Identification of 30 transition fibre proteins in Trypanosoma brucei reveals a complex and dynamic structure
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
Wellcome Trust - United Kingdom
Nigel Groome PhD studentship
211075/Z/18/Z
Wellcome Trust - United Kingdom
Oxford Brookes University
PubMed
38572631
PubMed Central
PMC11190437
DOI
10.1242/jcs.261692
PII: 352266
Knihovny.cz E-zdroje
- Klíčová slova
- Trypanosoma, Cilia, Ciliogenesis, Distal appendages, Flagella, Transition fibres,
- MeSH
- bazální tělíska metabolismus MeSH
- časové faktory MeSH
- cilie genetika metabolismus MeSH
- flagella genetika metabolismus MeSH
- konzervovaná sekvence MeSH
- protozoální proteiny * genetika metabolismus MeSH
- regulace genové exprese MeSH
- transport proteinů MeSH
- Trypanosoma brucei brucei * genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- protozoální proteiny * MeSH
Transition fibres and distal appendages surround the distal end of mature basal bodies and are essential for ciliogenesis, but only a few of the proteins involved have been identified and functionally characterised. Here, through genome-wide analysis, we have identified 30 transition fibre proteins (TFPs) and mapped their arrangement in the flagellated eukaryote Trypanosoma brucei. We discovered that TFPs are recruited to the mature basal body before and after basal body duplication, with differential expression of five TFPs observed at the assembling new flagellum compared to the existing fixed-length old flagellum. RNAi-mediated depletion of 17 TFPs revealed six TFPs that are necessary for ciliogenesis and a further three TFPs that are necessary for normal flagellum length. We identified nine TFPs that had a detectable orthologue in at least one basal body-forming eukaryotic organism outside of the kinetoplastid parasites. Our work has tripled the number of known transition fibre components, demonstrating that transition fibres are complex and dynamic in their composition throughout the cell cycle, which relates to their essential roles in ciliogenesis and flagellum length regulation.
Department of Biological and Medical Sciences Oxford Brookes University Gipsy Lane Oxford OX3 0BP UK
Peter Medawar Building for Pathogen Research University of Oxford Oxford OX1 3SY UK
Zobrazit více v PubMed
Amos, B., Aurrecoechea, C., Barba, M., Barreto, A., Basenko, E. Y., Bażant, W., Belnap, R., Blevins, A. S., Böhme, U., Brestelli, J.et al. (2022). VEuPathDB: the eukaryotic pathogen, vector and host bioinformatics resource center. Nucleic. Acids Res. 50, D898-D911. 10.1093/nar/gkab929 PubMed DOI PMC
Anderson, R. G. (1972). The three-dimensional structure of the basal body from the rhesus monkey oviduct. J. Cell Biol. 54, 246-265. 10.1083/jcb.54.2.246 PubMed DOI PMC
Andre, J., Kerry, L., Qi, X., Hawkins, E., Drizyte, K., Ginger, M. L. and McKean, P. G. (2014). An alternative model for the role of RP2 protein in flagellum assembly in the African trypanosome. J. Biol. Chem. 289, 464-475. 10.1074/jbc.M113.509521 PubMed DOI PMC
Atkins, M., Týč, J., Shafiq, S., Ahmed, M., Bertiaux, E., De Castro Neto, A. L., Sunter, J., Bastin, P., Dean, S. D. and Vaughan, S. (2021). CEP164C regulates flagellum length in stable flagella. J. Cell Biol. 220, e202001160. 10.1083/jcb.202001160 PubMed DOI PMC
