Kinesin-13 regulates the quantity and quality of tubulin inside cilia

• Type of Material: Article
• Authors: Krishna Kumar Vasudevan, University of Georgia; Yu-Yang Jiang, University of Georgia; Karl F. Lechtreck, University of Georgia; Yasuharu Kushida, University of Tsukuba; Lea Alford, Emory University; Winfield Sale, Emory University; Todd Hennessey, State University of New York at Buffalo; Jacek Gaertig, University of Georgia
• Language: English
• Date: 2015-02-01
• Publisher: American Society for Cell Biology
• Publication Version: Final Published Version
• Copyright Statement: © 2015 Vasudevan et al. This article is distributed by The American Society for Cell Biology under license from the author(s).
• License: Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported
• Final Published Version (URL): http://dx.doi.org/10.1091/mbc.E14-09-1354
• Title of Journal or Parent Work: Molecular Biology of the Cell
• ISSN: 1059-1524
• Volume: 26
• Issue: 3
• Start Page: 478
• End Page: 494
• Grant/Funding Information: This study was supported by grants from the National Science Foundation (MBC-033965) and the National Institutes of Health (RO1GM089912 to J.G., RO1GM0571173 to W.S.S., and RO1GM110413 to K.L.).
• Keywords: MICRONUCLEAR DIVISION; TETRAHYMENA-THERMOPHILA; LENGTH CONTROL; MICROTUBULE-DEPOLYMERIZING KINESIN; FLAGELLAR MICROTUBULES; ALPHA-TUBULIN; ACETYLTRANSFERASE; Life Sciences & Biomedicine; SPINDLE ULTRASTRUCTURE; POSTTRANSLATIONAL MODIFICATIONS; Science & Technology; Cell Biology; MOLECULAR-BASIS
• Research Categories: Biology, Cell; Biology, General

Abstract

Kinesin-13, an end depolymerizer of cytoplasmic and spindle microtubules, also affects the length of cilia. However, in different models, depletion of kinesin-13 either lengthens or shortens cilia, and therefore the exact function of kinesin-13 in cilia remains unclear. We generated null mutations of all kinesin-13 paralogues in the ciliate Tetrahymena. One of the paralogues, Kin13Ap, localizes to the nuclei and is essential for nuclear divisions. The remaining two paralogues, Kin13Bp and Kin13Cp, localize to the cell body and inside assembling cilia. Loss of both Kin13Bp and Kin13Cp resulted in slow cell multiplication and motility, overgrowth of cell body microtubules, shortening of cilia, and synthetic lethality with either paclitaxel or a deletion of MEC-17/ATAT1, the α-tubulin acetyltransferase. The mutant cilia assembled slowly and contained abnormal tubulin, characterized by altered posttranslational modifications and hypersensitivity to paclitaxel. The mutant cilia beat slowly and axonemes showed reduced velocity of microtubule sliding. Thus kinesin-13 positively regulates the axoneme length, influences the properties of ciliary tubulin, and likely indirectly, through its effects on the axonemal microtubules, affects the ciliary dynein-dependent motility.