1. Cell Biology
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The Nesprin-1/-2 ortholog ANC-1 regulates organelle positioning in C. elegans independently from its KASH or actin-binding domains

  1. Hongyan Hao
  2. Shilpi Kalra
  3. Laura E Jameson
  4. Leslie A Guerrero
  5. Natalie E Cain
  6. Jessica Bolivar
  7. Daniel A Starr  Is a corresponding author
  1. University of California, Davis, United States
Research Article
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Cite this article as: eLife 2021;10:e61069 doi: 10.7554/eLife.61069

Abstract

KASH proteins in the outer nuclear membrane comprise the cytoplasmic half of LINC complexes that connect nuclei to the cytoskeleton. Caenorhabditis elegans ANC-1, an ortholog of Nesprin-1/2, contains actin-binding and KASH domains at opposite ends of a long spectrin-like region. Deletion of either the KASH or calponin homology (CH) domains does not completely disrupt nuclear positioning, suggesting neither KASH nor CH domains are essential. Deletions in the spectrin-like region of ANC-1 led to significant defects, but only recapitulated the null phenotype in combination with mutations in the trans-membrane span. In anc-1 mutants, the ER, mitochondria, and lipid droplets were unanchored, moving throughout the cytoplasm. The data presented here support a cytoplasmic integrity model where ANC-1 localizes to the ER membrane and extends into the cytoplasm to position nuclei, ER, mitochondria, and likely other organelles in place.

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The list of strains generated is detailed in Table 1. All data points are displayed in the histograms in the figures.

Article and author information

Author details

  1. Hongyan Hao

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Shilpi Kalra

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Laura E Jameson

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Leslie A Guerrero

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Natalie E Cain

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1391-404X
  6. Jessica Bolivar

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Daniel A Starr

    Molecular and Cellular Biology, University of California, Davis, Davis, United States
    For correspondence
    dastarr@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7339-6606

Funding

National Institutes of Health (R01GM073874)

  • Daniel A Starr

National Institutes of Health (R35GM134859)

  • Daniel A Starr

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

Reviewing Editor

  1. Maddy Parsons, King's College London, United Kingdom

Publication history

  1. Received: July 14, 2020
  2. Accepted: April 11, 2021
  3. Accepted Manuscript published: April 16, 2021 (version 1)

Copyright

© 2021, Hao 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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