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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Autores principales: Shubha Vij, Jochen C Rink, Hao Kee Ho, Deepak Babu, Michael Eitel, Vijayashankaranarayanan Narasimhan, Varnesh Tiku, Jody Westbrook, Bernd Schierwater, Sudipto Roy
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spelling oai:doaj.org-article:90c04b3620684d5090d575e0ef456a952021-11-18T06:20:35ZEvolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program.1553-73901553-740410.1371/journal.pgen.1003019https://doaj.org/article/90c04b3620684d5090d575e0ef456a952012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23144623/pdf/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404It 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.Shubha VijJochen C RinkHao Kee HoDeepak BabuMichael EitelVijayashankaranarayanan NarasimhanVarnesh TikuJody WestbrookBernd SchierwaterSudipto RoyPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 8, Iss 11, p e1003019 (2012)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Shubha Vij
Jochen C Rink
Hao Kee Ho
Deepak Babu
Michael Eitel
Vijayashankaranarayanan Narasimhan
Varnesh Tiku
Jody Westbrook
Bernd Schierwater
Sudipto Roy
Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program.
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.
format article
author Shubha Vij
Jochen C Rink
Hao Kee Ho
Deepak Babu
Michael Eitel
Vijayashankaranarayanan Narasimhan
Varnesh Tiku
Jody Westbrook
Bernd Schierwater
Sudipto Roy
author_facet Shubha Vij
Jochen C Rink
Hao Kee Ho
Deepak Babu
Michael Eitel
Vijayashankaranarayanan Narasimhan
Varnesh Tiku
Jody Westbrook
Bernd Schierwater
Sudipto Roy
author_sort Shubha Vij
title 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_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_sort evolutionarily ancient association of the foxj1 transcription factor with the motile ciliogenic program.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/90c04b3620684d5090d575e0ef456a95
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