The role of actin filaments in patterning the Caenorhabditis elegans cuticle

Nematodes are covered by a cuticle with a prominent pattern of circumferentially oriented, parallel furrows. We report here that the pattern of furrows on the first larval cuticle of Caenorhabditis elegans, which is secreted during embryogenesis, is coincident with a pattern of submembranous actin filament bundles in the epithelial cells that secrete the cuticle. We propose that the pattern of cortical actin filaments biases the growth of the epithelial cell membranes, creating a furrowed surface template for deposition of the first cuticle layer. This layer then detaches from the epithelial cell surface as additional, nonpatterned components of the cuticle are secreted. Furrows are present on the surfaces of each of the four larval cuticles in C. elegans and on the adult cuticle. We show that similar ordered arrays of actin filaments appear during each of the postembryonic molts when new cuticles are synthesized. Our analysis suggests that conditions or mutations that affect the pattern of cuticle furrows might cause primary defects in the cytoskeletal organization of the epithelial cells that secrete the cuticle.