The Tubulation Activity of a Fission Yeast F-BAR Protein Is Dispensable for Its Function in Cytokinesis

Authors

Nathan A. McDonald, Vanderbilt University
Yoshimasa Takizawa, Vanderbilt University
Anna Feoktistova, Vanderbilt University
Ping Xu, University of KentuckyFollow
Melanie D. Ohi, Vanderbilt University
Craig W. Vander Kooi, University of KentuckyFollow
Kathleen L. Gould, Vanderbilt University

Abstract

F-BAR proteins link cellular membranes to the actin cytoskeleton in many biological processes. Here we investigated the function of the Schizosaccharomyces pombe Imp2 F-BAR domain in cytokinesis and find that it is critical for Imp2's role in contractile ring constriction and disassembly. To understand mechanistically how the F-BAR domain functions, we determined its structure, elucidated how it interacts with membranes, and identified an interaction between dimers that allows helical oligomerization and membrane tubulation. Using mutations that block either membrane binding or tubulation, we find that membrane binding is required for Imp2's cytokinetic function but that oligomerization and tubulation, activities often deemed central to F-BAR protein function, are dispensable. Accordingly, F-BARs that do not have the capacity to tubulate membranes functionally substitute for the Imp2 F-BAR, establishing that its major role is as a cell-cycle-regulated bridge between the membrane and Imp2 protein partners, rather than as a driver of membrane curvature.

Document Type

Article

Publication Date

1-26-2016

Notes/Citation Information

Published in Cell Reports, v. 14, no. 3, p. 534-546.

©2016 The Authors

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Digital Object Identifier (DOI)

http://dx.doi.org/10.1016/j.celrep.2015.12.062

Funding Information

The authors thank Dr. Rachel Roberts-Galbraith and members of the K.L.G. laboratory, especially Dr. Janel Beckley, for critical review of the manuscript; the Vanderbilt Center for Structural Biology for Analytical Ultracentrifuge and Electron Microscopy Facility support; and NIH grant P20GM103486 for University of Kentucky core support. N.A.M. was supported by AHA fellowship 15PRE21780003. This work was supported by NIH grant GM101035 to K.L.G.

Repository Citation

McDonald, Nathan A.; Takizawa, Yoshimasa; Feoktistova, Anna; Xu, Ping; Ohi, Melanie D.; Vander Kooi, Craig W.; and Gould, Kathleen L., "The Tubulation Activity of a Fission Yeast F-BAR Protein Is Dispensable for Its Function in Cytokinesis" (2016). Molecular and Cellular Biochemistry Faculty Publications. 79.
https://uknowledge.uky.edu/biochem_facpub/79