Centrin deficiency in Chlamydomonas causes defects in basal body replication, segregation and maturation

Journal of Cell Science

Volumn 116, Issue 13, 2003, Pages 2635-2646

  Koblenz, Bettina ^a   Schoppmeier, Jutta ^a   Grunow, Andrea ^a   Lechtreck, Karl Ferdinand ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Centriole; Centrosome; Flagella; RNAi; Spindle pole

Indexed keywords

CALCIUM BINDING PROTEIN; CENTRIN; RNA;

ARTICLE; CELL COUNT; CELL MEMBRANE; CENTROSOME; CHLAMYDOMONAS; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; FLAGELLUM; GENE CONSTRUCT; KINETOSOME; MICROTUBULE; MITOSIS SPINDLE; MULTINUCLEAR CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SPINDLE POLE BODY;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CENTRIOLES; CENTROSOME; CHLAMYDOMONAS; CHROMOSOMAL PROTEINS, NON-HISTONE; FLAGELLA; MICROSCOPY, ELECTRON; MICROTUBULES; MITOTIC SPINDLE APPARATUS; RNA INTERFERENCE;

ALGAE; CHLAMYDOMONAS; EUKARYOTA; PROTISTA; PROTOZOA; RUMEX;

EID: 0038783297     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00497     Document Type: Article

References (56)