Azimzadeh, J., Hergert, P., Delouvée, A., Euteneuer, U., Formstecher, E., Khodjakov, A. and Bornens, M. (2009). hPOC5 is a centrin-binding protein required for assembly of full-length centrioles. J. Cell Biol. 185, 101-114. 10.1083/jcb.200808082 PubMed DOI PMC
Barker, A. R., Renzaglia, K. S., Fry, K. and Dawe, H. R. (2014). Bioinformatic analysis of ciliary transition zone proteins reveals insights into the evolution of ciliopathy networks. BMC Genomics 15, 531. 10.1186/1471-2164-15-531 PubMed DOI PMC
Bellofatto, V. and Palenchar, J. B. (2008). RNA interference as a genetic tool in trypanosomes. Methods Mol. Biol. 442, 83-94. 10.1007/978-1-59745-191-8_7 PubMed DOI
Bertiaux, E. and Bastin, P. (2020). Dealing with several flagella in the same cell. Cell. Microbiol. 22, e13162. 10.1111/cmi.13162 PubMed DOI
Bertiaux, E., Morga, B., Blisnick, T., Rotureau, B. and Bastin, P. (2018). A grow-and-lock model for the control of flagellum length in trypanosomes. Curr. Biol. 28, 3802-3814.e3. 10.1016/j.cub.2018.10.031 PubMed DOI
Billington, K., Halliday, C., Madden, R., Dyer, P., Barker, A. R., Moreira-Leite, F. F., Carrington, M., Vaughan, S., Hertz-Fowler, C., Dean, S.et al. (2023). Genome-wide subcellular protein map for the flagellate parasite Trypanosoma brucei. Nat. Microbiol. 8, 533-547. 10.1038/s41564-022-01295-6 PubMed DOI PMC
Bowler, M., Kong, D., Sun, S., Nanjundappa, R., Evans, L., Farmer, V., Holland, A., Mahjoub, M. R., Sui, H. and Loncarek, J. (2019). High-resolution characterization of centriole distal appendage morphology and dynamics by correlative STORM and electron microscopy. Nat. Commun. 10, 993. 10.1038/s41467-018-08216-4 PubMed DOI PMC
Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S., Hart, S. R., Portman, N., Shaw, M. K., Ginger, M. L., Gaskell, S. J., McKean, P. G.et al. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227. 10.1038/nature04541 PubMed DOI
Brun, R. and Schönenberger. (1979). Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop. 36, 289-292. PubMed
Carvalho-Santos, Z., Azimzadeh, J., Pereira-Leal, J. B. and Bettencourt-Dias, M. (2011). Evolution: Tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 194, 165-175. 10.1083/jcb.201011152 PubMed DOI PMC
Chaki, M., Airik, R., Ghosh, A. K., Giles, R. H., Chen, R., Slaats, G. G., Wang, H., Hurd, T. W., Zhou, W., Cluckey, A.et al. (2012). Exome capture reveals ZNF423 and CEP164 mutations, linking renal ciliopathies to DNA damage response signaling. Cell 150, 533-548. 10.1016/j.cell.2012.06.028 PubMed DOI PMC
Chan, K. Y. and Ersfeld, K. (2010). The role of the Kinesin-13 family protein TbKif13-2 in flagellar length control of Trypanosoma brucei. Mol. Biochem. Parasitol. 174, 137-140. 10.1016/j.molbiopara.2010.08.001 PubMed DOI PMC
Dacheux, D., Landrein, N., Thonnus, M., Gilbert, G., Sahin, A., Wodrich, H., Robinson, D. R. and Bonhivers, M. (2012). A MAP6-related protein is present in protozoa and is involved in flagellum motility. PLoS ONE 7, e31344. 10.1371/journal.pone.0031344 PubMed DOI PMC
Dang, H. Q., Zhou, Q., Rowlett, V. W., Hu, H., Lee, K. J., Margolin, W. and Li, Z. (2017). Proximity interactions among basal body components in Trypanosoma brucei identify novel regulators of basal body biogenesis and inheritance. MBio 8, e02120-16. 10.1128/mBio.02120-16 PubMed DOI PMC
Dean, S., Sunter, J., Wheeler, R. J., Hodkinson, I., Gluenz, E. and Gull, K. (2015). A toolkit enabling efficient, scalable and reproducible gene tagging in trypanosomatids. Open Biol. 5, 140197. 10.1098/rsob.140197 PubMed DOI PMC
