FBN-1, a fibrillin-related protein, is required for resistance of the epidermis to mechanical deformation during C. elegans embryogenesis
Melissa Kelley,
John Yochem,
Michael Krieg,
Andrea Calixto,
Maxwell G Heiman,
Aleksandra Kuzmanov,
Vijaykumar Meli,
Martin Chalfie,
Miriam B Goodman,
Shai Shaham,
Alison Frand,
David S Fay
Affiliations
Melissa Kelley
Department of Molecular Biology, University of Wyoming, Laramie, United States
John Yochem
Department of Molecular Biology, University of Wyoming, Laramie, United States
Michael Krieg
Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States; Department of Chemical Engineering, Stanford University, Stanford, United States
Andrea Calixto
Department of Biological Sciences, Columbia University, New York, United States; Center for Genomic and Bioinformatics, Universidad Mayor, Santiago, Chile
Maxwell G Heiman
Department of Genetics, Harvard Medical School, Boston Children's Hospital, Boston, United States; Division of Genetics, Boston Children's Hospital, Boston, United States
Aleksandra Kuzmanov
Department of Molecular Biology, University of Wyoming, Laramie, United States
Vijaykumar Meli
Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, United States
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.
