Control of ciliogenesis by FOR20, a novel centrosome and pericentriolar satellite protein

Journal of Cell Science

Volumn 123, Issue 14, 2010, Pages 2391-2401

  Sedjaï, Fatima ^a,b,c   Acquaviva, Claire ^a,b,c   Chevrier, Véronique ^a,b,c   Chauvin, Jean Paul ^c,d   Coppin, Emilie ^a,b,c   Aouane, Aicha ^c,d   Coulier, François ^a,b,c   Tolun, Aslihan ^e   Pierres, Michel ^c,f   Birnbaum, Daniel ^a,b,c   Rosnet, Olivier ^a,b,c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUT PAOLI CALMETTES   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d AIX MARSEILLE UNIVERSITÉ   (France)

^e BOGAZICI UNIVERSITY   (Turkey)

^f CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

Centrosome; Microtubule; PCM1; Pericentriolar satellites; Primary cilium

Indexed keywords

DETERGENT; MICROTUBULE PROTEIN; PROTEIN FOR20; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL ORGANELLE; CENTROSOME; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; MICROTUBULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STAINING;

ANIMALS; ANTIBODIES, MONOCLONAL; AUTOANTIGENS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CENTROSOME; CHROMOSOMAL PROTEINS, NON-HISTONE; CILIA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; HYBRIDOMAS; MICROTUBULES; PHYLOGENY; PROTEIN ENGINEERING; PROTEINS; RATS; RETINAL PIGMENT EPITHELIUM; RNA, SMALL INTERFERING;

EID: 77954899288     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.065045     Document Type: Article

References (56)

