Choosing sides - asymmetric centriole and basal body assembly

Journal of Cell Science

Volumn 127, Issue 13, 2014, Pages 2803-2810

  Pearson, Chad G ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Asymmetry; Basal body; Centriole; Pericentriolar material; Polarity

Indexed keywords

POLO LIKE KINASE; POLO LIKE KINASE 4; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MOTILITY; CENTRIOLE; CENTRIOLE AND BASAL BODY ASSEMBLY; CHLAMYDOMONAS; CILIATE; DAUGHTER CELL; DAUGHTER CENTRIOLE; ELECTRON MICROSCOPY; HUMAN; KINETOSOME; MICROTUBULE ASSEMBLY; MOTHER CENTRIOLE; NONHUMAN; PARAMECIUM; PERICENTRIOLAR REGION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTIST; SPINDLE POLE; TETRAHYMENA; ANIMAL; METABOLISM; MICROTUBULE;

ANIMALS; BASAL BODIES; CENTRIOLES; HUMANS; MICROTUBULES;

EID: 84903777108     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.151761     Document Type: Article

References (80)

1. Allen, R. D. (1969). The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J. Cell Biol. 40, 716-733.
2. Anderson, C. T. and Stearns, T. (2009). Centriole age underlies asynchronous primary cilium growth in mammalian cells. Curr. Biol. 19, 1498-1502.
3. Azimzadeh, J. and Marshall, W. F. (2010). Building the centriole. Curr. Biol. 20, R816-R825.
4. Backer, C. B., Gutzman, J. H., Pearson, C. G. and Cheeseman, I. M. (2012). CSAP localizes to polyglutamylated microtubules and promotes proper cilia function and zebrafish development. Mol. Biol. Cell 23, 2122-2130.
5. Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F. and Nigg, E. A. (2005). Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J. Cell Biol. 171, 27-33.
6. Beisson, J. (2008). Preformed cell structure and cell heredity. Prion 2, 1-8.
7. Beisson, J. and Jerka-Dziadosz, M. (1999). Polarities of the centriolar structure:morphogenetic consequences. Biol. Cell 91, 367-378.
8. Beisson, J. and Sonneborn, T. M. (1965). Cytoplasmic Inheritance of the Organization of the Cell Cortex in Paramecium Aurelia. Proc. Natl. Acad. Sci. USA 53, 275-282.
9. Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34.
10. Brito, D. A., Gouveia, S. M. and Bettencourt-Dias, M. (2012). Deconstructing the centriole: structure and number control. Curr. Opin. Cell Biol. 24, 4-13.
11. Carvalho-Santos, Z., Machado, P., Branco, P., Tavares-Cadete, F., Rodrigues-Martins, A., Pereira-Leal, J. B. and Bettencourt-Dias, M. (2010). Stepwise evolution of the centriole-assembly pathway. J. Cell Sci. 123, 1414-1426.
12. Cavalier-Smith, T. (1974). Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J. Cell Sci. 16, 529-556.
13. Conduit, P. T., Feng, Z., Richens, J. H., Baumbach, J., Wainman, A., Bakshi, S. D., Dobbelaere, J., Johnson, S., Lea, S. M. and Raff, J. W. (2014). The centrosome-specific phosphorylation of cnn by polo/plk1 drives cnn scaffold assembly and centrosome maturation. Dev. Cell 28, 659-669.
14. Dammermann, A., Müller-Reichert, T., Pelletier, L., Habermann, B., Desai, A. and Oegema, K. (2004). Centriole assembly requires both centriolar and pericentriolar material proteins. Dev. Cell 7, 815-829.
15. Dantas, T. J., Daly, O. M. and Morrison, C. G. (2012). Such small hands: the roles of centrins/caltractins in the centriole and in genome maintenance. Cell. Mol. Life Sci. 69, 2979-2997.
16. Dippell, R. V. (1968). The development of basal bodies in paramecium. Proc. Natl. Acad. Sci. USA 61, 461-468.
17. Dutcher, S. K. (2007). Finding treasures in frozen cells: new centriole intermediates. Bioessays 29, 630-634.
