Bug22 influences cilium morphology and the posttranslational modification of ciliary microtubules

Biology Open

Volumn 3, Issue 2, 2014, Pages 138-151

  Maia, Teresa Mendes ^a   Gogendeau, Delphine ^a   Pennetier, Carole ^a   Janke, Carsten ^b   Basto, Renata ^a  

^a INSTITUT CURIE   (France)

^b INSERM U1005   (France)

Author keywords

Basal bodies; Cilia; Sperm individualization; Spermatogenesis; Tubulin post translation modifications

Indexed keywords

EID: 84979072219     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20146577     Document Type: Article

References (65)

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. Arama, E., Agapite, J. and Steller, H. (2003). Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev. Cell 4, 687-697.
3. Avidor-Reiss, T., Maer, A. M., Koundakjian, E., Polyanovsky, A., Keil, T., Subramaniam, S. and Zuker, C. S. (2004). Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117, 527-539.
4. Baker, J. D., Adhikarakunnathu, S. and Kernan, M. J. (2004). Mechanosensorydefective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 131, 3411-3422.
5. 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.
6. Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A. and Raff, J. W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042.
7. Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M. K., Carmo, N., Balloux, F., Callaini, G. and Glover, D. M. (2005). SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207.
8. Blachon, S., Cai, X., Roberts, K. A., Yang, K., Polyanovsky, A., Church, A. and Avidor-Reiss, T. (2009). A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 182,133-144.
9. Bressac, C., Bré, M. H., Darmanaden-Delorme, J., Laurent, M., Levilliers, N. and Fleury, A. (1995). A massive new posttranslational modification occurs on axonemal tubulin at the final step of spermatogenesis in Drosophila. Eur. J. Cell Biol. 67, 346-355.
10. Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S., Hart, S. R., Portman, N., Shaw, M. K., Ginger, M. L., Gaskell, S. J., McKean, P. G. et al. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227.
11. Carvalho-Santos, Z., Machado, P., Alvarez-Martins, I., Gouveia, S. M., Jana, S. C., Duarte, P., Amado, T., Branco, P., Freitas, M. C., Silva, S. T. et al. (2012). BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. Dev. Cell23, 412-424.
12. Chatterjee, N., Rollins, J., Mahowald, A. P. and Bazinet, C. (2011). Neurotransmitter Transporter-Like: a male germline-specific SLC6 transporter required for Drosophila spermiogenesis. PLoS ONE 6, e16275.
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.
14. Delgehyr, N., Rangone, H., Fu, J., Mao, G., Tom, B., Riparbelli, M. G., Callaini, G. and Glover, D. M. (2012). Klp10A, a microtubule-depolymerizing kinesin-13, cooperates with CP110 to control Drosophila centriole length. Curr. Biol. 22, 502-509.
15. Eddé, B., Rossier, J., Le Caer, J. P., Desbruyères, E., Gros, F. and Denoulet, P. (1990). Posttranslational glutamylation of alpha-tubulin. Science 247, 83-85.
16. Enjolras, C., Thomas, J., Chhin, B., Cortier, E., Duteyrat, J. L., Soulavie, F., Kernan, M. J., Laurençon, A. and Durand, B. (2012). Drosophila chibby is required for basal body formation and ciliogenesis but not for Wg signaling. J. Cell Biol. 197, 313-325.
17. Fabrizio, J. J., Hime, G., Lemmon, S. K. and Bazinet, C. (1998). Genetic dissection of sperm individualization in Drosophila melanogaster. Development 125, 1833-1843.
18. Gogendeau, D. and Basto, R. (2010). Centrioles in flies: the exception to the rule? Semin. Cell Dev. Biol. 21, 163-173.
19. Gong, Z., Son, W., Chung, Y. D., Kim, J., Shin, D. W., McClung, C. A., Lee, Y., Lee, H. W., Chang, D. J., Kaang, B. K. et al. (2004). Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 24, 9059-9066.
20. Greene, J. C., Whitworth, A. J., Kuo, I., Andrews, L. A., Feany, M. B. and Pallanck, L. J. (2003). Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. USA 100, 4078-4083.
