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C. elegans neurons have functional dendritic spines

  1. Andrea Cuentas-Condori
  2. Ben Mulcahy
  3. Siwei He
  4. Sierra Palumbos
  5. Mei Zhen
  6. David M Miller  Is a corresponding author
  1. Vanderbilt University, United States
  2. University of Toronto, Canada
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Cite this article as: eLife 2019;8:e47918 doi: 10.7554/eLife.47918

Abstract

Dendritic spines are specialized postsynaptic structures that transduce presynaptic signals, are regulated by neural activity and correlated with learning and memory. Most studies of spine function have focused on the mammalian nervous system. However, spine-like protrusions have been reported in C. elegans (Philbrook et al. 2018), suggesting that the experimental advantages of smaller model organisms could be exploited to study the biology of dendritic spines. Here, we used super-resolution microscopy, electron microscopy, live-cell imaging and genetics to show that C. elegans motor neurons have functional dendritic spines that: (1) are structurally defined by a dynamic actin cytoskeleton; (2) appose presynaptic dense projections; (3) localize ER and ribosomes; (4) display calcium transients triggered by presynaptic activity and propagated by internal Ca++ stores; (5) respond to activity-dependent signals that regulate spine density. These studies provide a solid foundation for a new experimental paradigm that exploits the power of C. elegans genetics and live-cell imaging for fundamental studies of dendritic spine morphogenesis and function.

Article and author information

Author details

  1. Andrea Cuentas-Condori

    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:" 0000-0002-4847-0031
  2. Ben Mulcahy

    Lunenfeld-Tanenbaum Research Institute, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3336-245X
  3. Siwei He

    Neuroscience Program, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Sierra Palumbos

    Neuroscience Program, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mei Zhen

    Lunenfeld-Tanenbaum Research Institute, University of Toronto, Toronto, Canada
    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
  6. David M Miller

    Department of Cell and Developmental Biology, Vanderbilt University, Nashville, United States
    For correspondence
    david.miller@vanderbilt.edu
    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

Funding

National Institute of Neurological Disorders and Stroke (R01NS081259)

  • David M Miller

National Institute of Neurological Disorders and Stroke (R01NS106951)

  • David M Miller

American Heart Association (18PRE33960581)

  • Andrea Cuentas-Condori

National Science Foundation (DGE:1445197)

  • Sierra Palumbos

Canadian Institutes of Health Research (FS154274)

  • Mei Zhen

American Heart Association (19PRE34380582)

  • Sierra Palumbos

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

Reviewing Editor

  1. Kang Shen, Howard Hughes Medical Institute, Stanford University, United States

Publication history

  1. Received: April 24, 2019
  2. Accepted: October 3, 2019
  3. Accepted Manuscript published: October 4, 2019 (version 1)
  4. Version of Record published: October 21, 2019 (version 2)

Copyright

© 2019, Cuentas-Condori 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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