Epithelial cells secrete apical extracellular matrices to form protruding structures such as denticles, ridges, scales, or teeth. The mechanisms that shape these structures remain poorly understood. Here, we show how the actin cytoskeleton and a provisional matrix work together to sculpt acellular longitudinal alae ridges in the cuticle of adult C. elegans. Transient assembly of longitudinal actomyosin filaments in the underlying lateral epidermis accompanies deposition of the provisional matrix at the earliest stages of alae formation. Actin is required to pattern the provisional matrix into longitudinal bands that are initially offset from the pattern of longitudinal actin filaments. These bands appear ultrastructurally as alternating regions of adhesion and separation within laminated provisional matrix layers. The provisional matrix is required to establish these demarcated zones of adhesion and separation, which ultimately give rise to alae ridges and their intervening valleys, respectively. Provisional matrix proteins shape the alae ridges and valleys but are not present within the final structure. We propose a morphogenetic mechanism wherein cortical actin patterns are relayed to the laminated provisional matrix to set up distinct zones of matrix layer separation and accretion that shape a permanent and acellular matrix structure.

Specialized epithelia produce apical matrices with distinctive topographies by enigmatic mechanisms. Here, we describe a holistic mechanism that integrates cortical actomyosin dynamics with apical matrix remodeling to pattern C. elegans cuticles. Therein, axial AFBs appear near the surface of lateral epidermal syncytia during an interval of transverse apical constriction (AC). AC gives rise to three temporary semi-circular cellular protrusions beneath a provisional matrix (sheath). In turn, sheath components pattern durable ridges along the midline of adult cuticles (alae). We propose that forces generated by AC are relayed via the sheath to sculpt the the acellular adult cuticle manifest several hours later. Furthermore, we provide evidence that circumferential actin filament bundles (CFBs) near the surface of the adjacent syncytia (hyp7) are largely dispensable for the propagation of annular cuticle structures from one larval stage to the next. Rather, the temporary CFBs extend from actin bundles overlying body wall muscles, which are situated between Ce. hemidesmosomes. Similar mechanisms may contribute to the morphogenesis of integumentary organs in higher metazoans.

Apical extracellular matrices can form protruding structures such as denticles, ridges, scales, or teeth on the surfaces of epithelia. The mechanisms that shape these structures remain poorly understood. Here, we show how the actin cytoskeleton and a provisional matrix work together to sculpt acellular longitudinal alae ridges in the cuticle of adult C. elegans. Transient actomyosin-dependent constriction of the underlying lateral epidermis accompanies deposition of the provisional matrix at the earliest stages of alae formation. Actin is required to pattern the provisional matrix into longitudinal bands that are initially offset from the pattern of longitudinal actin filaments. These bands appear ultrastructurally as alternating regions of adhesion and separation within laminated provisional matrix layers. The provisional matrix is required to establish these demarcated zones of adhesion and separation, which ultimately give rise to alae ridges and their intervening valleys, respectively. Provisional matrix proteins shape the alae ridges and valleys but are not present within the final structure. We propose a morphogenetic mechanism wherein cortical actin patterns are relayed mechanically to the laminated provisional matrix to set up distinct zones of matrix layer separation and accretion that shape a permanent and acellular matrix structure.