Sfr13, a member of a large family of asymmetrically localized Sfi1-repeat proteins, is important for basal body separation and stability in Tetrahymena thermophila

Journal of Cell Science

Volumn 126, Issue 7, 2013, Pages 1659-1671

  Stemm Wolf, Alexander J ^a   Meehl, Janet B ^a   Winey, Mark ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Asymmetry; Basal body; Centrin; Sfi1 repeat

Indexed keywords

CENTRIN; PEPTIDES AND PROTEINS; PROTEIN SFI1; PROTEIN SFR13; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; GENE DELETION; KINETOSOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; TETRAHYMENA THERMOPHILA;

ASYMMETRY; BASAL BODY; CENTRIN; SFI1-REPEAT;

CENTRIOLES; PROTOZOAN PROTEINS; TETRAHYMENA THERMOPHILA;

EID: 84877979676     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.120238     Document Type: Article

References (87)

1. Abal, M., Keryer, G. and Bornens, M. (2005). Centrioles resist forces applied on centrosomes during G2/M transition. Biol. Cell 97, 425-434.
2. 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.
3. Aufderheide, K. J., Frankel, J. and Williams, N. E. (1980). Formation and positioning of surface-related structures in protozoa. Microbiol. Rev. 44, 252-302.
4. 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.
5. Badano, J. L., Mitsuma, N., Beales, P. L. and Katsanis, N. (2006). The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148.
6. Baker, K. and Beales, P. L. (2009). Making sense of cilia in disease: the human ciliopathies. Am. J. Med. Genet. C. Semin. Med. Genet. 151C, 281-295.
7. Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods, C. G., Khodjakov, A. and Raff, J. W. (2006). Flies without centrioles. Cell 125, 1375-1386.
8. Bayless, B. A., Giddings, T. H., Jr, Winey, M. and Pearson, C. G. (2012). Bld10/ Cep135 stabilizes basal bodies to resist cilia-generated forces. Mol. Biol. Cell 23, 4820-4832.
9. Beisson, J. and Jerka-Dziadosz, M. (1999). Polarities of the centriolar structure: morphogenetic consequences. Biol. Cell 91, 367-378.
10. 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.
11. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. and Godinho, S. A. (2011). Centrosomes and cilia in human disease. Trends Genet. 27, 307-315.
12. Bobinnec, Y., Khodjakov, A., Mir, L. M., Rieder, C. L., Eddé, B. and Bornens, M. (1998). Centriole disassembly in vivo and its effect on centrosome structure and function in vertebrate cells. J. Cell Biol. 143, 1575-1589.
13. Bozzone, D. M. (2000). Investigating phagocytosis in "Tetrahymena": an experimental system suitable for introductory and advanced instruction. Am. Biol. Teach. 62, 136-139.
14. Bruns, P. J. and Cassidy-Hanley, D. (1999). Biolistic transformation of macro- and micronuclei. Methods Cell Biol. 62, 501-512.
15. 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.
16. Chen, L. and Madura, K. (2008). Centrin/Cdc31 is a novel regulator of protein degradation. Mol. Cell. Biol. 28, 1829-1840.
17. Chevenet, F., Brun, C., Bañuls, A.-L., Jacq, B. and Christen, R. (2006). TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7, 439.
18. Crooks, G. E., Hon, G., Chandonia, J.-M. and Brenner, S. E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
19. Day, R. N. and Davidson, M. W. (2009). The fluorescent protein palette: tools for cellular imaging. Chem. Soc. Rev. 38, 2887-2921.
20. Delaval, B., Covassin, L., Lawson, N. D. and Doxsey, S. (2011). Centrin depletion causes cyst formation and other ciliopathy-related phenotypes in zebrafish. Cell Cycle 10, 3964-3972.
21. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M. et al. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, W465-W469.
22. Dippell, R. V. (1968). The development of basal bodies in Paramecium. Proc. Natl. Acad. Sci. USA 61, 461-468.
23. Doxsey, S. (2001). Re-evaluating centrosome function. Nat. Rev. Mol. Cell Biol. 2, 688-698.
24. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797.
25. Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J. R., Badger, J. H., Ren, Q., Amedeo, P., Jones, K. M. et al. (2006). Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4, e286.
26. Finn, R. D., Clements, J. and Eddy, S. R. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39 Suppl. 2, W29-W37.
27. Fischer, T., Rodri{dotless}́guez-Navarro, S., Pereira, G., Rácz, A., Schiebel, E. and Hurt, E. (2004). Yeast centrin Cdc31 is linked to the nuclear mRNA export machinery. Nat. Cell Biol. 6, 840-848.
28. Frankel, J. (1999). Cell biology of Tetrahymena thermophila. Methods Cell Biol. 62, 27-125.
29. Gaertig, J. and Kapler, G. (1999). Transient and stable DNA transformation of Tetrahymena thermophila by electroporation. Methods Cell Biol. 62, 485-500.
30. Gaertig, J., Gu, L., Hai, B. and Gorovsky, M. A. (1994). High frequency vectormediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22, 5391-5398.
31. 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.
32. Giddings, T. H., Jr, Meehl, J. B., Pearson, C. G. and Winey, M. (2010). Electron tomography and immuno-labeling of Tetrahymena thermophila basal bodies. Methods Cell Biol. 96, 117-141.
33. Gogendeau, D., Beisson, J., de Loubresse, N. G., Le Caer, J.-P., Ruiz, F., Cohen, J., Sperling, L., Koll, F. and Klotz, C. (2007). An Sfi1p-like centrin-binding protein mediates centrin-based Ca2+-dependent contractility in Paramecium tetraurelia. Eukaryot. Cell 6, 1992-2000.
34. Gogendeau, D., Klotz, C., Arnaiz, O., Malinowska, A., Dadlez, M., de Loubresse, N. G., Ruiz, F., Koll, F. and Beisson, J. (2008). Functional diversification of centrins and cell morphological complexity. J. Cell Sci. 121, 65-74.
35. Graser, S., Stierhof, Y.-D., Lavoie, S. B., Gassner, O. S., Lamla, S., Le Clech, M. and Nigg, E. A. (2007). Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179, 321-330.
36. Hagiwara, H., Ohwada, N. and Takata, K. (2004). Cell biology of normal and abnormal ciliogenesis in the ciliated epithelium. Int. Rev. Cytol. 234, 101-141.
37. Hai, B., Gaertig, J. and Gorovsky, M. A. (1999). Knockout heterokaryons enable facile mutagenic analysis of essential genes in Tetrahymena. Methods Cell Biol. 62, 513-531.
38. Hinchcliffe, E. H. (2011). The centrosome and bipolar spindle assembly: does one have anything to do with the other? Cell Cycle 10, 3841-3848.
39. 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.
40. Hoffmann, E. K., Rasmussen, L. and Zeuthen, E. (1974). Cytochalasin B: aspects of phagocytosis in nutrient uptake in Tetrahymena. J. Cell Sci. 15, 403-406.
41. Howard-Till, R. A. and Yao, M.-C. (2007). Tudor nuclease genes and programmed DNA rearrangements in Tetrahymena thermophila. Eukaryot. Cell 6, 1795-1804.
42. Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
43. Jaspersen, S. L. and Winey, M. (2004). The budding yeast spindle pole body: structure, duplication, and function. Annu. Rev. Cell Dev. Biol. 20, 1-28.
44. Jerka-Dziadosz, M., Koll, F., Włoga, D., Gogendeau, D., Garreau de Loubresse, N., Ruiz, F., Fabczak, S. and Beisson, J. (2012). A centrin3-dependent, transient, appendage of the mother basal body guides the positioning of the daughter basal body in Paramecium. Protist. [Epub ahead of print].
