Nematodes are covered by a cuticle with a prominent pattern of circumf
erentially oriented, parallel furrows. We report here that the pattern
of furrows on the first larval cuticle of Caenorhabditis elegans, whi
ch is secreted during embryogenesis, is coincident with a pattern of s
ubmembranous actin filament bundles in the epithelial cells that secre
te the cuticle. We propose that the pattern of cortical actin filament
s biases the growth of the epithelial cell membranes, creating a furro
wed surface template for deposition of the first cuticle layer. This l
ayer then detaches from the epithelial cell surface as additional, non
patterned 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 fil
aments appear during each of the postembryonic molts when new cuticles
are synthesized. Our analysis suggests that conditions or mutations t
hat affect the pattern of cuticle furrows might cause primary defects
in the cytoskeletal organization of the epithelial cells that secrete
the cuticle. (C) 1997 Academic Press.