Caenorhabditis elegans SORB-1 localizes to integrin adhesion sites and is required for organization of sarcomeres and mitochondria in myocytes

Abstract

We have identified and characterized sorb-1, the only sorbin and SH3 domain–containing protein family member in Caenorhabditis elegans. SORB-1 is strongly localized to integrin adhesion complexes in larvae and adults, including adhesion plaques and dense bodies (Z-disks) of striated muscles and attachment plaques of smooth muscles. SORB-1 is recruited to the actin-binding, membrane-distal regions of dense bodies via its C-terminal SH3 domains in an ATN-1(α-actinin)– and ALP-1(ALP/Enigma)–dependent manner, where it contributes to the organization of sarcomeres. SORB-1 is also found in other tissues known to be under mechanical stress, including stress fibers in migratory distal tip cells and the proximal gonad sheath, where it becomes enriched in response to tissue distention. We provide evidence for a novel role for sorbin family proteins: SORB-1 is required for normal positioning of the mitochondrial network in muscle cells. Finally, we demonstrate that SORB-1 interacts directly with two other dense body components, DEB-1(vinculin) and ZYX-1(zyxin). This work establishes SORB-1 as a bona fide sorbin family protein—one of the late additions to the dense body complex and a conserved regulator of body wall muscle sarcomere organization and organelle positioning.