45. Jones, M. H. and Winey, M. (2006). Centrosome duplication: is asymmetry the clue? Curr. Biol. 16, R808-R810.
46. 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.
47. 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.
48. Kochanski, R. S. and Borisy, G. G. (1990). Mode of centriole duplication and distribution. J. Cell Biol. 110, 1599-1605.
49. Kunimoto, K., Yamazaki, Y., Nishida, T., Shinohara, K., Ishikawa, H., Hasegawa, T., Okanoue, T., Hamada, H., Noda, T., Tamura, A. et al. (2012). Coordinated ciliary beating requires Odf2-mediated polarization of basal bodies via basal feet. Cell 148, 189-200.
50. Lansing, T. J., Frankel, J. and Jenkins, L. M. (1985). Oral ultrastructure and oral development of the misaligned undulating membrane mutant of Tetrahymena thermophila. J. Protozool. 32, 126-139.
51. Laoukili, J., Perret, E., Middendorp, S., Houcine, O., Guennou, C., Marano, F., Bornens, M. and Tournier, F. (2000). Differential expression and cellular distribution of centrin isoforms during human ciliated cell differentiation in vitro. J. Cell Sci. 113, 1355-1364.
52. Li, S., Sandercock, A. M., Conduit, P., Robinson, C. V., Williams, R. L. and Kilmartin, J. V. (2006). Structural role of Sfi1p-centrin filaments in budding yeast spindle pole body duplication. J. Cell Biol. 173, 867-877.
53. Marshall, W. F. (2012). Centriole asymmetry determines algal cell geometry. Curr. Opin. Plant Biol. 15, 632-637.
54. Martinez-Sanz, J., Yang, A., Blouquit, Y., Duchambon, P., Assairi, L. and Craescu, C. T. (2006). Binding of human centrin 2 to the centrosomal protein hSfi1. FEBS J. 273, 4504-4515.
55. Martinez-Sanz, J., Kateb, F., Assairi, L., Blouquit, Y., Bodenhausen, G., Abergel, D., Mouawad, L. and Craescu, C. T. (2010). Structure, dynamics and thermodynamics of the human centrin 2/hSfi1 complex. J. Mol. Biol. 395, 191-204.
56. Meehl, J. B., Giddings, T. H., Jr and Winey, M. (2009). High pressure freezing, electron microscopy, and immuno-electron microscopy of Tetrahymena thermophila basal bodies. Methods Mol. Biol. 586, 227-241.
57. Miao, W., Xiong, J., Bowen, J., Wang, W., Liu, Y., Braguinets, O., Grigull, J., Pearlman, R. E., Orias, E. and Gorovsky, M. A. (2009). Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS ONE 4, e4429.
58. Mochizuki, K., Fine, N. A., Fujisawa, T. and Gorovsky, M. A. (2002). Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in Tetrahymena. Cell 110, 689-699.
59. 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.
60. Nigg, E. A. and Stearns, T. (2011). The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160.
61. Nishi, R., Okuda, Y., Watanabe, E., Mori, T., Iwai, S., Masutani, C., Sugasawa, K. and Hanaoka, F. (2005). Centrin 2 stimulates nucleotide excision repair by interacting with xeroderma pigmentosum group C protein. Mol. Cell. Biol. 25, 5664-5674.
62. Orias, E. and Rasmussen, L. (1976). Dual capacity for nutrient uptake in Tetrahymena. IV. Growth without food vacuoles and its implications. Exp. Cell Res. 102, 127-137.
63. Orias, E., Hamilton, E. P. and Orias, J. D. (1999). Tetrahymena as a laboratory organism: useful strains, cell culture, and cell line maintenance. Methods Cell Biol. 62, 189-211.
64. 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.
65. Pearson, C. G., Giddings, T. H., Jr and Winey, M. (2009a). Basal body components exhibit differential protein dynamics during nascent basal body assembly. Mol. Biol. Cell 20, 904-914.
