Imaging intraflagellar transport in trypanosomes

Methods in Cell Biology

Volumn 127, Issue , 2015, Pages 487-508

  Santi Rocca, Julien ^a   Chenouard, Nicolas ^a   Fort, Cécile ^a   Lagache, Thibault ^a   Olivo Marin, Jean Christophe ^a   Bastin, Philippe ^a  

^a CNRS   (France)

Author keywords

Cilia and flagella; Imaging; Intraflagellar transport; Trafficking; Trypanosome

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN; PROTOZOAL PROTEIN; RED FLUORESCENT PROTEIN; SMALL INTERFERING RNA; TUBULIN;

ELECTROKYMOGRAPHY; EUKARYOTIC FLAGELLUM; FLAGELLUM; FLUORESCENCE IMAGING; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEIN TRANSPORT; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI;

CILIA; FLAGELLA; GREEN FLUORESCENT PROTEINS; KYMOGRAPHY; LUMINESCENT PROTEINS; OPTICAL IMAGING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRYPANOSOMA BRUCEI BRUCEI; TUBULIN;

EID: 84955336762     PISSN: 0091679X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.mcb.2015.01.005     Document Type: Article

References (57)

1. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Dore, G., Julkowska, D., et al. (2008). Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Molecular Biology of the Cell, 19, 929-944.
2. Adhiambo, C., Blisnick, T., Toutirais, G., Delannoy, E., & Bastin, P. (2009). A novel function for the atypical small G protein Rab-like 5 in the assembly of the trypanosome flagellum. Journal of Cell Science, 122, 834-841.
3. Archer, S. K., Inchaustegui, D., Queiroz, R., & Clayton, C. (2011). The cell cycle regulated transcriptome of Trypanosoma brucei. PLoS One, 6, e18425.
4. Arts, H. H., Bongers, E. M., Mans, D. A., van Beersum, S. E., Oud, M. M., Bolat, E., et al. (2011). C14ORF179 encoding IFT43 is mutated in Sensenbrenner syndrome. Journal of Medical Genetics, 48, 390-395.
5. ten Asbroek, A. L., Ouellette, M., & Borst, P. (1990). Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature, 348, 174-175.
6. Bader, J. R., Kusik, B.W., & Besharse, J. C. (2012). Analysis of KIF17 distal tip trafficking in zebrafish cone photoreceptors. Vision Research, 75, 37-43.
7. Bastin, P., MacRae, T. H., Francis, S. B., Matthews, K. R., & Gull, K. (1999). Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of trypanosomes. Molecular and Cellular Biology, 19, 8191-8200.
8. Besschetnova, T. Y., Roy, B., & Shah, J. V. (2009). Imaging intraflagellar transport in mammalian primary cilia. Methods in Cell Biology, 93, 331-346.
9. Bhogaraju, S., Cajanek, L., Fort, C., Blisnick, T., Weber, K., Taschner, M., et al. (2013). Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science, 341, 1009-1012.
10. Blisnick, T., Buisson, J., Absalon, S., Marie, A., Cayet, N., & Bastin, P. (2014). The intraflagellar transport dynein complex of trypanosomes is made of a heterodimer of dynein heavy chains and of light and intermediate chains of distinct functions. Molecular Biology of the Cell, 25, 2620-2633.
11. Briggs, L. J., Davidge, J. A., Wickstead, B., Ginger, M. L., & Gull, K. (2004). More than one way to build a flagellum: comparative genomics of parasitic protozoa. Current Biology, 14, R611-R612.
12. Brun, R., & Schonenberger. (1979). Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Tropica, 36, 289-292.
13. Buisson, J., Chenouard, N., Lagache, T., Blisnick, T., Olivo-Marin, J. C., & Bastin, P. (2013). Intraflagellar transport proteins cycle between the flagellum and its base. Journal of Cell Science, 126, 327-338.
14. Burkard, G., Fragoso, C. M., & Roditi, I. (2007). Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Molecular and Biochemical Parasitology, 153, 220-223.
15. de Chaumont, F., Dallongeville, S., Chenouard, N., Herve, N., Pop, S., Provoost, T., et al. (2012). Icy: an open bioimage informatics platform for extended reproducible research. Nature Methods, 9, 690-696.
16. Chenouard, N., Buisson, J., Bloch, I., Bastin, P., & Olivo-Marin, J. C. (2010). Curvelet analysis of kymograph for tracking bi-directional particles in fluorescence microscopy images. Proceedings International Conference on Image Processing, 3657-3660.