18. Dutcher, S. K. (2013). The awesome power of dikaryons for studying flagella and basal bodies in Chlamydomonas reinhardtii. Cytoskeleton (Hoboken) 71, 79-94.
19. Feldman, J. L., Geimer, S. and Marshall, W. F. (2007). The mother centriole plays an instructive role in defining cell geometry. PLoS Biol. 5, e149.
20. Frankel, J. (1989). Pattern Formation: Ciliate Studies and Models. Oxford: Oxford University Press.
21. Fu, J. and Glover, D. M. (2012). Structured illumination of the interface between centriole and peri-centriolar material. Open Biol. 2, 120104.
22. Geimer, S. and Melkonian, M. (2004). The ultrastructure of the Chlamydomonas reinhardtii basal apparatus: identification of an early marker of radial asymmetry inherent in the basal body. J. Cell Sci. 117, 2663-2674.
23. Goetz, S. C. and Anderson, K. V. (2010). The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344.
24. Gönczy, P. (2012). Towards a molecular architecture of centriole assembly. Nat. Rev. Mol. Cell Biol. 13, 425-435.
25. Guichard, P., Chrétien, D., Marco, S. and Tassin, A. M. (2010). Procentriole assembly revealed by cryo-electron tomography. EMBO J. 29, 1565-1572.
26. 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.
27. Holmes, J. A. and Dutcher, S. K. (1989). Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94, 273-285.
28. Iftode, F. and Fleury-Aubusson, A. (2003). Structural inheritance in Paramecium:ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission. Biol. Cell 95, 39-51.
29. Jana, S. C., Marteil, G. and Bettencourt-Dias, M. (2014). Mapping molecules to structure: unveiling secrets of centriole and cilia assembly with near-atomic resolution. Curr. Opin. Cell Biol. 26, 96-106.
30. Jerka-Dziadosz, M., Jenkins, L. M., Nelsen, E. M., Williams, N. E., Jaeckel-Williams, R. and Frankel, J. (1995). Cellular polarity in ciliates: persistence of global polarity in a disorganized mutant of Tetrahymena thermophila that disrupts cytoskeletal organization. Dev. Biol. 169, 644-661.
31. Jerka-Dziadosz, M., Koll, F., Włoga, D., Gogendeau, D., Garreau de Loubresse, N., Ruiz, F., Fabczak, S. and Beisson, J. (2013). A Centrin3-dependent, transient, appendage of the mother basal body guides the positioning of the daughter basal body in Paramecium. Protist 164, 352-368.
32. Khodjakov, A., Rieder, C. L., Sluder, G., Cassels, G., Sibon, O. and Wang, C. L. (2002). De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 158, 1171-1181.
33. Kilburn, C. L., Pearson, C. G., Romijn, E. P., Meehl, J. B., Giddings, T. H., Jr, Culver, B. P., Yates, J. R., 3rd and Winey, M. (2007). New Tetrahymena basal body protein components identify basal body domain structure. J. Cell Biol. 178, 905-912.
34. Kilmartin, J. V. (2003). Sfi1p has conserved centrin-binding sites and an essential function in budding yeast spindle pole body duplication. J. Cell Biol. 162, 1211-1221.
35. Kim, T. S., Park, J. E., Shukla, A., Choi, S., Murugan, R. N., Lee, J. H., Ahn, M., Rhee, K., Bang, J. K., Kim, B. Y. et al. (2013). Hierarchical recruitment of Plk4 and regulation of centriole biogenesis by two centrosomal scaffolds, Cep192 and Cep152. Proc. Natl. Acad. Sci. USA 110, E4849-E4857.
36. Kirschner, M., Gerhart, J. and Mitchison, T. (2000). Molecular ''vitalism''. Cell 100, 79-88.
37. Klos Dehring, D. A., Vladar, E. K., Werner, M. E., Mitchell, J. W., Hwang, P. and Mitchell, B. J. (2013). Deuterosome-mediated centriole biogenesis. Dev. Cell 27, 103-112.
38. Kochanski, R. S. and Borisy, G. G. (1990). Mode of centriole duplication and distribution. J. Cell Biol. 110, 1599-1605.
39. Lange, B. M. and Gull, K. (1995). A molecular marker for centriole maturation in the mammalian cell cycle. J. Cell Biol. 130, 919-927.
40. Lawo, S., Hasegan, M., Gupta, G. D. and Pelletier, L. (2012). Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat. Cell Biol. 14, 1148-1158.
41. Lechtreck, K. F. and Grunow, A. (1999). Evidence for a direct role of nascent basal bodies during spindle pole initiation in the green alga Spermatozopsis similis. Protist 150, 163-181.
42. Lechtreck, K. F. and Melkonian, M. (1991). Striated microtubule-associated fibers: identification of assemblin, a novel 34-kD protein that forms paracrystals of 2-nm filaments in vitro. J. Cell Biol. 115, 705-716.
43. Lee, K. and Rhee, K. (2012). Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis. Cell Cycle 11, 2476-2485.
44. Lin, Y. C., Chang, C. W., Hsu, W. B., Tang, C. J., Lin, Y. N., Chou, E. J., Wu, C. T. and Tang, T. K. (2013). Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J. 32, 1141-1154.
45. Loncarek, J., Hergert, P., Magidson, V. and Khodjakov, A. (2008). Control of daughter centriole formation by the pericentriolar material. Nat. Cell Biol. 10, 322-328.
46. Lüders, J. (2012). The amorphous pericentriolar cloud takes shape. Nat. Cell Biol. 14, 1126-1128.
47. Mardin, B. R. and Schiebel, E. (2012). Breaking the ties that bind: new advances in centrosome biology. J. Cell Biol. 197, 11-18.
48. Mardin, B. R., Lange, C., Baxter, J. E., Hardy, T., Scholz, S. R., Fry, A. M. and Schiebel, E. (2010). Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction. Nat. Cell Biol. 12, 1166-1176.
49. Marshall, W. F. (2012). Centriole asymmetry determines algal cell geometry. Curr. Opin. Plant Biol. 15, 632-637.
50. Matsuo, K., Ohsumi, K., Iwabuchi, M., Kawamata, T., Ono, Y. and Takahashi, M. (2012). Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr. Biol. 22, 915-921.
51. Megraw, T. L., Li, K., Kao, L. R. and Kaufman, T. C. (1999). The centrosomin protein is required for centrosome assembly and function during cleavage in Drosophila. Development 126, 2829-2839.
52. Mennella, V., Keszthelyi, B., McDonald, K. L., Chhun, B., Kan, F., Rogers, G. C., Huang, B. and Agard, D. A. (2012). Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14, 1159-1168.
53. Mennella, V., Agard, D. A., Huang, B. and Pelletier, L. (2013). Amorphous no more: subdiffraction view of the pericentriolar material architecture. Trends Cell Biol.
54. Munn, E. A. (1970). Fine structure of basal bodies (kinetosomes) and associated components of Tetrahymena. Tissue Cell 2, 499-512.
55. Nakamura, A., Arai, H. and Fujita, N. (2009). Centrosomal Aki1 and cohesin function in separase-regulated centriole disengagement. J. Cell Biol. 187, 607-614.
56. Ng, S. F. and Frankel, J. (1977). 180 degrees rotation of ciliary rows and its morphogenetic implications in Tetrahymena pyriformis. Proc. Natl. Acad. Sci. USA 74, 1115-1119.
57. Nigg, E. A. and Stearns, T. (2011). The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160.
58. O'Toole, E. T. and Dutcher, S. K. (2013). Site-specific basal body duplication in Chlamydomonas. Cytoskeleton 71, 108-118.
59. Palazzo, R. E., Vogel, J. M., Schnackenberg, B. J., Hull, D. R. and Wu, X. (1999). Centrosome maturation. Curr. Top. Dev. Biol. 49, 449-470.
60. Pazour, G. J. and Witman, G. B. (2003). The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15, 105-110.
61. Pearson, C. G. and Winey, M. (2009). Basal body assembly in ciliates: the power of numbers. Traffic 10, 461-471.