Dean, S., Moreira-Leite, F., Varga, V. and Gull, K. (2016). Cilium transition zone proteome reveals compartmentalization and differential dynamics of ciliopathy complexes. Proc. Natl. Acad. Sci. USA 113, E5135-E5143. 10.1073/pnas.1604258113 PubMed DOI PMC
Dean, S., Moreira-Leite, F. and Gull, K. (2019). Basalin is an evolutionarily unconstrained protein revealed via a conserved role in flagellum basal plate function. eLife 8, e42282. 10.7554/eLife.42282 PubMed DOI PMC
Emms, D. M. and Kelly, S. (2015). OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157. 10.1186/s13059-015-0721-2 PubMed DOI PMC
Emms, D. M. and Kelly, S. (2019). OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238. 10.1186/s13059-019-1832-y PubMed DOI PMC
Failler, M., Gee, H. Y., Krug, P., Joo, K., Halbritter, J., Belkacem, L., Filhol, E., Porath, J. D., Braun, D. A., Schueler, M.et al. (2014). Mutations of CEP83 Cause Infantile Nephronophthisis and Intellectual Disability. Am. J. Hum. Genet. 94, 905-914. 10.1016/j.ajhg.2014.05.002 PubMed DOI PMC
Florimond, C., Sahin, A., Vidilaseris, K., Dong, G., Landrein, N., Dacheux, D., Albisetti, A., Byard, E. H., Bonhivers, M. and Robinson, D. R. (2015). BILBO1 is a scaffold protein of the flagellar pocket collar in the pathogen Trypanosoma brucei. PLoS Pathog. 11, e1004654. 10.1371/journal.ppat.1004654 PubMed DOI PMC
Focşa, I. O., Budişteanu, M. and Bălgrădean, M. (2021). Clinical and genetic heterogeneity of primary ciliopathies (Review). Int. J. Mol. Med. 48, 176. 10.3892/ijmm.2021.5009 PubMed DOI PMC
Fong, C. S., Kim, M., Yang, T. T., Liao, J.-C. and Tsou, M.-F. B. (2014). SAS-6 assembly templated by the lumen of cartwheel-less centrioles precedes centriole duplication. Dev. Cell 30, 238-245. 10.1016/j.devcel.2014.05.008 PubMed DOI PMC
Gluenz, E., Povelones, M. L., Englund, P. T. and Gull, K. (2011). The kinetoplast duplication cycle in Trypanosoma brucei is orchestrated by cytoskeleton-mediated cell morphogenesis. Mol. Cell. Biol. 31, 1012-1021. 10.1128/MCB.01176-10 PubMed DOI PMC
Gorilak, P., Pružincová, M., Vachova, H., Olšinová, M., Schmidt Cernohorska, M. and Varga, V. (2021). Expansion microscopy facilitates quantitative super-resolution studies of cytoskeletal structures in kinetoplastid parasites. Open Biol. 11, 210131. 10.1098/rsob.210131 PubMed DOI PMC
Harmer, J., Qi, X., Toniolo, G., Patel, A., Shaw, H., Benson, F. E., Ginger, M. L. and McKean, P. G. (2017). Variation in basal body localisation and targeting of trypanosome RP2 and FOR20 proteins. Protist 168, 452-466. 10.1016/j.protis.2017.07.002 PubMed DOI
Hodges, M. E., Scheumann, N., Wickstead, B., Langdale, J. A. and Gull, K. (2010). Reconstructing the evolutionary history of the centriole from protein components. J. Cell Sci. 123, 1407-1413. 10.1242/jcs.064873 PubMed DOI PMC
Hou, Y., Zheng, S., Wu, Z., Augière, C., Morel, V., Cortier, E., Duteyrat, J.-L., Zhang, Y., Chen, H., Peng, Y.et al. (2023). Drosophila transition fibers are essential for IFT-dependent ciliary elongation but not basal body docking and ciliary budding. Curr. Biol. 33, 727-736.e6. 10.1016/j.cub.2022.12.046 PubMed DOI
Hu, H., Liu, Y., Zhou, Q., Siegel, S. and Li, Z. (2015). The centriole cartwheel protein SAS-6 in Trypanosoma brucei is required for probasal body biogenesis and flagellum assembly. Eukaryot. Cell 14, 898-907. 10.1128/EC.00083-15 PubMed DOI PMC
