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

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. ele...

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Autores principales: Kelley, Melissa, Yochem, John, Krieg, Michael, Calixto, Andrea, Heiman, Maxwell G, Kuzmanov, Aleksandra, Meli, Vijaykumar, Chalfie, Martin, Goodman, Miriam B, Shaham, Shai, Frand, Alison, Fay, David S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395870/
https://www.ncbi.nlm.nih.gov/pubmed/25798732
http://dx.doi.org/10.7554/eLife.06565
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author Kelley, Melissa
Yochem, John
Krieg, Michael
Calixto, Andrea
Heiman, Maxwell G
Kuzmanov, Aleksandra
Meli, Vijaykumar
Chalfie, Martin
Goodman, Miriam B
Shaham, Shai
Frand, Alison
Fay, David S
author_facet Kelley, Melissa
Yochem, John
Krieg, Michael
Calixto, Andrea
Heiman, Maxwell G
Kuzmanov, Aleksandra
Meli, Vijaykumar
Chalfie, Martin
Goodman, Miriam B
Shaham, Shai
Frand, Alison
Fay, David S
author_sort Kelley, Melissa
collection PubMed
description 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. DOI: http://dx.doi.org/10.7554/eLife.06565.001
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spelling pubmed-43958702015-04-14 FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis Kelley, Melissa Yochem, John Krieg, Michael Calixto, Andrea Heiman, Maxwell G Kuzmanov, Aleksandra Meli, Vijaykumar Chalfie, Martin Goodman, Miriam B Shaham, Shai Frand, Alison Fay, David S eLife Cell Biology 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. DOI: http://dx.doi.org/10.7554/eLife.06565.001 eLife Sciences Publications, Ltd 2015-03-23 /pmc/articles/PMC4395870/ /pubmed/25798732 http://dx.doi.org/10.7554/eLife.06565 Text en © 2015, Kelley et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Kelley, Melissa
Yochem, John
Krieg, Michael
Calixto, Andrea
Heiman, Maxwell G
Kuzmanov, Aleksandra
Meli, Vijaykumar
Chalfie, Martin
Goodman, Miriam B
Shaham, Shai
Frand, Alison
Fay, David S
FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title_full FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title_fullStr FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title_full_unstemmed FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title_short FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
title_sort fbn-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during c. elegans embryogenesis
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4395870/
https://www.ncbi.nlm.nih.gov/pubmed/25798732
http://dx.doi.org/10.7554/eLife.06565
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