1. Cell Biology
  2. Developmental Biology

FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis

  1. Melissa Kelley
  2. John Yochem
  3. Michael Krieg
  4. Andrea Calixto
  5. Maxwell G Heiman
  6. Aleksandra Kuzmanov
  7. Vijaykumar Meli
  8. Martin Chalfie
  9. Miriam B Goodman
  10. Shai Shaham
  11. Alison Frand
  12. David S Fay  Is a corresponding author
  1. University of Wyoming, United States
  2. Stanford University, United States
  3. Columbia University, United States
  4. Boston Children's Hospital, United States
  5. University of California, United States
  6. Standford University, United States
  7. The Rockefeller University, United States
https://doi.org/10.7554/eLife.06565
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Cite this article
  1. Melissa Kelley
  2. John Yochem
  3. Michael Krieg
  4. Andrea Calixto
  5. Maxwell G Heiman
  6. Aleksandra Kuzmanov
  7. Vijaykumar Meli
  8. Martin Chalfie
  9. Miriam B Goodman
  10. Shai Shaham
  11. Alison Frand
  12. David S Fay
(2015)
FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
eLife 4:e06565.
https://doi.org/10.7554/eLife.06565
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Abstract

During development, biomechanical forces contour the body and provide shape to internal organs. Using genetic and molecular approaches in combination with a FRET-based tension sensor, we characterized a pulling force exerted by the elongating pharynx (foregut) on the anterior epidermis during C. elegans embryogenesis. Resistance of the epidermis to this force and to actomyosin-based circumferential constricting forces is mediated by FBN-1, a ZP domain protein related to vertebrate fibrillins. fbn-1 was required specifically within the epidermis and FBN-1 was expressed in epidermal cells and secreted to the apical surface as a putative component of the embryonic sheath. Tiling array studies indicated that fbn-1 mRNA processing requires the conserved alternative splicing factor MEC-8/RBPMS. The conserved SYM-3/FAM102A and SYM-4/WDR44 proteins, which are linked to protein trafficking, function as additional components of this network. Our studies demonstrate the importance of the apical extracellular matrix in preventing mechanical deformation of the epidermis during development.

Article and author information

Author details

  1. Melissa Kelley

    Department of Molecular Biology, University of Wyoming, Laramie, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. John Yochem

    Department of Molecular Biology, University of Wyoming, Laramie, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Michael Krieg

    Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Andrea Calixto

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Maxwell G Heiman

    Department of Genetics, Harvard Medical School, Boston Children's Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Aleksandra Kuzmanov

    Department of Molecular Biology, University of Wyoming, Laramie, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Vijaykumar Meli

    Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Martin Chalfie

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Miriam B Goodman

    Department of Molecular and Cellular Physiology, Standford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.

  10. Shai Shaham

    Laboratory of Developmental Genetics, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. Alison Frand

    Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.

  12. David S Fay

    Department of Molecular Biology, University of Wyoming, Laramie, United States
    For correspondence
    davidfay@uwyo.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Julie Ahringer, University of Cambridge, United Kingdom

Version history

  1. Received: January 19, 2015
  2. Accepted: March 20, 2015
  3. Accepted Manuscript published: March 23, 2015 (version 1)
  4. Version of Record published: April 14, 2015 (version 2)

Copyright

© 2015, Kelley 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. Melissa Kelley
  2. John Yochem
  3. Michael Krieg
  4. Andrea Calixto
  5. Maxwell G Heiman
  6. Aleksandra Kuzmanov
  7. Vijaykumar Meli
  8. Martin Chalfie
  9. Miriam B Goodman
  10. Shai Shaham
  11. Alison Frand
  12. David S Fay
(2015)
FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
eLife 4:e06565.
https://doi.org/10.7554/eLife.06565

Share this article

https://doi.org/10.7554/eLife.06565

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