Inoue, M., Nakamura, Y., Yasuda, K., Yasaka, N., Hara, T., Schnaufer, A., Stuart, K. and Fukuma, T. (2005). The 14-3-3 proteins of Trypanosoma brucei function in motility, cytokinesis, and cell cycle. J. Biol. Chem. 280, 14085-14096. 10.1074/jbc.M412336200 PubMed DOI
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A.et al. (2021). Highly accurate protein structure prediction with AlphaFold. Nature 596, 583-589. 10.1038/s41586-021-03819-2 PubMed DOI PMC
Kabsch, W. and Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637. 10.1002/bip.360221211 PubMed DOI
Kalichava, A. and Ochsenreiter, T. (2021). Ultrastructure expansion microscopy in Trypanosoma brucei. Open Biol. 11, 210132. 10.1098/rsob.210132 PubMed DOI PMC
Kilmartin, J. V., Wright, B. and Milstein, C. (1982). Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J. Cell Biol. 93, 576-582. 10.1083/jcb.93.3.576 PubMed DOI PMC
Kumar, D., Rains, A., Herranz-Pérez, V., Lu, Q., Shi, X., Swaney, D. L., Stevenson, E., Krogan, N. J., Huang, B., Westlake, C.et al. (2021). A ciliopathy complex builds distal appendages to initiate ciliogenesis. J. Cell Biol. 220, e202011133. 10.1083/jcb.202011133 PubMed DOI PMC
Kurtulmus, B., Yuan, C., Schuy, J., Neuner, A., Hata, S., Kalamakis, G., Martin-Villalba, A. and Pereira, G. (2018). LRRC45 contributes to early steps of axoneme extension. J. Cell Sci. 131, jcs223594. 10.1242/jcs.223594 PubMed DOI
Langousis, G., Cavadini, S., Boegholm, N., Lorentzen, E., Kempf, G. and Matthias, P. (2022). Structure of the ciliogenesis-associated CPLANE complex. Sci. Adv. 8, eabn0832. 10.1126/sciadv.abn0832 PubMed DOI PMC
Marshall, W. F. and Rosenbaum, J. L. (2001). Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J. Cell Biol. 155, 405-414. 10.1083/jcb.200106141 PubMed DOI PMC
McCulloch, R., Vassella, E., Burton, P., Boshart, M. and Barry, J. D. (2004). Transformation of monomorphic and pleomorphic Trypanosoma brucei. Methods Mol. Biol. 262, 53-86. 10.1385/1-59259-761-0:053 PubMed DOI
Moran, J., McKean, P. G. and Ginger, M. L. (2014). Eukaryotic flagella: variations in form, function, and composition during evolution. Bioscience 64, 1103-1114. 10.1093/biosci/biu175 DOI
Nakazawa, Y., Hiraki, M., Kamiya, R. and Hirono, M. (2007). SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr. Biol. 17, 2169-2174. 10.1016/j.cub.2007.11.046 PubMed DOI
Nishijima Y., Hagiya, Y., Kubo, T., Takei, R., Katoh, Y. and Nakayama, K. (2017). RABL2 interacts with the intraflagellar transport-B complex and CEP19 and participates in ciliary assembly. Mol. Biol. Cell 28, 1652-1666. 10.1091/mbc.E17-01-0017 PubMed DOI PMC
O'Hara, P. T. (1970). Spiral tilt of triplet fibers in human leukocyte centrioles. J. Ultrastruct. Res. 31, 195-198. 10.1016/s0022-5320(70)90154-1 PubMed DOI
Poon, S. K., Peacock, L., Gibson, W., Gull, K. and Kelly, S. (2012). A modular and optimized single marker system for generating Trypanosoma brucei cell lines expressing T7 RNA polymerase and the tetracycline repressor. Open Biol. 2, 110037. 10.1098/rsob.110037 PubMed DOI PMC
Ramanantsalama, M. R., Landrein, N., Casas, E., Salin, B., Blancard, C., Bonhivers, M., Robinson, D. R. and Dacheux, D. (2022). TFK1, a basal body transition fibre protein that is essential for cytokinesis in Trypanosoma brucei. J. Cell Sci. 135, jcs259893. 10.1242/jcs.259893 PubMed DOI