1. Adams, I. R. and Kilmartin, J. V. (1999). Localization of core spindle pole body (SPB) components during SPB duplication in Saccharomyces cerevisiae. J. Cell Biol. 145, 809-823.
2. Adams, I. R. and Kilmartin, V. (2000). Spindle pole body duplication: a model for centrosome duplication. Trends Cell Biol. 10, 329-335.
3. 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.
4. Brazelton, W. J., Amundsen, C. D., Silflow, C. D. and Lefebvre, P. A. (2001). The bld1 mutation identifies the Chlamydomonas osm-6 homolog as a gene required for flagellar assembly. Curr Biol. 11, 1591-1594.
5. Compton, D. A. (2000). Spindle assembly in animal cells. Annu. Rev. Biochem. 69, 95-114.
6. Coss, R. A. (1974). Mitosis in Chlamydomonas reinhardtii basal bodies and the mitotic apparatus. J. Cell Biol. 63, 325-329.
7. Doonan, J. H. and Grief, C. (1987). Microtubule cycle in Chlamydomonas reinhardtii: an immunofluorescence study. Cell Motil. Cytoskeleton 7, 381-392.
8. Dutcher, S. K. and Trabuco, E. C. (1998). The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes delta-tubulin, a new member of the tubulin superfamily. Mol. Biol. Cell 9, 1293-1308.
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. Fuhrmann, M., Oertel, W. and Hegemann, P. (1999). A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 19, 353-361.
11. Fuhrmann, M., Stahlberg, A., Govorunova, E., Rank, S. and Hegemann, P. (2001). The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J. Cell Sci. 114, 3857-3863.
12. Gaffal, K. P. and el-Gammal, S. (1990). Elucidation of the enigma of the 'metaphase band' of Chlamydomonas reinhardtii. Protoplasma 156, 139-148.
13. Gorman, D. S. and Levine, R. P. (1965). Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonnas reinhardi. Proc. Natl. Acad. Sci. USA 54, 1665-1669.
14. Grunow, A. and Lechtreck, K.-F. (2001). Mitosis in Dunaliella bioculata (Chlorophyta): Centrin but not basal bodies are at the spindle poles. J. Phycol. 37, 1030-1043.
15. Guerra, C., Wada, Y., Leick, V., Bell, A. and Satir, P. (2003). Cloning, localization, and axonemal function of Tetrahymena centrin. Mol. Biol. Cell 14, 251-261.
16. 2+-binding protein: homology in its protein sequence with calmodulin and the yeast CDC31 gene product. J. Cell Biol. 107, 133-140.
17. Ivanovska, I. and Rose, M. D. (2001). Fine structure analysis of the yeast Centrin, CDC31p, identifies residues specific for cell morphology and spindle pole body duplication. Genetics 157, 503-518.
18. Jarvik, J. W. and Suhan, J. P. (1991). The role of the flagella transition region: interferences from the analysis of a Chlamydomonas mutant with defective transition region structures. J. Cell Sci. 99, 731-740.
19. Johnson, U. and Porter, K. R. (1968). Fine structure of cell divison in Chlamydomonas reinhardi: basal bodies and microtubules. J. Cell Biol. 38, 403-425.
20. Karey, K. P. and Sirbasku, D. A. (1998). Glutaraldehyde fixation increases retention of low molecular weight proteins (growth factors) transferred to nylon membranes for western blot analysis. Anal. Biochem. 187, 255-259.
21. Kindle, K. L. (1990). High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 1228-1232.
22. Klink, V. P. and Wolniak, S. M. (2001). Centrin is necessary for the formation of the motile apparatus in spermatids of Marsilea. Mol. Biol. Cell 12, 761-776.
23. Kochanski, R. S. and Borisy, G. G. (1990). Mode of centriole duplication and distribution. J. Cell Biol. 110, 1599-1605.
24. 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.
25. Lechtreck, K.-F. and Geimer, S. (2000). Distribution of polyglutamylated tubulin in the flagellar apparatus of green flagellates. Cell Motil. Cytoskeleton 47, 219-235.
26. Lechtreck, K.-F. and Bornens, M. (2001). Basal body replication in green algae - when and where does it start? Eur. J. Cell Biol. 80, 631-641.
27. Lechtreck, K.-F., Reize, I. B. and Melkonian, M. (1997). The cytoskeleton of the naked green flagellate Spermatozopsis similis (Chlorophyta): Flagellar and basal body developmental cycle. J. Phycol. 33, 254-265.
28. Lechtreck, K.-F., Rostmann, J. and Grunow, A. (2002). Analysis of Chlamydomonas SF-assemblin by GFP tagging and expression of antisense constructs. J. Cell Sci. 115, 1511-1522.
29. LeDizet, M. and Piperno, G. (1986). Cytoplasmic microtubules containing acetylated alpha-tubulin in Chlamydomonas reinhardtii: spatial arrangement and properties. J. Cell Biol. 103, 13-22.
30. LeDizet, M. and Piperno, G. (1995). The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol. Biol. Cell. 6, 697-711.
31. Levy, Y. Y., Lai, E. Y., Remillard, S. P. and Fulton, C. (1998). Centrin is synthesized and assembled into basal bodies during Naegleria differentiation. Cell Motil. Cytoskeleton 40, 249-260.
32. Lingle, W. L. and Salisbury, J. L. (2000). The role of the centrosome in the development of malignant tumors. Curr. Top. Dev. Biol. 49, 313-329.
33. Marshall, W. F. and Rosenbaum, J. L. (2000). How centrioles work: lessons from green yeast. Curr. Opin. Cell Biol. 12, 119-225.
34. 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.
35. -/- cells. EMBO J. 21, 483-492.
36. Middendorp, S., Paoletti, A., Schiebel, E. and Bornens, M. (1997). Identification of a new mammalian centrin gene, more closely related to Saccharomyces cerevisiae CDC31 gene. Proc. Nat. Acad. Sci. USA 94, 9141-9146.
37. Pennisi, E. (1999). Trigger for centrosome replication found. Science 283, 770-771.
38. Regnard, C., Desbruyères, E., Huet, J. C., Beauvallet, C., Pernollet, J. C. and Eddé, B. (2000). Polyglutamylation of nucleosome assembly proteins. J. Biol. Chem. 275, 15969-15976.
39. Ruiz-Binder, N. E., Geimer, S. and Melkonian, M. (2002). In vivo localization of centrin in the green alga Chlamydomonas reinhardtii. Cell Motil. Cytoskeleton 52, 43-55.
40. Salisbury, J. L. (1995). Centrin, centrosomes, and mitotic spindle poles. Curr. Opin. Cell Biol. 7, 39-45.
41. Salisbury, J. L., Baron, A., Surek, B. and Melkonian, M. (1984). Striated flagella roots: Isolation and partial characterization of a calcium-modulated contractile organelle. J. Cell Biol. 99, 962-970.
42. Salisbury, J. L., Baron, A. T. and Sanders, M. A. (1988). The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. J. Cell Biol. 107, 635-641.
43. Salisbury, J. L., Suino, K., Busby, R. and Springett, M. (2002). Centrin-2 is required for centriole duplication in mammalian cells. Curr. Biol. 12, 1287-1392.
44. Schroda, M., Blocker, D. and Beck, C. F. (2000). The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J. 21, 121-131.
45. Schulze, D., Robenek, H., McFadden, G. I. and Melkonian, M. (1987). Immunlocalization of a calcium-modulated contractile protein in the flagellar apparatus of green algae: the nucleus-basal body-connector. Eur. J. Cell Biol. 45, 51-61.
46. Sluiman, H. J. and Blommers, P. C. J. (1990). Basal apparatus behavior during cellular division (sporulation) in the coccoid green alga Chlorosarcina. Protoplasma 155, 66-75.
47. Smith, N. A., Singh, S. P., Wang, M. B., Stoutjesdijk, P. A., Green, A. G. and Waterhouse, P. M. (2000). Total silencing by intron-spliced hairpin RNAs. Nature 407, 319-320.
48. Spang, A., Courtney, I., Grein, K., Matzner, M. and Schiebel, E. (1995). The Cdc31p-binding protein Kar1p is a component of the half bridge of the yeast spindle pole body. J. Cell Biol. 128, 863-877.
49. Stevens, D. R., Rochaix, J. D. and Purton, S. (1996). The bacterial phleomycin resistance gene ble as a dominant selectable marker in Chlamydomonas. Mol. Gen. Genet. 251, 23-30.
50. Taillon, B. E. and Jarvik, J. W. (1995). Central helix mutations in the centrosome-associated EF-hand protein centrin. Protoplasma 189, 203-215.
51. Taillon, B. E., Adler, S. A., Suhan, J. P. and Jarvik, J. W. (1992). Mutational analysis of centrin: an EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas. J. Cell Biol. 119, 1613-1624.
52. Tassin, A. M. and Bornens, M. (1999). Centrosome structure and microtubule nucleation in animal cells. Biol. Cell 91, 343-354.
53. Winey, M. (1996). Keeping the centrosome cycle on track. Genome stability. Curr. Biol. 6, 962-964.
54. Wolff, A., de Néchaud, B., Chillet, D., Mazarguil. H., Desbruyères, E., Audebert, S., Eddé, B., Gros, F. and Denoulet, P. (1992). Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59, 425-432.
55. Wright, R. L., Adler, S. A., Spanier, J. G. and Jarvik, J. W. (1989). Nucleus-basal body connector in Chlamydomonas: evidence for a role in basal body segregation and against essential roles in mitosis or in determining cell polarity. Cell Motil. Cytoskeleton 14, 516-526.
56. Wu-Scharf, D., Jeong, B., Zhang, C. and Cerutti, H. (2000). Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science 290, 1159-1162.