21. Hicks, J. L., Deng, W. M., Rogat, A. D., Miller, K. G. and Bownes, M. (1999). Class VI unconventional myosin is required for spermatogenesis in Drosophila. Mol. Biol. Cell 10, 4341-4353.
22. Hodges, M. E., Wickstead, B., Gull, K. and Langdale, J. A. (2011). Conservation of ciliary proteins in plants with no cilia. BMC Plant Biol. 11, 185.
23. Hoyle, H. D., Turner, F. R. and Raff, E. C. (2008). Axoneme-dependent tubulin modifications in singlet microtubules of the Drosophila sperm tail. Cell Motil. Cytoskeleton 65, 295-313.
24. Huang, J., Zhou, W., Watson, A. M., Jan, Y. N. and Hong, Y. (2008). Efficient endsout gene targeting in Drosophila. Genetics 180, 703-707.
25. Ishikawa, H., Thompson, J., Yates, J. R., 3rd and Marshall, W. F. (2012). Proteomic analysis of mammalian primary cilia. Curr. Biol. 22, 414-419.
26. Janke, C. and Bulinski, J. C. (2011). Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12, 773-786.
27. Kaplan, Y., Gibbs-Bar, L., Kalifa, Y., Feinstein-Rotkopf, Y. and Arama, E. (2010). Gradients of a ubiquitin E3 ligase inhibitor and a caspase inhibitor determine differentiation or death in spermatids. Dev. Cell 19, 160-173.
28. Kavlie, R. G., Kernan, M. J. and Eberl, D. F. (2010). Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185, 177-188.
29. 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.
30. Kernan, M. and Zuker, C. (1995). Genetic approaches to mechanosensory transduction. Curr. Opin. Neurobiol. 5, 443-448.
31. Kernan, M., Cowan, D. and Zuker, C. (1994). Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12, 1195-1206.
32. Kim, S., Zaghloul, N. A., Bubenshchikova, E., Oh, E. C., Rankin, S., Katsanis, N., Obara, T. and Tsiokas, L. (2011). Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat. Cell Biol. 13, 351-360.
33. Ko, H. W., Norman, R. X., Tran, J., Fuller, K. P., Fukuda, M. and Eggenschwiler, J. T. (2010). Broad-minded links cell cycle-related kinase to cilia assembly and hedgehog signal transduction. Dev. Cell 18, 237-247.
34. Laligné, C., Klotz, C., de Loubresse, N. G., Lemullois, M., Hori, M., Laurent, F. X., Papon, J. F., Louis, B., Cohen, J. and Koll, F. (2010). Bug22p, a conserved centrosomal/ciliary protein also present in higher plants, is required for an effective ciliary stroke in Paramecium. Eukaryot. Cell 9, 645-655.
35. 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.
36. Lindsley, K. T. D. (1980). Spermatogenesis. In The Genetics and Biology of Drosophila, Vol. 2b (ed. M. Ashburner and T. R. F. Wright). London: Academic Press.
37. Luo, L., Liao, Y. J., Jan, L. Y. and Jan, Y. N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
38. Martinez-Campos, M., Basto, R., Baker, J., Kernan, M. and Raff, J. W. (2004). The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol. 165, 673-683.
39. Mottier-Pavie, V. and Megraw, T. L. (2009). Drosophila bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol. Biol. Cell 20, 2605-2614.
40. Noguchi, T. and Miller, K. G. (2003). A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130, 1805-1816.
41. Noguchi, T., Lenartowska, M. and Miller, K. G. (2006). Myosin VI stabilizes an actin network during Drosophila spermatid individualization. Mol. Biol. Cell 17, 2559-2571.
42. Ostrowski, L. E., Blackburn, K., Radde, K. M., Moyer, M. B., Schlatzer, D. M., Moseley, A. and Boucher, R. C. (2002). A proteomic analysis of human cilia: identification of novel components. Mol. Cell. Proteomics 1, 451-465.
43. Pazour, G. J., Agrin, N., Leszyk, J. and Witman, G. B. (2005). Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170, 103-113.
44. Peel, N., Stevens, N. R., Basto, R. and Raff, J. W. (2007). Overexpressing centriolereplication proteins in vivo induces centriole overduplication and de novo formation. Curr. Biol. 17, 834-843.