1. Acquaviva, C., Chevrier, V., Chauvin, J. P., Fournier, G., Birnbaum, D. and Rosnet, O. (2009). The centrosomal FOP protein is required for cell cycle progression and survival. Cell Cycle 8, 1217-1227.
2. Azimzadeh, J., Nacry, P., Christodoulidou, A., Drevensek, S., Camilleri, C., Amiour, N., Parcy, F., Pastuglia, M. and Bouchez, D. (2008). Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20, 2146-2159.
3. 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.
4. Balczon, R., Varden, C. E. and Schroer, T. A. (1999). Role for microtubules in centrosome doubling in Chinese hamster ovary cells. Cell Motil. Cytoskeleton 42, 60-72.
5. Black, M. M. and Kurdyla, J. T. (1983). Microtubule-associated proteins of neurons. J. Cell Biol. 97, 1020-1028.
6. Blacque, O. E., Reardon, M. J., Li, C., McCarthy, J., Mahjoub, M. R., Ansley, S. J., Badano, J. L., Mah, A. K., Beales, P. L., Davidson, W. S. et al. (2004). Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev. 18, 1630-1642.
7. Bond, J. and Woods, C. G. (2006). Cytoskeletal genes regulating brain size. Curr. Opin. Cell Biol. 18, 95-101.
8. Bornens, M., Paintrand, M., Berges, J., Marty, M. C. and Karsenti, E. (1987). Structural and chemical characterization of isolated centrosomes. Cell Motil. Cytoskeleton 8, 238-249.
9. Boucrot, E., Henry, T., Borg, J. P., Gorvel, J. P. and Meresse, S. (2005). The intracellular fate of Salmonella depends on the recruitment of kinesin. Science 308, 1174-1178.
10. Burkhardt, J. K., Echeverri, C. J., Nilsson, T. and Vallee, R. B. (1997). Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139, 469-484.
11. Christensen, S. T., Pedersen, S. F., Satir, P., Veland, I. R. and Schneider, L. (2008). The primary cilium coordinates signaling pathways in cell cycle control and migration during development and tissue repair. Curr. Top. Dev. Biol. 85, 261-301.
12. Dammermann, A. and Merdes, A. (2002). Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J. Cell Biol. 159, 255-266. (Pubitemid 35283395)
13. Dawe, H. R., Farr, H. and Gull, K. (2007). Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J. Cell Sci. 120, 7-15. (Pubitemid 46206644)
14. Deane, J. A., Cole, D. G., Seeley, E. S., Diener, D. R. and Rosenbaum, J. L. (2001). Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 11, 1586-1590.
15. Didier, C., Merdes, A., Gairin, J. E. and Jabrane-Ferrat, N. (2008). Inhibition of proteasome activity impairs centrosome-dependent microtubule nucleation and organization. Mol. Biol. Cell 19, 1220-1229. (Pubitemid 351481833)
16. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. (Pubitemid 38832724)
17. Emes, R. D. and Ponting, C. P. (2001). A new sequence motif linking lissencephaly, Treacher Collins and oral-facial-digital type 1 syndromes, microtubule dynamics and cell migration. Hum. Mol. Genet. 10, 2813-2120.
18. Engelender, S., Sharp, A. H., Colomer, V., Tokito, M. K., Lanahan, A., Worley, P., Holzbaur, E. L. and Ross, C. A. (1997). Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 6, 2205-2212. (Pubitemid 27501070)
19. Fabunmi, R. P., Wigley, W. C., Thomas, P. J. and DeMartino, G. N. (2000). Activity and regulation of the centrosome-associated proteasome. J. Biol. Chem. 275, 409-413.
20. Felsenstein, J. (1989). PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5.
21. Ferrante, M. I., Giorgio, G., Feather, S. A., Bulfone, A., Wright, V., Ghiani, M., Selicorni, A., Gammaro, L., Scolari, F., Woolf, A. S. et al. (2001). Identification of the gene for oral-facial-digital type I syndrome. Am. J. Hum. Genet. 68, 569-576.
22. Ferrante, M. I., Zullo, A., Barra, A., Bimonte, S., Messaddeq, N., Studer, M., Dolle, P. and Franco, B. (2006). Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat. Genet. 38, 112-117.
23. Galtier, N., Gouy, M. and Gautier, C. (1996). SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12, 543-548.
24. Gerdes, J. M. and Katsanis, N. (2008). Ciliary function and Wnt signal modulation. Curr. Top. Dev. Biol. 85, 175-195.
25. Gerlitz, G., Darhin, E., Giorgio, G., Franco, B. and Reiner, O. (2005). Novel functional features of the Lis-H domain: role in protein dimerization, half-life and cellular localization. Cell Cycle 4, 1632-1640.
26. Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
27. Jekely, G. and Arendt, D. (2006). Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. BioEssays 28, 191-198.
28. Kavaslar, G. N., Onengut, S., Derman, O., Kaya, A. and Tolun, A. (2000). The novel genetic disorder microhydranencephaly maps to chromosome 16p13.3-12.1. Am. J. Hum. Genet. 66, 1705-1709.
29. 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.
30. Kim, J. C., Badano, J. L., Sibold, S., Esmail, M. A., Hill, J., Hoskins, B. E., Leitch, C. C., Venner, K., Ansley, S. J., Ross, A. J. et al. (2004a). The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 36, 462-470.
