LF4/MOK and a CDK-related kinase regulate the number and length of cilia in Tetrahymena

The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena, carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is de...

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Published inPLoS genetics Vol. 15; no. 7; p. e1008099
Main Authors Jiang, Yu-Yang, Maier, Wolfgang, Baumeister, Ralf, Minevich, Gregory, Joachimiak, Ewa, Wloga, Dorota, Ruan, Zheng, Kannan, Natarajan, Bocarro, Stephen, Bahraini, Anoosh, Vasudevan, Krishna Kumar, Lechtreck, Karl, Orias, Eduardo, Gaertig, Jacek
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 24.07.2019
Public Library of Science (PLoS)
Subjects
Basal bodies
Biochemistry
Bioinformatics
Biology and Life Sciences
Cellular biology
Cilia
Cilia - metabolism
Cyclin-dependent kinase
Cyclin-Dependent Kinases - metabolism
Funding
Gene Expression Regulation
Genetic aspects
Genetic screening
Genomes
Kinases
Laboratories
Locomotion
Medicine and Health Sciences
Mitogen-Activated Protein Kinases - metabolism
Mutation
Phosphorylation
Phosphotransferases
Physiological aspects
Proteins
Protozoan Proteins - metabolism
Research and Analysis Methods
Supervision
Tetrahymena
Tetrahymena - cytology
Tetrahymena - metabolism
Tetrahymena - physiology
United States
New York
Santa Barbara California
United States > US
Poland
Georgia
California
Germany
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Abstract The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena, carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is dependent on their position with the cell. In Tetrahymena, loss of an LF4/MOK ortholog, LF4A, lengthened the locomotory cilia, but also reduced their number. Without LF4A, cilia assembled faster and showed signs of increased intraflagellar transport (IFT). Consistently, overproduced LF4A shortened cilia and downregulated IFT. GFP-tagged LF4A, expressed in the native locus and imaged by total internal reflection microscopy, was enriched at the basal bodies and distributed along the shafts of cilia. Within cilia, most LF4A-GFP particles were immobile and a few either diffused or moved by IFT. We suggest that the distribution of LF4/MOK along the cilium delivers a uniform dose of inhibition to IFT trains that travel from the base to the tip. In a longer cilium, the IFT machinery may experience a higher cumulative dose of inhibition by LF4/MOK. Thus, LF4/MOK activity could be a readout of cilium length that helps to balance the rate of IFT-driven assembly with the rate of disassembly at steady state. We used a forward genetic screen to identify a CDK-related kinase, CDKR1, whose loss-of-function suppressed the shortening of cilia caused by overexpression of LF4A, by reducing its kinase activity. Loss of CDKR1 alone lengthened both the locomotory and oral cilia. CDKR1 resembles other known ciliary CDK-related kinases: LF2 of Chlamydomonas, mammalian CCRK and DYF-18 of C. elegans, in lacking the cyclin-binding motif and acting upstream of RCKs. The new genetic tools we developed here for Tetrahymena have potential for further dissection of the principles of cilia length regulation in multiciliated cells.
AbstractList The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena , carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is dependent on their position with the cell. In Tetrahymena , loss of an LF4/MOK ortholog, LF4A, lengthened the locomotory cilia, but also reduced their number. Without LF4A, cilia assembled faster and showed signs of increased intraflagellar transport (IFT). Consistently, overproduced LF4A shortened cilia and downregulated IFT. GFP-tagged LF4A, expressed in the native locus and imaged by total internal reflection microscopy, was enriched at the basal bodies and distributed along the shafts of cilia. Within cilia, most LF4A-GFP particles were immobile and a few either diffused or moved by IFT. We suggest that the distribution of LF4/MOK along the cilium delivers a uniform dose of inhibition to IFT trains that travel from the base to the tip. In a longer cilium, the IFT machinery may experience a higher cumulative dose of inhibition by LF4/MOK. Thus, LF4/MOK activity could be a readout of cilium length that helps to balance the rate of IFT-driven assembly with the rate of disassembly at steady state. We used a forward genetic screen to identify a CDK-related kinase, CDKR1, whose loss-of-function suppressed the shortening of cilia caused by overexpression of LF4A, by reducing its kinase activity. Loss of CDKR1 alone lengthened both the locomotory and oral cilia. CDKR1 resembles other known ciliary CDK-related kinases: LF2 of Chlamydomonas , mammalian CCRK and DYF-18 of C . elegans , in lacking the cyclin-binding motif and acting upstream of RCKs. The new genetic tools we developed here for Tetrahymena have potential for further dissection of the principles of cilia length regulation in multiciliated cells. Cilia are conserved organelles that generate motility and mediate vital sensory functions, including olfaction and vision. Cilia that are either too short or too long fail to generate proper forces or responses to extracellular signals. Several cilia-based diseases (ciliopathies) are associated with defects in cilia length. We used the multiciliated model protist Tetrahymena , to study a conserved protein kinase whose activity shortens cilia, LF4/MOK. We find that cells lacking a LF4/MOK kinase of Tetrahymena , LF4A, have excessively long, but also fewer cilia. We show that LF4A decreases intraflagellar transport, a mechanism that shuttles ciliary precursors from the cilium base to the tip. Live imaging revealed that LF4A is distributed along the entire length of the cilium and remains mostly immobile, likely due to its anchoring to ciliary microtubules. We speculate that in longer cilia, the intraflagellar transport machinery is exposed to a higher dose of inhibition by LF4A, which could decrease the rate of cilium assembly, to balance the rate of cilium disassembly in mature cilia that maintain stable length. We use a genetic screen to identify another kinase, CDKR1, as an activator of LF4A. The new tools described here should be useful in further dissection of the principles of cilia length regulation in multiciliated cells.
