Competition between myosin II and βH-spectrin regulates cytoskeletal tension

Author:

Ibar Consuelo1ORCID,Chinthalapudi Krishna2ORCID,Heissler Sarah M2,Irvine Kenneth D1ORCID

Affiliation:

1. Waksman Institute and Department of Molecular Biology and Biochemistry, Rutgers University

2. Department of Physiology and Cell Biology, Dorothy M. Davis Heart and Lung Research Institute, The Ohio State University College of Medicine

Abstract

Spectrins are membrane cytoskeletal proteins generally thought to function as heterotetramers comprising two α-spectrins and two β-spectrins. They influence cell shape and Hippo signaling, but the mechanism by which they influence Hippo signaling has remained unclear. We have investigated the role and regulation of the Drosophila β-heavy spectrin (βH-spectrin, encoded by the karst gene) in wing imaginal discs. Our results establish that βH-spectrin regulates Hippo signaling through the Jub biomechanical pathway due to its influence on cytoskeletal tension. While we find that α-spectrin also regulates Hippo signaling through Jub, unexpectedly, we find that βH-spectrin localizes and functions independently of α-spectrin. Instead, βH-spectrin co-localizes with and reciprocally regulates and is regulated by myosin. In vivo and in vitro experiments support a model in which βH-spectrin and myosin directly compete for binding to apical F-actin. This competition can explain the influence of βH-spectrin on cytoskeletal tension and myosin accumulation. It also provides new insight into how βH-spectrin participates in ratcheting mechanisms associated with cell shape change.

Funder

National Institute of General Medical Sciences

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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