Scaffolding function of the chlamydomonas procentriole protein CRC70, a member of the conserved cep70 family

Journal of Cell Science

Volumn 124, Issue 17, 2011, Pages 2964-2975

  Shiratsuchi, Gen ^a   Kamiya, Ritsu ^a   Hirono, Masafumi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Basal body; Bld10; Bld12; Cartwheel; Centriole; SAS 6

Indexed keywords

CYTOPLASM PROTEIN; PROTEIN CRC70; PROTOZOAL PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN 3T3; CENTRIOLE; CHLAMYDOMONAS; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE SILENCING; MICROTUBULE ASSEMBLY; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; RNA INTERFERENCE;

AMINO ACID SEQUENCE; ANIMALS; CENTRIOLES; CHLAMYDOMONAS; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; MICE; MICROSCOPY, ELECTRON; MICROTUBULES; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PLANT PROTEINS; RNA INTERFERENCE; TRANSFECTION;

CHLAMYDOMONAS; MAMMALIA;

EID: 80054018263     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.084715     Document Type: Article

References (58)

1. Andersen, J. S., Wilkinson, C. J., Mayor, T., Mortensen, P., Nigg, E. A. and Mann, M. (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574.
2. Azimzadeh, J. and Bornens, M. (2007). Structure and duplication of the centrosome. J. Cell Sci. 120, 2139-2142.
3. Berger, B., Wilson, D. B., Wolf, E., Tonchev, T., Milla, M. and Kim, P. S. (1995). Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. USA 92, 8259-8263.
4. Dammermann, A., Muller-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.
5. Delattre, M., Leidel, S., Wani, K., Baumer, K., Bamat, J., Schnabel, H., Feichtinger, R., Schnabel, R. and Gönczy, P. (2004). Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat. Cell Biol. 6, 656-664.
6. Dippell, R. V. (1968). The development of basal bodies in paramecium. Proc. Natl. Acad. Sci. USA 61, 461-468.
7. Dutcher, S. K. (2007). Finding treasures in frozen cells: new centriole intermediates. BioEssays 29, 630-634.
8. Dutcher, S. K., Morrissette, N. S., Preble, A. M., Rackley, C. and Stanga, J. (2002). e{open}-tubulin is an essential component of the centriole. Mol. Biol. Cell 13, 3859-3869.
9. Ehler, L. L., Holmes, J. A. and Dutcher, S. K. (1995). Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. Genetics 141, 945-960.
10. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
11. Fry, A. M., Mayor, T., Meraldi, P., Stierhof, Y. D., Tanaka, K. and Nigg, E. A. (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell. Biol. 141, 1563-1574.
12. Gaffal, K. P. (1988). The basal body-root complex of Chlamydomonas reinhardtii during mitosis. Protoplasma 143, 118-129.
13. 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.
14. Goodenough, U. W. and St. Clair, H. S. (1975). BALD-2: a mutation affecting the formation of doublet and triplet sets of microtubules in Chlamydomonas reinhardtii. J. Cell Biol. 66, 480-491.
15. Gorman, D. S. and Levine, R. P. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 54, 1665-1669.
16. Harris, E. H. (1989). The Chlamydomonas Sourcebook. San Diego: Academic Press, 780.
17. Higuchi, R., Dollinger, G., Walsh, P. S. and Griffith, R. (1992). Simultaneous amplification and detection of specific DNA sequences. Biotechnology 10, 413-417.
18. Higuchi, R., Fockler, C., Dollinger, G. and Watson, R. (1993). Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology 11, 1026-1030.
19. Hiraki, M., Nakazawa, Y., Kamiya, R. and Hirono, M. (2007). Bld10p constitutes the Cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr. Biol. 17, 1778-1783.
20. Holmes, J. A. and Dutcher, S. K. (1989). Cellular asymmetry in Chlamydomonas reinhardtii. J. Cell Sci. 94, 273-285.
21. Huang, B., Ramanis, Z., Dutcher, S. K. and Luck, D. J. (1982). Uniflagellar mutants of Chlamydomonas: evidence for the role of basal bodies in transmission of positional information. Cell 29, 745-753.
22. Ishikawa, H., Kubo, A., Tsukita, S. and Tsukita, S. (2005). Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat. Cell Biol. 7, 517-524.
23. Kathir, P., LaVoie, M., Brazelton, W. J., Haas, N. A., Lefebvre, P. A. and Silflow, C. D. (2003). Molecular map of the Chlamydomonas reinhardtii nuclear genome. Eukaryot. Cell 2, 362-379.
24. Keller, L. C., Romijn, E. P., Zamora, I., Yates, J. R., 3rd and Marshall, W. F. (2005). Proteomic analysis of isolated Chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr. Biol. 15, 1090-1098.
25. Kemp, C. A., Kopish, K. R., Zipperlen, P., Ahringer, J. and O'Connell, K. F. (2004). Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev. Cell 6, 511-523.
26. 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.
27. 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.
28. Koblenz, B., Schoppmeier, J., Grunow, A. and Lechtreck, K. F. (2003). Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation. J. Cell Sci. 116, 2635-2646.
29. Lechtreck, K. F. and Geimer, S. (2000). Distribution of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil. Cytoskeleton 47, 219-235.