66. Pearson, C. G., Osborn, D. P. S., Giddings, T. H., Jr, Beales, P. L. and Winey, M. (2009b). Basal body stability and ciliogenesis requires the conserved component Poc1. J. Cell Biol. 187, 905-920.
67. Resendes, K. K., Rasala, B. A. and Forbes, D. J. (2008). Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export. Mol. Cell. Biol. 28, 1755-1769.
68. 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.
69. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N. G., Palmer, A. E. and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
70. Shang, Y., Song, X., Bowen, J., Corstanje, R., Gao, Y., Gaertig, J. and Gorovsky, M. A. (2002). A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 99, 3734-3739.
71. Shang, Y., Tsao, C.-C. and Gorovsky, M. A. (2005). Mutational analyses reveal a novel function of the nucleotide-binding domain of gamma-tubulin in the regulation of basal body biogenesis. J. Cell Biol. 171, 1035-1044.
72. Stemm-Wolf, A. J.,Morgan,G.,Giddings, T.H., Jr,White, E. A.,Marchione, R.,McDonald, H. B. andWiney,M. (2005). Basal body duplication and maintenance require one member of the Tetrahymena thermophila centrin gene family. Mol. Biol. Cell 16, 3606-3619.
73. Stover, N. A., Krieger, C. J., Binkley, G., Dong, Q., Fisk, D. G., Nash, R., Sethuraman, A., Weng, S. and Cherry, J. M. (2006). Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research. Nucleic Acids Res. 34 Database issue, D500-D503.
74. Stuart, K. R. and Cole, E. S. (1999). Nuclear and cytoskeletal fluorescence microscopy techniques. Methods Cell Biol. 62, 291-311.
75. Thompson, J. R., Ryan, Z. C., Salisbury, J. L. and Kumar, R. (2006). The structure of the human centrin 2-xeroderma pigmentosum group C protein complex. J. Biol. Chem. 281, 18746-18752.
76. Vladar, E. K. and Stearns, T. (2007). Molecular characterization of centriole assembly in ciliated epithelial cells. J. Cell Biol. 178, 31-42.
77. Vonderfecht, T., Stemm-Wolf, A. J., Hendershott, M., Giddings, T. H., Jr, Meehl, J. B. and Winey, M. (2011). The two domains of centrin have distinct basal body functions in Tetrahymena. Mol. Biol. Cell 22, 2221-2234.
78. Vonderfecht, T., Cookson, M. W., Giddings, T. H., Jr, Clarissa, C. and Winey, M. (2012). The two human centrin homologues have similar but distinct functions at Tetrahymena basal bodies. Mol. Biol. Cell 23, 4766-4777.
79. Vorobjev, I. A. and Chentsov, Yu. S. (1982). Centrioles in the cell cycle. I. Epithelial cells. J. Cell Biol. 93, 938-949.
80. Wallingford, J. B. (2010). Planar cell polarity signaling, cilia and polarized ciliary beating. Curr. Opin. Cell Biol. 22, 597-604.
81. Williams, N. E., Honts, J. E. and Kaczanowska, J. (1990). The formation of basal body domains in the membrane skeleton of Tetrahymena. Development 109, 935-942.
82. Winey, M., Stemm-Wolf, A. J., Giddings, T. H., Jr and Pearson, C. G. (2012). Cytological analysis of Tetrahymena thermophila. Methods Cell Biol. 109, 357-378.
83. Wloga, D. and Frankel, J. (2012). From molecules to morphology: cellular organization of Tetrahymena thermophila. Methods Cell Biol. 109, 83-140.
84. Wright, R. L., Salisbury, J. and Jarvik, 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.
85. Yamashita, Y. M. and Fuller, M. T. (2008). Asymmetric centrosome behavior and the mechanisms of stem cell division. J. Cell Biol. 180, 261-266.
86. Yang, C.-H., Kasbek, C., Majumder, S., Yusof, A. M. and Fisk, H. A. (2010). Mps1 phosphorylation sites regulate the function of centrin 2 in centriole assembly. Mol. Biol. Cell 21, 4361-4372.
87. Yao, M.-C., Fuller, P. and Xi, X. (2003). Programmed DNA deletion as an RNAguided system of genome defense. Science 300, 1581-1584.