TIAM-1/GEF can shape somatosensory dendrites independently of its GEF activity by regulating F-actin localization

Abstract

Dendritic arbors are a crucial for nervous system assembly, but the intracellular mechanisms that govern their assembly remain incompletely understood. Here we show that the dendrites of PVD neurons in Caenorhabditis elegans are patterned by distinct pathways downstream of the DMA-1 leucine rich transmembrane (LRR-TM) receptor. DMA-1/LRR-TM interacts through a PDZ ligand motif with the guanine nucleotide exchange factor TIAM-1/GEF in a complex with act-4/Actin to pattern higher order 4º dendrite branches by localizing F-actin to the distal ends of developing dendrites. Surprisingly, TIAM-1/GEF appears to function independently of Rac1 guanine nucleotide exchange factor activity. A partially redundant pathway, dependent on HPO-30/Claudin, regulates formation of 2º and 3º branches, possibly by regulating membrane localization and trafficking of DMA-1/LRR-TM. Collectively, our experiments suggest that HPO-30/Claudin localizes the DMA-1/LRR-TM receptor on PVD dendrites, which in turn can control dendrite patterning by directly modulating F-actin dynamics through TIAM-1/GEF.

Data availability

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

Article and author information

Author details

  1. Leo TH Tang

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Carlos A Diaz-Balzac

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4723-1282
  3. Maisha Rahman

    Dominick P Purpura Department of Neuroscience, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nelson J Ramirez-Suarez

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7394-860X
  5. Yehuda Salzberg

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Maria I Lázaro-Peña

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Hannes E Bülow

    Department of Genetics, Albert Einstein College of Medicine, New York, United States
    For correspondence
    hannes.buelow@einstein.yu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6271-0572

Funding

National Institute of Neurological Disorders and Stroke (R21NS081505)

  • Hannes E Bülow

National Institute of General Medical Sciences (T32GM007288)

  • Carlos A Diaz-Balzac

Eunice Kennedy Shriver National Institute of Child Health and Human Development (F31HD066967)

  • Carlos A Diaz-Balzac

Fulbright-Colciencias

  • Nelson J Ramirez-Suarez

Irma T Hirschl/Monique Weill-Caulier

  • Hannes E Bülow

National Institute of Neurological Disorders and Stroke (F31NS100370)

  • Maisha Rahman

National Institute of General Medical Sciences (T32GM07491)

  • Maria I Lázaro-Peña

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

Reviewing Editor

  1. Shai Shaham, The Rockefeller University, United States

Version history

  1. Received: June 5, 2018
  2. Accepted: January 28, 2019
  3. Accepted Manuscript published: January 29, 2019 (version 1)
  4. Version of Record published: February 11, 2019 (version 2)

Copyright

© 2019, Tang 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. Leo TH Tang
  2. Carlos A Diaz-Balzac
  3. Maisha Rahman
  4. Nelson J Ramirez-Suarez
  5. Yehuda Salzberg
  6. Maria I Lázaro-Peña
  7. Hannes E Bülow
(2019)
TIAM-1/GEF can shape somatosensory dendrites independently of its GEF activity by regulating F-actin localization
eLife 8:e38949.
https://doi.org/10.7554/eLife.38949

Share this article

https://doi.org/10.7554/eLife.38949

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