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Tau Tubulin Kinase is required for spermatogenesis and development of motile cilia in planarian flatworms.

Abstract

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 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 homologs 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 paralogs by RNA-interference (RNAi) revealed a specific requirement for Smed-TTBK-d in post-meiotic 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 multi-ciliated 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 post-meiotic regulators of sperm development and also contribute to the formation of motile cilia in the soma.

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  • Authors+Show Affiliations

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    Department of Biological Sciences, Wright State University, 3640 Colonel Glenn Highway, Dayton, OH 45435, U.S.A.

    Department of Biological Sciences, Wright State University, 3640 Colonel Glenn Highway, Dayton, OH 45435, U.S.A.

    Source

    Molecular biology of the cell : 2019 05 29 pg mbcE18100663

    Pub Type(s)

    Journal Article

    Language

    eng

    PubMed ID

    31141462

    Citation

    Magley, Robert Alan, and Labib Rouhana. "Tau Tubulin Kinase Is Required for Spermatogenesis and Development of Motile Cilia in Planarian Flatworms." Molecular Biology of the Cell, 2019, pp. mbcE18100663.
    Magley RA, Rouhana L. Tau Tubulin Kinase is required for spermatogenesis and development of motile cilia in planarian flatworms. Mol Biol Cell. 2019.
    Magley, R. A., & Rouhana, L. (2019). Tau Tubulin Kinase is required for spermatogenesis and development of motile cilia in planarian flatworms. Molecular Biology of the Cell, pp. mbcE18100663. doi:10.1091/mbc.E18-10-0663.
    Magley RA, Rouhana L. Tau Tubulin Kinase Is Required for Spermatogenesis and Development of Motile Cilia in Planarian Flatworms. Mol Biol Cell. 2019 05 29;mbcE18100663. PubMed PMID: 31141462.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Tau Tubulin Kinase is required for spermatogenesis and development of motile cilia in planarian flatworms. AU - Magley,Robert Alan, AU - Rouhana,Labib, Y1 - 2019/05/29/ PY - 2019/5/30/entrez PY - 2019/5/30/pubmed PY - 2019/5/30/medline SP - mbcE18100663 EP - mbcE18100663 JF - Molecular biology of the cell JO - Mol. Biol. Cell N2 - 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 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 homologs 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 paralogs by RNA-interference (RNAi) revealed a specific requirement for Smed-TTBK-d in post-meiotic 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 multi-ciliated 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 post-meiotic regulators of sperm development and also contribute to the formation of motile cilia in the soma. SN - 1939-4586 UR - https://www.unboundmedicine.com/medline/citation/31141462/Tau_Tubulin_Kinase_is_required_for_spermatogenesis_and_development_of_motile_cilia_in_planarian_flatworms L2 - https://www.molbiolcell.org/doi/full/10.1091/mbc.E18-10-0663?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -