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Published online 19 May 2003. doi:10.1083/jcb.200302151
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© The Rockefeller University Press, 0021-9525/2003/5/757 $5.00
The Journal of Cell Biology, Volume 161, Number 4, 757-768

Article

 The Caenorhabditis elegans vab-10 spectraplakin isoforms protect the epidermis against internal and external forces

Julia M. Bosher1, Bum-Soo Hahn1, Renaud Legouis1, Satis Sookhareea1, Robby M. Weimer2, Anne Gansmuller1, Andrew D. Chisholm3, Ann M. Rose4, Jean-Louis Bessereau2 and Michel Labouesse1

1 Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), CNRS/INSERM/ULP, BP10142, Illkirch Cedex F-67404, France
2 Ecole Normale Supérieure de Paris, INSERM U 497, 75005 Paris, France
3 Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Cruz, CA 95064
4 Department of Medical Genetics, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z3

Address correspondence to Michel Labouesse, IGBMC, CNRS/INSERM/ULP, BP10142, CU de Strasbourg, Illkirch Cedex F-67404, France. Tel.: (33) 3-88-65-33-93. Fax: (33) 3-88-65-32-01. E-mail: lmichel{at}igbmc.u-strasbg.fr

Morphogenesis of the Caenorhabditis elegans embryo is driven by actin microfilaments in the epidermis and by sarcomeres in body wall muscles. Both tissues are mechanically coupled, most likely through specialized attachment structures called fibrous organelles (FOs) that connect muscles to the cuticle across the epidermis. Here, we report the identification of new mutations in a gene known as vab-10, which lead to severe morphogenesis defects, and show that vab-10 corresponds to the C. elegans spectraplakin locus. Our analysis of vab-10 reveals novel insights into the role of this plakin subfamily. vab-10 generates isoforms related either to plectin (termed VAB-10A) or to microtubule actin cross-linking factor plakins (termed VAB-10B). Using specific antibodies and mutations, we show that VAB-10A and VAB-10B have distinct distributions and functions in the epidermis. Loss of VAB-10A impairs the integrity of FOs, leading to epidermal detachment from the cuticle and muscles, hence demonstrating that FOs are functionally and molecularly related to hemidesmosomes. We suggest that this isoform protects against forces external to the epidermis. In contrast, lack of VAB-10B leads to increased epidermal thickness during embryonic morphogenesis when epidermal cells change shape. We suggest that this isoform protects cells against tension that builds up within the epidermis.

Key Words: plakin; cytoskeleton; hemidesmosome; cell adhesion; morphogenesis

J.M. Bosher, B.-S. Hahn, and R. Legouis contributed equally to this paper.

The online version of this article includes supplemental material.

B.-S. Hahn's present address is National Institute of Agricultural Biotechnology, Metabolic Engineering, Division 225, Seodun-Dong, Suwon, 441-707, South Korea.

R. Legouis' present address is CNRS-CGM, Avenue de la Terrasse, 91190 Gif-sur-Yvette, France.

* Abbreviations used in this paper: ABD, actin-binding domain; BPAG, bullous pemphigoid antigen; FO, fibrous organelle; GAR, growth-arrest protein 2–related homology; IF, intermediate filament; MCAF, microtubule actin cross-linking factor; MF, microfilament; MT, microtubule; RNAi, RNA interference.


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