45. Pisano, C., Bonaccorsi, S. and Gatti, M. (1993). The kl-3 loop of the Y chromosome of Drosophila melanogaster binds a tektin-like protein. Genetics 133, 569-579.
46. Rathke, C., Barckmann, B., Burkhard, S., Jayaramaiah-Raja, S., Roote, J. and Renkawitz-Pohl, R. (2010). Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis. Eur. J. Cell Biol. 89, 326-338.
47. Redeker, V., Levilliers, N., Schmitter, J. M., Le Caer, J. P., Rossier, J., Adoutte, A. and Bré, M. H. (1994). Polyglycylation of tubulin: a posttranslational modification in axonemal microtubules. Science 266, 1688-1691.
48. Riparbelli, M. G. and Callaini, G. (2007). The Drosophila parkin homologue is required for normal mitochondrial dynamics during spermiogenesis. Dev. Biol. 303, 108-120.
49. Riparbelli, M. G. and Callaini, G. (2011). Male gametogenesis without centrioles. Dev. Biol. 349, 427-439.
50. Riparbelli, M. G., Callaini, G. and Megraw, T. L. (2012). Assembly and persistence of primary cilia in dividing Drosophila spermatocytes. Dev. Cell 23, 425-432.
51. Riparbelli, M. G., Cabrera, O. A., Callaini, G. and Megraw, T. L. (2013). Unique properties of Drosophila spermatocyte primary cilia. Biol. Open 2, 1137-1147.
52. Rodrigues-Martins, A., Bettencourt-Dias, M., Riparbelli, M., Ferreira, C., Ferreira, I., Callaini, G. and Glover, D. M. (2007). DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr. Biol. 17, 1465-1472.
53. Rogowski, K., Juge, F., van Dijk, J., Wloga, D., Strub, J. M., Levilliers, N., Thomas, D., Bré, M. H., Van Dorsselaer, A., Gaertig, J. et al. (2009). Evolutionary divergence of enzymatic mechanisms for posttranslational polyglycylation. Cell 137, 1076-1087.
54. Sabino, D., Brown, N. H. and Basto, R. (2011). Drosophila Ajuba is not an Aurora-A activator but is required to maintain Aurora-A at the centrosome. J. Cell Sci. 124, 1156-1166.
55. Seroude, L., Brummel, T., Kapahi, P. and Benzer, S. (2002). Spatio-temporal analysis of gene expression during aging in Drosophila melanogaster. Aging Cell 1, 47-56.
56. Sharma, Y., Cheung, U., Larsen, E. W. and Eberl, D. F. (2002). PPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in drosophila. Genesis 34, 115-118.
57. Smith, J. C., Northey, J. G., Garg, J., Pearlman, R. E. and Siu, K. W. (2005). Robust method for proteome analysis by MS/MS using an entire translated genome: demonstration on the ciliome of Tetrahymena thermophila. J. Proteome Res. 4, 909-919.
58. Stolc, V., Samanta, M. P., Tongprasit, W. and Marshall, W. F. (2005). Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc. Natl. Acad. Sci. USA 102, 3703-3707.
59. Tam, L. W., Wilson, N. F. and Lefebvre, P. A. (2007). A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J. Cell Biol. 176, 819-829.
60. Tates, A. D. (1971). Cytodifferentiation during Spermatogenesis in Drosophila melanogaster. PhD dissertation, University of Leiden, The Netherlands.
61. Texada, M. J., Simonette, R. A., Johnson, C. B., Deery, W. J. and Beckingham, K. M. (2008). Yuri gagarin is required for actin, tubulin and basal body functions in Drosophila spermatogenesis. J. Cell Sci. 121, 1926-1936.
62. Tokuyasu, K. T., Peacock, W. J. and Hardy, R. W. (1972a). Dynamics of spermiogenesis in Drosophila melanogaster. I. Individualization process. Z. Zellforsch. Mikrosk. Anat. 124, 479-506.
63. Tokuyasu, K. T., Peacock, W. J. and Hardy, R. W. (1972b). Dynamics of spermiogenesis in Drosophila melanogaster. II. Coiling process. Z. Zellforsch. Mikrosk. Anat. 127, 492-525.
64. Varmark, H., Llamazares, S., Rebollo, E., Lange, B., Reina, J., Schwarz, H. and Gonzalez, C. (2007). Asterless is a centriolar protein required for centrosome function and embryo development in Drosophila. Curr. Biol. 17, 1735-1745.
65. Zhou, X., Fabian, L., Bayraktar, J. L., Ding, H. M., Brill, J. A. and Chang, H. C. (2011). Auxilin is required for formation of Golgi-derived clathrin-coated vesicles during Drosophila spermatogenesis. Development 138, 1111-1120.