31. Kim, M. H., Cooper, D. R., Oleksy, A., Devedjiev, Y., Derewenda, U., Reiner, O., Otlewski, J. and Derewenda, Z. S. (2004b). The structure of the N-terminal domain of the product of the lissencephaly gene Lis1 and its functional implications. Structure 12, 987-998.
32. Kubo, A. and Tsukita, S. (2003). Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cell-cycle-dependent assembly/disassembly. J. Cell Sci. 116, 919-928. (Pubitemid 36367641)
33. Kubo, A., Sasaki, H., Yuba-Kubo, A., Tsukita, S. and Shiina, N. (1999). Centriolar satellites: molecular characterization, ATP-dependent movement toward centrioles and possible involvement in ciliogenesis. J. Cell Biol. 147, 969-980.
34. Lechtreck, K. F., Delmotte, P., Robinson, M. L., Sanderson, M. J. and Witman, G. B. (2008). Mutations in Hydin impair ciliary motility in mice. J. Cell Biol. 180, 633-643. (Pubitemid 351240709)
35. Loktev, A. V., Zhang, Q., Beck, J. S., Searby, C. C., Scheetz, T. E., Bazan, J. F., Slusarski, D. C., Sheffield, V. C., Jackson, P. K. and Nachury, M. V. (2008). A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev. Cell 15, 854-865.
36. Marshall, W. F. (2008). Basal bodies platforms for building cilia. Curr. Top. Dev. Biol. 85, 1-22.
37. Marshall, W. F. and Rosenbaum, J. L. (2001). Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J. Cell Biol. 155, 405-414.
38. Marshall, W. F. and Nonaka, S. (2006). Cilia: tuning in to the cell's antenna. Curr. Biol. 16, R604-R614.
39. Marshall, W. F., Qin, H., Rodrigo Brenni, M. and Rosenbaum, J. L. (2005). Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol. Biol. Cell 16, 270-278. (Pubitemid 40024309)
40. Megraw, T. L., Kilaru, S., Turner, F. R. and Kaufman, T. C. (2002). The centrosome is a dynamic structure that ejects PCM flares. J. Cell Sci. 115, 4707-4718. (Pubitemid 36004427)
41. Mikolajka, A., Yan, X., Popowicz, G. M., Smialowski, P., Nigg, E. A. and Holak, T. A. (2006). Structure of the N-terminal domain of the FOP (FGFR1OP) protein and implications for its dimerization and centrosomal localization. J. Mol. Biol. 359, 863-875. (Pubitemid 43831933)
42. Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, C. J., Peranen, J., Merdes, A., Slusarski, D. C., Scheller, R. H., Bazan, J. F., Sheffield, V. C. et al. (2007). A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213.
43. Ou, G., Blacque, O. E., Snow, J. J., Leroux, M. R. and Scholey, J. M. (2005). Functional coordination of intraflagellar transport motors. Nature 436, 583-587. (Pubitemid 41112934)
44. Park, T. J., Mitchell, B. J., Abitua, P. B., Kintner, C. and Wallingford, J. B. (2008). Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 40, 871-879. (Pubitemid 351913644)
45. Pazour, G. J. and Bloodgood, R. A. (2008). Targeting proteins to the ciliary membrane. Curr. Top. Dev. Biol. 85, 115-149.
46. Pedersen, L. B. and Rosenbaum, J. L. (2008). Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 85, 23-61.
47. Popovici, C., Zhang, B., Gregoire, M. J., Jonveaux, P., Lafage-Pochitaloff, M., Birnbaum, D. and Pebusque, M. J. (1999). The t(6;8)(q27;p11) translocation in a stem cell myeloproliferative disorder fuses a novel gene, FOP, to fibroblast growth factor receptor 1. Blood 93, 1381-1389. (Pubitemid 29076154)
48. Romio, L., Fry, A. M., Winyard, P. J., Malcolm, S., Woolf, A. S. and Feather, S. A. (2004). OFD1 is a centrosomal/basal body protein expressed during mesenchymal-epithelial transition in human nephrogenesis. J. Am. Soc. Nephrol. 15, 2556-2568.
49. Satir, P. and Christensen, S. T. (2007). Overview of structure and function of mammalian cilia. Annu. Rev. Physiol. 69, 377-400.
50. Sawin, K. E., Lourenco, P. C. and Snaith, H. A. (2004). Microtubule nucleation at nonspindle pole body microtubule-organizing centers requires fission yeast centrosomin-related protein mod20p. Curr. Biol. 14, 763-775.
51. Singla, V. and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
52. Srsen, V., Gnadt, N., Dammermann, A. and Merdes, A. (2006). Inhibition of centrosome protein assembly leads to p53-dependent exit from the cell cycle. J. Cell Biol. 174, 625-630.
53. Tassin, A. M., Celati, C., Moudjou, M. and Bornens, M. (1998). Characterization of the human homologue of the yeast spc98p and its association with gamma-tubulin. J. Cell Biol. 141, 689-701.
54. Town, T., Breunig, J. J., Sarkisian, M. R., Spilianakis, C., Ayoub, A. E., Liu, X., Ferrandino, A. F., Gallagher, A. R., Li, M. O., Rakic, P. et al. (2008). The stumpy gene is required for mammalian ciliogenesis. Proc. Natl. Acad. Sci. USA 105, 2853-2858.
55. Wheatley, D. N., Wang, A. M. and Strugnell, G. E. (1996). Expression of primary cilia in mammalian cells. Cell Biol. Int. 20, 73-81.
56. Wong, S. Y. and Reiter, J. F. (2008). The primary cilium at the crossroads of mammalian hedgehog signaling. Curr. Top. Dev. Biol. 85, 225-260.