30. Leidel, S., Delattre, M., Cerutti, L., Baumer, K. and Gönczy, P. (2005). SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat. Cell Biol. 7, 115-125.
31. Li, J. B., Gerdes, J. M., Haycraft, C. J., Fan, Y., Teslovich, T. M., May-Simera, H., Li, H., Blacque, O. E., Li, L., Leitch, C. C. et al. (2004). Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117, 541-552.
32. Marshall, W. F., Vucica, Y. and Rosenbaum, J. L. (2001). Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication. Curr. Biol. 11, 308-317.
33. Matsuura, K., Lefebvre, P. A., Kamiya, R. and Hirono, M. (2002). Kinesin-II is not essential for mitosis and cell growth in Chlamydomonas. Cell Motil. Cytoskeleton 52, 195-201.
34. Matsuura, K., Lefebvre, P. A., Kamiya, R. and Hirono, M. (2004). Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly. J. Cell Biol. 165, 663-671.
35. Molnar, A., Bassett, A., Thuenemann, E., Schwach, F., Karkare, S., Ossowski, S., Weigel, D. and Baulcombe, D. (2009). Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J. 58, 165-174.
36. Myers, T. W. and Gelfand, D. H. (1991). Reverse transcription and DNA amplification by a Thermus thermophilus DNA polymerase. Biochemistry 30, 7661-7666.
37. Nakagawa, Y., Yamane, Y., Okanoue, T., Tsukita, S. and Tsukita, S. (2001). Outer dense fiber 2 is a widespread centrosome scaffold component preferentially associated with mother centrioles: its identification from isolated centrosomes. Mol. Biol. Cell 12, 1687-1697.
38. 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.
39. Neumann, B., Walter, T., Hériché, J. K., Bulkescher, J., Erfle, H., Conrad, C., Rogers, P., Poser, I., Held, M., Liebel, U. et al. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727.
40. Neupert, J., Karcher, D. and Bock, R. (2009). Generation of Chlamydomonas strains that efficiently express nuclear transgenes. Plant J. 57, 1140-1150.
41. Nigg, E. A. (2004). A proteomic approach to the inventory of the human centrosome. In Centrosomes in Development and Disease (ed. E. Nigg), p. 125. Weinheim: Wiley-VCH.
42. O'Connell, K. F., Caron, C., Kopish, K. R., Hurd, D. D., Kemphues, K. J., Li, Y. and White, J. G. (2001). The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105, 547-558.
43. O'Toole, E. T., Giddings, T. H., McIntosh, J. R. and Dutcher, S. K. (2003). Three-dimensional organization of basal bodies from wild-type and δ-tubulin deletion strains of Chlamydomonas reinhardtii. Mol. Biol. Cell 14, 2999-3012.
44. Olmsted, J. B. (1981). Affinity purification of antibodies from diazotized paper bots of heterogeneous protein samples. J. Biol. Chem. 256, 11955-11957.
45. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J. L. and Bornens, M. (1996). Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109, 3089-3102.
46. Pelletier, L., Ozlü, N., Hannak, E., Cowan, C., Habermann, B., Ruer, M., Müller-Reichert, T. and Hyman, A. A. (2004). The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr. Biol. 14, 863-873.
47. Perrière, G. and Gouy, M. (1996). WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie 78, 364-369.
48. Piasecki, B. P., LaVoie, M., Tam, L. W., Lefebvre, P. A. and Silflow, C. D. (2008). The Uni2 phosphoprotein is a cell cycle regulated component of the basal body maturation pathway in Chlamydomonas reinhardtii. Mol. Biol. Cell 19, 262-273.
49. Rebhan, M., Chalifa-Caspi, V., Prilusky, J. and Lancet, D. (1998). GeneCards: a novel functional genomics compendium with automated data mining and query reformulation support. Bioinformatics 14, 656-664.
50. Schroda, M. (2006). RNA silencing in Chlamydomonas: mechanisms and tools. Curr. Genet. 49, 69-84.
51. Shimogawara, K., Fujiwara, S., Grossman, A. and Usuda, H. (1998). High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148, 1821-1828.
52. Silflow, C. D., LaVoie, M., Tam, L. W., Tousey, S., Sanders, M., Wu, W., Borodovsky, M. and Lefebvre, P. A. (2001). The Vfl1 protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of the basal bodies. J. Cell Biol. 153, 63-74.
53. Spudich, J. L. and Sager, R. (1980). Regulation of the Chlamydomonas cell cycle by light and dark. J. Cell Biol. 85, 136-145.
54. Strnad, P. and Gönczy, P. (2008). Mechanisms of procentriole formation. Trends Cell Biol. 18, 389-396.
55. Strnad, P., Leidel, S., Vinogradova, T., Euteneuer, U., Khodjakov, A. and Gönczy, P. (2007). Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell 13, 203-213.
56. Wilkinson, C. J., Carl, M. and Harris, W. A. (2009). Cep70 and Cep131 contribute to ciliogenesis in zebrafish embryos. BMC Cell Biol. 10, 17.
57. Wright, R. L., Salisbury, J. and Jarvlk, J. W. (1985). A nucleus-basal body connector in Chlamydomonas reinhardtii that may function in basal body localization or segregation. J. Cell Biol. 101, 1903-1912.
58. Zhao, T., Wang, W., Bai, X. and Qi, Y. (2009). Gene silencing by artificial microRNAs in Chlamydomonas. Plant J. 58, 157-164.