A multicellular rosette-mediated collective dendrite extension

  1. Li Fan
  2. Ismar Kovacevic
  3. Maxwell G Heiman
  4. Zhirong Bao  Is a corresponding author
  1. Sloan-Kettering Institute, United States
  2. Boston Children's Hospital, United States

Abstract

Coordination of neurite morphogenesis with surrounding tissues is crucial to the establishment of neural circuits, but the underlying cellular and molecular mechanisms remain poorly understood. We show that neurons in a C. elegans sensory organ, called the amphid, undergo a collective dendrite extension to form the sensory nerve. The amphid neurons first assemble into a multicellular rosette. The vertex of the rosette, which becomes the dendrite tips, is attached to the anteriorly migrating epidermis and carried to the sensory depression, extruding the dendrites away from the neuronal cell bodies. Multiple adhesion molecules including DYF-7, SAX-7, HMR-1 and DLG-1 function redundantly in rosette-to-epidermis attachment. PAR-6 is localized to the rosette vertex and dendrite tips, and promotes DYF-7 localization and dendrite extension. Our results suggest a collective mechanism of neurite extension that is distinct from the classical pioneer-follower model and highlight the role of mechanical cues from surrounding tissues in shaping neurites.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Li Fan

    Developmental Biology, Sloan-Kettering Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ismar Kovacevic

    Developmental Biology Program, Sloan-Kettering Institute, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Maxwell G Heiman

    Division of Genetics and Genomics, Boston Children's Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2557-6490
  4. Zhirong Bao

    Developmental Biology Program, Sloan-Kettering Institute, New York, United States
    For correspondence
    baoz@mskcc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2201-2745

Funding

National Institutes of Health (R01 GM097576)

  • Zhirong Bao

National Institutes of Health (R24 OD016474)

  • Zhirong Bao

National Institutes of Health (R01 GM108754)

  • Maxwell G Heiman

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

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Publication history

  1. Received: May 3, 2018
  2. Accepted: February 14, 2019
  3. Accepted Manuscript published: February 15, 2019 (version 1)
  4. Version of Record published: March 5, 2019 (version 2)

Copyright

© 2019, Fan 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. Li Fan
  2. Ismar Kovacevic
  3. Maxwell G Heiman
  4. Zhirong Bao
(2019)
A multicellular rosette-mediated collective dendrite extension
eLife 8:e38065.
https://doi.org/10.7554/eLife.38065

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