine modulation sustains the C. elegans forward motor state
eLife 5:e19887.
https://doi.org/10.7554/eLife.19887

Further reading

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