62. Pearson, C. G., Giddings, T. H., Jr and Winey, M. (2009). Basal body components exhibit differential protein dynamics during nascent basal body assembly. Mol. Biol. Cell 20, 904-914.
63. Pelletier, L. and Yamashita, Y. M. (2012). Centrosome asymmetry and inheritance during animal development. Curr. Opin. Cell Biol. 24, 541-546.
64. Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. and Bornens, M. (2000). The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-330.
65. Ruiz, F., Beisson, J., Rossier, J. and Dupuis-Williams, P. (1999). Basal body duplication in Paramecium requires gamma-tubulin. Curr. Biol. 9, 43-46.
66. Ruiz, F., Garreau de Loubresse, N., Klotz, C., Beisson, J. and Koll, F. (2005). Centrin deficiency in Paramecium affects the geometry of basal-body duplication. Curr. Biol. 15, 2097-2106.
67. Sandoz, D. and Biosvieux-Ulrich, E. (1976). [Ciliogenesis in the mucous cells of the quail oviduct. I. Ultrastructural study in the laying quail]. J. Cell Biol. 71, 449-459.
68. Schöckel, L., Möckel, M., Mayer, B., Boos, D. and Stemmann, O. (2011). Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat. Cell Biol. 13, 966-972.
69. Shang, Y., Li, B. and Gorovsky, M. A. (2002). Tetrahymena thermophila contains a conventional gamma-tubulin that is differentially required for the maintenance of different microtubule-organizing centers. J. Cell Biol. 158, 1195-1206.
70. Sir, J. H., Pütz, M., Daly, O., Morrison, C. G., Dunning, M., Kilmartin, J. V. and Gergely, F. (2013). Loss of centrioles causes chromosomal instability in vertebrate somatic cells. J. Cell Biol. 203, 747-756.
71. Sonneborn, T. M. (1964). The Determinants and Evolution of Life. The Differentiation of Cells. Proc. Natl. Acad. Sci. USA 51, 915-929.
72. Sonnen, K. F., Schermelleh, L., Leonhardt, H. and Nigg, E. A. (2012). 3Dstructured illumination microscopy provides novel insight into architecture of human centrosomes. Biol. Open 1, 965-976.
73. Sperling, L., Keryer, G., Ruiz, F. and Beisson, J. (1991). Cortical morphogenesis in Paramecium: a transcellular wave of protein phosphorylation involved in ciliary rootlet disassembly. Dev. Biol. 148, 205-218.
74. Stemm-Wolf, A. J., Morgan, G., Giddings, T. H., Jr, White, E. A., Marchione, R., McDonald, H. B. and Winey, M. (2005). Basal body duplication and maintenance require one member of the Tetrahymena thermophila centrin gene family. Mol. Biol. Cell 16, 3606-3619.
75. Stemm-Wolf, A. J., Meehl, J. B. and Winey, M. (2013). Sfr13, a member of a large family of asymmetrically localized Sfi1-repeat proteins, is important for basal body separation and stability in Tetrahymena thermophila. J. Cell Sci. 126, 1659-1671.
76. Tsou, M. F. and Stearns, T. (2006). Mechanism limiting centrosome duplication to once per cell cycle. Nature 442, 947-951.
77. Tsou, M. F., Wang, W. J., George, K. A., Uryu, K., Stearns, T. and Jallepalli, P. V. (2009). Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev. Cell 17, 344-354.
78. Vorobjev, I. A. and Chentsov, Y. S. (1980). The ultrastructure of centriole in mammalian tissue culture cells. Cell Biol. Int. Rep. 4, 1037-1044.
79. Wloga, D. and Frankel, J. (2012). From molecules to morphology: cellular organization of Tetrahymena thermophila. Methods Cell Biol. 109, 83-140.
80. Zhao, H., Zhu, L., Zhu, Y., Cao, J., Li, S., Huang, Q., Xu, T., Huang, X., Yan, X. and Zhu, X. (2013). The Cep63 paralogue Deup1 enables massive de novo centriole biogenesis for vertebrate multiciliogenesis. Nat. Cell Biol. 15, 1434-1444.