Redmond, S., Vadivelu, J. and Field, M. C. (2003). RNAit: an automated web-based tool for the selection of RNAi targets in Trypanosoma brucei. Mol. Biochem. Parasitol. 128, 115-118. 10.1016/s0166-6851(03)00045-8 PubMed DOI
Schmidt, K. N., Kuhns, S., Neuner, A., Hub, B., Zentgraf, H. and Pereira, G. (2012). Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J. Cell Biol. 199, 1083-1101. 10.1083/jcb.201202126 PubMed DOI PMC
Sherwin, T. and Gull, K. (1989). The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philos. Trans. R. Soc. Lond. B Biol. Sci. 323, 573-588. 10.1098/rstb.1989.0037 PubMed DOI
Stephan, A., Vaughan, S., Shaw, M. K., Gull, K. and McKean, P. G. (2007). An essential quality control mechanism at the eukaryotic basal body prior to intraflagellar transport. Traffic 8, 1323-1330. 10.1111/j.1600-0854.2007.00611.x PubMed DOI
Tanos, B. E., Yang, H.-J., Soni, R., Wang, W.-J., Macaluso, F. P., Asara, J. M. and Tsou, M.-F. B. (2013). Centriole distal appendages promote membrane docking, leading to cilia initiation. Genes Dev. 27, 163-168. 10.1101/gad.207043.112 PubMed DOI PMC
Tischer, J., Carden, S. and Gergely, F. (2021). Accessorizing the centrosome: new insights into centriolar appendages and satellites. Curr. Opin. Struct. Biol. 66, 148-155. 10.1016/j.sbi.2020.10.021 PubMed DOI
Trépout, S., Tassin, A.-M., Marco, S. and Bastin, P. (2018). STEM tomography analysis of the trypanosome transition zone. J. Struct. Biol. 202, 51-60. 10.1016/j.jsb.2017.12.005 PubMed DOI
van Kempen, M., Kim, S. S., Tumescheit, C., Mirdita, M., Lee, J., Gilchrist, C. L. M., Söding, J. and Steinegger, M. (2024). Fast and accurate protein structure search with Foldseek. Nat. Biotechnol. 42, 243-246. 10.1038/s41587-023-01773-0 PubMed DOI PMC
Wei, Q., Ling, K. and Hu, J. (2015). The essential roles of transition fibers in the context of cilia. Curr. Opin. Cell Biol. 35, 98-105. 10.1016/j.ceb.2015.04.015 PubMed DOI PMC
Wheeler, R. J. (2021). A resource for improved predictions of Trypanosoma and Leishmania protein three-dimensional structure. PLoS One, 16, e0259871. 10.1371/journal.pone.0259871 PubMed DOI PMC
Wheeler, R. J., Gull, K. and Sunter, J. D. (2019). Coordination of the cell cycle in trypanosomes. Annu. Rev. Microbiol. 73, 133-154. 10.1146/annurev-micro-020518-115617 PubMed DOI
Wilson, D., Pethica, R., Zhou, Y., Talbot, C., Vogel, C., Madera, M., Chothia, C. and Gough, J. (2009). SUPERFAMILY--sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res. 37, D380-D386. 10.1093/nar/gkn762 PubMed DOI PMC
Woodward, R., Carden, M. J. and Gull, K. (1995). Immunological characterization of cytoskeletal proteins associated with the basal body, axoneme and flagellum attachment zone of Trypanosoma brucei. Parasitology 111, 77-85. 10.1017/s0031182000064623 PubMed DOI
Yang, T. T., Chong, W. M., Wang, W.-J., Mazo, G., Tanos, B., Chen, Z., Tran, T. M. N., Chen, Y.-D., Weng, R. R., Huang, C.-E.et al. (2018). Super-resolution architecture of mammalian centriole distal appendages reveals distinct blade and matrix functional components. Nat. Commun. 9, 2023. 10.1038/s41467-018-04469-1 PubMed DOI PMC
Zhou, Q., Lee, K. J., Kurasawa, Y., Hu, H., An, T. and Li, Z. (2018). Faithful chromosome segregation in Trypanosoma brucei requires a cohort of divergent spindle-associated proteins with distinct functions. Nucleic Acids Res. 46, 8216-8231. 10.1093/nar/gky557 PubMed DOI PMC