Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program

It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved...

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Main Authors: Vij, Shubha, Eitel, Michael, Ho, Hao Kee, Babu, Deepak, Narasimhan, Vijayashankaranarayanan, Tiku, Varnesh, Westbrook, Jody, Schierwater, Bernd, Roy, Sudipto, Rink, Jochen C.
Other Authors: Malik, Harmit S.
Format: Journal Article
Language:English
Published: 2014
Subjects:
Online Access:https://hdl.handle.net/10356/101613
http://hdl.handle.net/10220/18689
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author Vij, Shubha
Eitel, Michael
Ho, Hao Kee
Babu, Deepak
Narasimhan, Vijayashankaranarayanan
Tiku, Varnesh
Westbrook, Jody
Schierwater, Bernd
Roy, Sudipto
Rink, Jochen C.
author2 Malik, Harmit S.
author_facet Malik, Harmit S.
Vij, Shubha
Eitel, Michael
Ho, Hao Kee
Babu, Deepak
Narasimhan, Vijayashankaranarayanan
Tiku, Varnesh
Westbrook, Jody
Schierwater, Bernd
Roy, Sudipto
Rink, Jochen C.
author_sort Vij, Shubha
collection NTU
description It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved structure, and their mechanism of motility, the evolution of the transcriptional program controlling ciliogenesis has remained incompletely understood. In particular, it is presently not known how the generation of motile cilia is programmed outside of the vertebrates, and whether and to what extent the FoxJ1-dependent regulation is conserved. We have performed a survey of numerous eukaryotic genomes and discovered that genes homologous to foxJ1 are restricted only to organisms belonging to the unikont lineage. Using a mis-expression assay, we then obtained evidence of a conserved ability of FoxJ1 proteins from a number of diverse phyletic groups to activate the expression of a host of motile ciliary genes in zebrafish embryos. Conversely, we found that inactivation of a foxJ1 gene in Schmidtea mediterranea, a platyhelminth (flatworm) that utilizes motile cilia for locomotion, led to a profound disruption in the differentiation of motile cilia. Together, all of these findings provide the first evolutionary perspective into the transcriptional control of motile ciliogenesis and allow us to propose a conserved FoxJ1-regulated mechanism for motile cilia biogenesis back to the origin of the metazoans.
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spelling ntu-10356/1016132023-02-28T17:05:01Z Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program Vij, Shubha Eitel, Michael Ho, Hao Kee Babu, Deepak Narasimhan, Vijayashankaranarayanan Tiku, Varnesh Westbrook, Jody Schierwater, Bernd Roy, Sudipto Rink, Jochen C. Malik, Harmit S. School of Biological Sciences DRNTU::Science::Biological sciences It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved structure, and their mechanism of motility, the evolution of the transcriptional program controlling ciliogenesis has remained incompletely understood. In particular, it is presently not known how the generation of motile cilia is programmed outside of the vertebrates, and whether and to what extent the FoxJ1-dependent regulation is conserved. We have performed a survey of numerous eukaryotic genomes and discovered that genes homologous to foxJ1 are restricted only to organisms belonging to the unikont lineage. Using a mis-expression assay, we then obtained evidence of a conserved ability of FoxJ1 proteins from a number of diverse phyletic groups to activate the expression of a host of motile ciliary genes in zebrafish embryos. Conversely, we found that inactivation of a foxJ1 gene in Schmidtea mediterranea, a platyhelminth (flatworm) that utilizes motile cilia for locomotion, led to a profound disruption in the differentiation of motile cilia. Together, all of these findings provide the first evolutionary perspective into the transcriptional control of motile ciliogenesis and allow us to propose a conserved FoxJ1-regulated mechanism for motile cilia biogenesis back to the origin of the metazoans. Published version 2014-01-22T06:03:48Z 2019-12-06T20:41:27Z 2014-01-22T06:03:48Z 2019-12-06T20:41:27Z 2012 2012 Journal Article Vij, S., Rink, J. C., Ho, H. K., Babu, D., Eitel, M., Narasimhan, V., et al. (2012). Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS genetics, 8(11), e1003019. 1553-7404 https://hdl.handle.net/10356/101613 http://hdl.handle.net/10220/18689 10.1371/journal.pgen.1003019 23144623 en PLoS genetics © 2012 The Authors. This paper was published in PLOS Genetics and is made available as an electronic reprint (preprint) with permission of the authors. The paper can be found at the following official DOI: [http://dx.doi.org/10.1371/journal.pgen.1003019].  One print or electronic copy may be made for personal use only. Systematic or multiple reproduction, distribution to multiple locations via electronic or other means, duplication of any material in this paper for a fee or for commercial purposes, or modification of the content of the paper is prohibited and is subject to penalties under law. application/pdf
spellingShingle DRNTU::Science::Biological sciences
Vij, Shubha
Eitel, Michael
Ho, Hao Kee
Babu, Deepak
Narasimhan, Vijayashankaranarayanan
Tiku, Varnesh
Westbrook, Jody
Schierwater, Bernd
Roy, Sudipto
Rink, Jochen C.
Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title_full Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title_fullStr Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title_full_unstemmed Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title_short Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program
title_sort evolutionarily ancient association of the foxj1 transcription factor with the motile ciliogenic program
topic DRNTU::Science::Biological sciences
url https://hdl.handle.net/10356/101613
http://hdl.handle.net/10220/18689
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