The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena, carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is dependent on their position with the cell. In Tetrahymena, loss of an LF4/MOK ortholog, LF4A, lengthened the locomotory cilia, but also reduced their number. Without LF4A, cilia assembled faster and showed signs of increased intraflagellar transport (IFT). Consistently, overproduced LF4A shortened cilia and downregulated IFT. GFP-tagged LF4A, expressed in the native locus and imaged by total internal reflection microscopy, was enriched at the basal bodies and distributed along the shafts of cilia. Within cilia, most LF4A-GFP particles were immobile and a few either diffused or moved by IFT. We suggest that the distribution of LF4/MOK along the cilium delivers a uniform dose of inhibition to IFT trains that travel from the base to the tip. In a longer cilium, the IFT machinery may experience a higher cumulative dose of inhibition by LF4/MOK. Thus, LF4/MOK activity could be a readout of cilium length that helps to balance the rate of IFT-driven assembly with the rate of disassembly at steady state. We used a forward genetic screen to identify a CDK-related kinase, CDKR1, whose loss-of-function suppressed the shortening of cilia caused by overexpression of LF4A, by reducing its kinase activity. Loss of CDKR1 alone lengthened both the locomotory and oral cilia. CDKR1 resembles other known ciliary CDK-related kinases: LF2 of Chlamydomonas, mammalian CCRK and DYF-18 of C. elegans, in lacking the cyclin-binding motif and acting upstream of RCKs. The new genetic tools we developed here for Tetrahymena have potential for further dissection of the principles of cilia length regulation in multiciliated cells.
The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena, carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is dependent on their position with the cell. In Tetrahymena, loss of an LF4/MOK ortholog, LF4A, lengthened the locomotory cilia, but also reduced their number. Without LF4A, cilia assembled faster and showed signs of increased intraflagellar transport (IFT). Consistently, overproduced LF4A shortened cilia and downregulated IFT. GFP-tagged LF4A, expressed in the native locus and imaged by total internal reflection microscopy, was enriched at the basal bodies and distributed along the shafts of cilia. Within cilia, most LF4A-GFP particles were immobile and a few either diffused or moved by IFT. We suggest that the distribution of LF4/MOK along the cilium delivers a uniform dose of inhibition to IFT trains that travel from the base to the tip. In a longer cilium, the IFT machinery may experience a higher cumulative dose of inhibition by LF4/MOK. Thus, LF4/MOK activity could be a readout of cilium length that helps to balance the rate of IFT-driven assembly with the rate of disassembly at steady state. We used a forward genetic screen to identify a CDK-related kinase, CDKR1, whose loss-of-function suppressed the shortening of cilia caused by overexpression of LF4A, by reducing its kinase activity. Loss of CDKR1 alone lengthened both the locomotory and oral cilia. CDKR1 resembles other known ciliary CDK-related kinases: LF2 of Chlamydomonas, mammalian CCRK and DYF-18 of C. elegans, in lacking the cyclin-binding motif and acting upstream of RCKs. The new genetic tools we developed here for Tetrahymena have potential for further dissection of the principles of cilia length regulation in multiciliated cells.The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK kinases. The multiciliated protist model, Tetrahymena, carries two types of cilia (oral and locomotory) and the length of the locomotory cilia is dependent on their position with the cell. In Tetrahymena, loss of an LF4/MOK ortholog, LF4A, lengthened the locomotory cilia, but also reduced their number. Without LF4A, cilia assembled faster and showed signs of increased intraflagellar transport (IFT). Consistently, overproduced LF4A shortened cilia and downregulated IFT. GFP-tagged LF4A, expressed in the native locus and imaged by total internal reflection microscopy, was enriched at the basal bodies and distributed along the shafts of cilia. Within cilia, most LF4A-GFP particles were immobile and a few either diffused or moved by IFT. We suggest that the distribution of LF4/MOK along the cilium delivers a uniform dose of inhibition to IFT trains that travel from the base to the tip. In a longer cilium, the IFT machinery may experience a higher cumulative dose of inhibition by LF4/MOK. Thus, LF4/MOK activity could be a readout of cilium length that helps to balance the rate of IFT-driven assembly with the rate of disassembly at steady state. We used a forward genetic screen to identify a CDK-related kinase, CDKR1, whose loss-of-function suppressed the shortening of cilia caused by overexpression of LF4A, by reducing its kinase activity. Loss of CDKR1 alone lengthened both the locomotory and oral cilia. CDKR1 resembles other known ciliary CDK-related kinases: LF2 of Chlamydomonas, mammalian CCRK and DYF-18 of C. elegans, in lacking the cyclin-binding motif and acting upstream of RCKs. The new genetic tools we developed here for Tetrahymena have potential for further dissection of the principles of cilia length regulation in multiciliated cells.
