Basal Body Assembly in Ciliates: the Power of Numbers

Overview

Journal Traffic

Publisher Wiley

Specialties Biology
Physiology

Date 2009 Feb 5

PMID 19192246

Citations 30

Authors

Chad G Pearson

Mark Winey

Affiliations

Soon will be listed here.

Abstract

Centrioles perform the dual functions of organizing both centrosomes and cilia. The biogenesis of nascent centrioles is an essential cellular event that is tightly coupled to the cell cycle so that each cell contains only two or four centrioles at any given point in the cell cycle. The assembly of centrioles and their analogs, basal bodies, is well characterized at the ultrastructural level whereby structural modules are built into a functional organelle. Genetic studies in model organisms combined with proteomic, bioinformatic and identifying ciliary disease gene orthologs have revealed a wealth of molecules requiring further analysis to determine their roles in centriole duplication, assembly and function. Nonetheless, at this stage, our understanding of how molecular components interact to build new centrioles and basal bodies is limited. The ciliates, Tetrahymena and Paramecium, historically have been the subject of cytological and genetic study of basal bodies. Recent advances in the ciliate genetic and molecular toolkit have placed these model organisms in a favorable position to study the molecular mechanisms of centriole and basal body assembly.

Citing Articles

Mapping molecular complexes with super-resolution microscopy and single-particle analysis.

Mendes A, Heil H, Coelho S, Leterrier C, Henriques R Open Biol. 2022; 12(7):220079.

PMID: 35892200 PMC: 9326279. DOI: 10.1098/rsob.220079.

Poc5 is a transient basal body component that is important for basal body maturation.

Heydeck W, Bayless B, Stemm-Wolf A, OToole E, Fabritius A, Ozzello C J Cell Sci. 2020; 133(11).

PMID: 32350068 PMC: 7286293. DOI: 10.1242/jcs.240838.

Motile Cilia: Innovation and Insight From Ciliate Model Organisms.

Bayless B, Navarro F, Winey M Front Cell Dev Biol. 2019; 7:265.

PMID: 31737631 PMC: 6838636. DOI: 10.3389/fcell.2019.00265.

Polarity in Ciliate Models: From Cilia to Cell Architecture.

Soares H, Carmona B, Nolasco S, Viseu Melo L Front Cell Dev Biol. 2019; 7:240.

PMID: 31681771 PMC: 6813674. DOI: 10.3389/fcell.2019.00240.

Coupled Active Systems Encode an Emergent Hunting Behavior in the Unicellular Predator Lacrymaria olor.

Coyle S, Flaum E, Li H, Krishnamurthy D, Prakash M Curr Biol. 2019; 29(22):3838-3850.e3.

PMID: 31679941 PMC: 7511173. DOI: 10.1016/j.cub.2019.09.034.

References

Kann M, Soues S, Levilliers N, Fouquet J . Glutamylated tubulin: diversity of expression and distribution of isoforms. Cell Motil Cytoskeleton. 2003; 55(1):14-25. DOI: 10.1002/cm.10107. View

Rodrigues-Martins A, Bettencourt-Dias M, Riparbelli M, Ferreira C, Ferreira I, Callaini G . DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol. 2007; 17(17):1465-72. DOI: 10.1016/j.cub.2007.07.034. View

Ruiz F, Beisson J, Rossier J, Dupuis-Williams P . Basal body duplication in Paramecium requires gamma-tubulin. Curr Biol. 1999; 9(1):43-6. DOI: 10.1016/s0960-9822(99)80045-1. View

Shang Y, Li B, Gorovsky M . Tetrahymena thermophila contains a conventional gamma-tubulin that is differentially required for the maintenance of different microtubule-organizing centers. J Cell Biol. 2002; 158(7):1195-206. PMC: 2173235. DOI: 10.1083/jcb.200205101. View

Jerka-Dziadosz M . Cytoskeleton-related structures in tetrahymena thermophila: microfilaments at the apical and division-furrow rings. J Cell Sci. 1981; 51:241-53. DOI: 10.1242/jcs.51.1.241. View

Paoletti A, Bordes N, Haddad R, Schwartz C, Chang F, Bornens M . Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication. Mol Biol Cell. 2003; 14(7):2793-808. PMC: 165677. DOI: 10.1091/mbc.e02-10-0661. View

Grimes G, Gavin R . Ciliary protein conservation during development in the ciliated protozoan, Oxytricha. J Cell Biol. 1987; 105(6 Pt 1):2855-9. PMC: 2114741. DOI: 10.1083/jcb.105.6.2855. View

Beisson J, Clerot J, Garreau de Loubresse N, Ruiz F, Klotz C . Basal body-associated nucleation center for the centrin-based cortical cytoskeletal network in Paramecium. Protist. 2002; 152(4):339-54. DOI: 10.1078/1434-4610-00072. View

SOROKIN S . Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol. 1962; 15:363-77. PMC: 2106144. DOI: 10.1083/jcb.15.2.363. View

10.

Sorokin S . Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J Cell Sci. 1968; 3(2):207-30. DOI: 10.1242/jcs.3.2.207. View

11.

Salisbury J, Baron A, Surek B, Melkonian M . Striated flagellar roots: isolation and partial characterization of a calcium-modulated contractile organelle. J Cell Biol. 1984; 99(3):962-70. PMC: 2113404. DOI: 10.1083/jcb.99.3.962. View

12.

Bre M, de Nechaud B, Wolff A, Fleury A . Glutamylated tubulin probed in ciliates with the monoclonal antibody GT335. Cell Motil Cytoskeleton. 1994; 27(4):337-49. DOI: 10.1002/cm.970270406. View

13.

Shang Y, Tsao C, Gorovsky M . Mutational analyses reveal a novel function of the nucleotide-binding domain of gamma-tubulin in the regulation of basal body biogenesis. J Cell Biol. 2005; 171(6):1035-44. PMC: 2171320. DOI: 10.1083/jcb.200508184. View

14.

Iftode F, Fleury-Aubusson A . Structural inheritance in Paramecium: ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission. Biol Cell. 2003; 95(1):39-51. DOI: 10.1016/s0248-4900(03)00005-4. View

15.

Hiraki M, Nakazawa Y, Kamiya R, Hirono M . Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr Biol. 2007; 17(20):1778-83. DOI: 10.1016/j.cub.2007.09.021. View

16.

Tsou M, Stearns T . Controlling centrosome number: licenses and blocks. Curr Opin Cell Biol. 2005; 18(1):74-8. DOI: 10.1016/j.ceb.2005.12.008. View

17.

Avidor-Reiss T, Maer A, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S . Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell. 2004; 117(4):527-39. DOI: 10.1016/s0092-8674(04)00412-x. View

18.

Nilsson J, Williams N . An electron microscope study of the oral apparatus of Tetrahymena pyriformis. C R Trav Lab Carlsberg. 1966; 35(7):119-41. View

19.

Allen R . The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J Cell Biol. 1969; 40(3):716-33. PMC: 2107651. DOI: 10.1083/jcb.40.3.716. View

20.

Ruiz F, Garreau de Loubresse N, Klotz C, Beisson J, Koll F . Centrin deficiency in Paramecium affects the geometry of basal-body duplication. Curr Biol. 2005; 15(23):2097-106. DOI: 10.1016/j.cub.2005.11.038. View