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Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms

Cilia are microtubule-based structures that protrude from the apical surface of cells to mediate motility, transport, intracellular signaling, and environmental sensing. Tau tubulin kinases (TTBKs) destabilize microtubules by phosphorylating microtubule-associated proteins (MAPs) of the MAP2/Tau fam...

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Autores principales: Magley, Robert Alan, Rouhana, Labib
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743461/
https://www.ncbi.nlm.nih.gov/pubmed/31141462
http://dx.doi.org/10.1091/mbc.E18-10-0663
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author Magley, Robert Alan
Rouhana, Labib
author_facet Magley, Robert Alan
Rouhana, Labib
author_sort Magley, Robert Alan
collection PubMed
description Cilia are microtubule-based structures that protrude from the apical surface of cells to mediate motility, transport, intracellular signaling, and environmental sensing. Tau tubulin kinases (TTBKs) destabilize microtubules by phosphorylating microtubule-associated proteins (MAPs) of the MAP2/Tau family, but also contribute to the assembly of primary cilia during embryogenesis. Expression of TTBKs is enriched in testicular tissue, but their relevance to reproductive processes is unknown. We identified six TTBK homologues in the genome of the planarian Schmidtea mediterranea (Smed-TTBK-a, -b, -c, -d, -e, and -f), all of which are preferentially expressed in testes. Inhibition of TTBK paralogues by RNA interference (RNAi) revealed a specific requirement for Smed-TTBK-d in postmeiotic regulation of spermatogenesis. Disrupting expression of Smed-TTBK-d results in loss of spermatozoa, but not spermatids. In the soma, Smed-TTBK-d RNAi impaired the function of multiciliated epidermal cells in propelling planarian movement, as well as the osmoregulatory function of protonephridia. Decreased density and structural defects of motile cilia were observed in the epidermis of Smed-TTBK-d(RNAi) by phase contrast, immunofluorescence, and transmission electron microscopy. Altogether, these results demonstrate that members of the TTBK family of proteins are postmeiotic regulators of sperm development and also contribute to the formation of motile cilia in the soma.
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spelling pubmed-67434612019-10-16 Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms Magley, Robert Alan Rouhana, Labib Mol Biol Cell Articles Cilia are microtubule-based structures that protrude from the apical surface of cells to mediate motility, transport, intracellular signaling, and environmental sensing. Tau tubulin kinases (TTBKs) destabilize microtubules by phosphorylating microtubule-associated proteins (MAPs) of the MAP2/Tau family, but also contribute to the assembly of primary cilia during embryogenesis. Expression of TTBKs is enriched in testicular tissue, but their relevance to reproductive processes is unknown. We identified six TTBK homologues in the genome of the planarian Schmidtea mediterranea (Smed-TTBK-a, -b, -c, -d, -e, and -f), all of which are preferentially expressed in testes. Inhibition of TTBK paralogues by RNA interference (RNAi) revealed a specific requirement for Smed-TTBK-d in postmeiotic regulation of spermatogenesis. Disrupting expression of Smed-TTBK-d results in loss of spermatozoa, but not spermatids. In the soma, Smed-TTBK-d RNAi impaired the function of multiciliated epidermal cells in propelling planarian movement, as well as the osmoregulatory function of protonephridia. Decreased density and structural defects of motile cilia were observed in the epidermis of Smed-TTBK-d(RNAi) by phase contrast, immunofluorescence, and transmission electron microscopy. Altogether, these results demonstrate that members of the TTBK family of proteins are postmeiotic regulators of sperm development and also contribute to the formation of motile cilia in the soma. The American Society for Cell Biology 2019-08-01 /pmc/articles/PMC6743461/ /pubmed/31141462 http://dx.doi.org/10.1091/mbc.E18-10-0663 Text en © 2019 Magley and Rouhana. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Magley, Robert Alan
Rouhana, Labib
Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title_full Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title_fullStr Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title_full_unstemmed Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title_short Tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
title_sort tau tubulin kinase is required for spermatogenesis and development of motile cilia in planarian flatworms
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6743461/
https://www.ncbi.nlm.nih.gov/pubmed/31141462
http://dx.doi.org/10.1091/mbc.E18-10-0663
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