Exoskeletal Proteins Enable Insect Locomotion

Abstract

Exo- and Endoskeleton function enables muscle-mediated locomotion in animals. In mammals, the defective protein matrix of bones found in systematic skeletal disorders such as osteoporosis causes fractures and severe skeletal deformations under high muscle tension. We identified an analogous mechanism for integrating muscle-mediated tension into the apical extracellular matrix (aECM) of the invertebrate body wall exoskeleton. Obstructor chitin-binding proteins, the chitin deacetylases, Chitinases, and the matrix-protecting proteins Knickkopf and Retroactive are epidermally expressed during late embryogenesis. Their control of forming epidermal chitinous structures protects the exoskeletal aECM from collapsing when embryos start moving and hatch as larvae. Consequently, mutation and knockdown of these genes cause changes in normal movement behavior and lower the speed of larvae. Moreover, we found that the transmembrane Zona Pellucida domain protein Piopio provides the adhesion between the epidermal apical membrane and the overlaying chitinous aECM in a matriptase-dependent manner. A failure of Pio and chitin-associated proteins leads to exoskeletal deformations and detachment from the epidermal membrane, destabilizing muscle forces and impairing larval mobility. Our data identifies an evolutionarily well-conserved protein network that transforms the chitinous aECM into a stable exoskeleton that directly resists muscle impact at epidermal tendon cells, thereby serving locomotion. Demonstrating the importance of these proteins in producing aECM as a three-dimensional cuticular scaffold for exoskeletal function opens up opportunities for the development of biomimetic applications of synthetic materials.

Keywords: chitin material, chitinase, cuticle, deacetylase, epithelium, exoskeleton, Extracellular matrix, muscle, tendon, zona pellucida