Audience Academic
Author Orias, Eduardo
Minevich, Gregory
Baumeister, Ralf
Gaertig, Jacek
Joachimiak, Ewa
Wloga, Dorota
Vasudevan, Krishna Kumar
Maier, Wolfgang
Lechtreck, Karl
Bahraini, Anoosh
Jiang, Yu-Yang
Bocarro, Stephen
Kannan, Natarajan
Ruan, Zheng
AuthorAffiliation 1 Department of Cellular Biology, University of Georgia, Athens, Georgia, United States of America
4 Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
3 Department of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, New York, United States of America
5 Institute of Bioinformatics, University of Georgia, Athens, Georgia, United States of America
6 Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, United States of America
7 Department of Molecular, Cellular and Developmental Biology, University of California Santa Barbara, Santa Barbara, California, United States of America
2 Bio 3/Bioinformatics and Molecular Genetics, Faculty of Biology and ZBMZ, Faculty of Medicine, Albert-Ludwigs-University of Freiburg, Freiburg, Germany
Washington University School of Medicine, UNITED STATES
AuthorAffiliation_xml – name: 3 Department of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, New York, United States of America
– name: 5 Institute of Bioinformatics, University of Georgia, Athens, Georgia, United States of America
– name: 7 Department of Molecular, Cellular and Developmental Biology, University of California Santa Barbara, Santa Barbara, California, United States of America
– name: Washington University School of Medicine, UNITED STATES
– name: 2 Bio 3/Bioinformatics and Molecular Genetics, Faculty of Biology and ZBMZ, Faculty of Medicine, Albert-Ludwigs-University of Freiburg, Freiburg, Germany
– name: 4 Laboratory of Cytoskeleton and Cilia Biology, Nencki Institute of Experimental Biology of Polish Academy of Sciences, Warsaw, Poland
– name: 6 Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, United States of America
– name: 1 Department of Cellular Biology, University of Georgia, Athens, Georgia, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31339880$$D View this record in MEDLINE/PubMed
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2019 Jiang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2019 Jiang et al 2019 Jiang et al
Copyright_xml – notice: COPYRIGHT 2019 Public Library of Science
– notice: 2019 Jiang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet The length of cilia is controlled by a poorly understood mechanism that involves members of the conserved RCK kinase group, and among them, the LF4/MOK...
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StartPage e1008099
SubjectTerms Basal bodies
Biochemistry
Bioinformatics
Biology and Life Sciences
Cellular biology
Cilia
Cilia - metabolism
Cyclin-dependent kinase
Cyclin-Dependent Kinases - metabolism
Funding
Gene Expression Regulation
Genetic aspects
Genetic screening
Genomes
Kinases
Laboratories
Locomotion
Medicine and Health Sciences
Mitogen-Activated Protein Kinases - metabolism
Mutation
Phosphorylation
Phosphotransferases
Physiological aspects
Proteins
Protozoan Proteins - metabolism
Research and Analysis Methods
Supervision
Tetrahymena
Tetrahymena - cytology
Tetrahymena - metabolism
Tetrahymena - physiology
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Title LF4/MOK and a CDK-related kinase regulate the number and length of cilia in Tetrahymena
URI https://www.ncbi.nlm.nih.gov/pubmed/31339880
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http://dx.doi.org/10.1371/journal.pgen.1008099
Volume 15
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