17. Chenouard, N., & Unser, M. (2012). 3D steerable wavelets in practice. IEEE Transactions on Image Processing, 21, 4522-4533.
18. Craft, J. M., Harris, J. A., Hyman, S., Kner, P., & Lechtreck, K. F. (2015). Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism. Journal of Cell Biology, 19(208), 223-237.
19. Dacheux, D., Landrein, N., Thonnus, M., Gilbert, G., Sahin, A., Wodrich, H., et al. (2012). A MAP6-related protein is present in protozoa and is involved in flagellum motility. PLoS One, 7, e31344.
20. van Dam, T. J., Townsend, M. J., Turk, M., Schlessinger, A., Sali, A., Field, M. C., et al. (2013). Evolution of modular intraflagellar transport from a coatomer-like progenitor. Proceedings of the National Academy of Sciences of the United States of America, 110, 6943-6948.
21. Davidge, J. A., Chambers, E., Dickinson, H. A., Towers, K., Ginger, M. L., McKean, P. G., et al. (2006). Trypanosome IFT mutants provide insight into the motor location for mobility of the flagella connector and flagellar membrane formation. Journal of Cell Science, 119, 3935-3943.
22. Davis, E. E., Zhang, Q., Liu, Q., Diplas, B. H., Davey, L. M., Hartley, J., et al. (2011). TTC21B contributes both causal and modifying alleles across the ciliopathy spectrum. Nature Genetics, 43, 189-196.
23. Durand-Dubief, M., Kohl, L., & Bastin, P. (2003). Efficiency and specificity of RNA interference generated by intra-and intermolecular double stranded RNA in Trypanosoma brucei. Molecular and Biochemical Parasitology, 129, 11-21.
24. Ersfeld, K., Asbeck, K., & Gull, K. (1998). Direct visualisation of individual gene organisation in Trypanosoma brucei by high-resolution in situ hybridisation. Chromosoma, 107, 237-240.
25. Follit, J. A., Tuft, R. A., Fogarty, K. E., & Pazour, G. J. (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Molecular Biology of the Cell, 17, 3781-3792.
26. Franklin, J. B., & Ullu, E. (2010). Biochemical analysis of PIFTC3, the Trypanosoma brucei orthologue of nematode DYF-13, reveals interactions with established and putative intraflagellar transport components. Molecular Microbiology, 78, 173-186.
27. Huet, D., Blisnick, T., Perrot, S., & Bastin, P. (2014). The GTPase IFT27 is involved in both anterograde and retrograde intraflagellar transport. eLife. http://dx.doi.org/10.7554/eLife.02419.
28. Ishikawa, H., Ide, T., Yagi, T., Jiang, X., Hirono, M., Sasaki, H., et al. (2014). TTC26/DYF13 is an intraflagellar transport protein required for transport of motility-related proteins into flagella. eLife, 3, e01566.
29. Johnson, K. A., & Rosenbaum, J. L. (1992). Polarity of flagellar assembly in Chlamydomonas. Journal of Cell Biology, 119, 1605-1611.
30. Julkowska, D., & Bastin, P. (2009). Tools for analyzing intraflagellar transport in trypanosomes. Methods in Cell Biology, 93, 59-80.
31. Kelly, S., Reed, J., Kramer, S., Ellis, L., Webb, H., Sunter, J., et al. (2007). Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Molecular and Biochemical Parasitology, 154, 103-109.
32. Kohl, L., Robinson, D., & Bastin, P. (2003). Novel roles for the flagellum in cell morphogenesis and cytokinesis of trypanosomes. EMBO Journal, 22, 5336-5346.
33. Kohl, L., Sherwin, T., & Gull, K. (1999). Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. Journal of Eukaryotic Microbiology, 46, 105-109.
34. Kozminski, K. G., Beech, P. L., & Rosenbaum, J. L. (1995). The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. Journal of Cell Biology, 131, 1517-1527.
35. Kozminski, K. G., Johnson, K. A., Forscher, P., & Rosenbaum, J. L. (1993). A motility in the eukaryotic flagellum unrelated to flagellar beating. Proceedings of the National Academy of Sciences of the United States of America, 90, 5519-5523.
36. Kramer, S., & Carrington, M. (2011). Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends in Parasitology, 27, 23-30.
37. Lechtreck, K. F., Johnson, E. C., Sakai, T., Cochran, D., Ballif, B. A., Rush, J., et al. (2009). The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. Journal of Cell Biology, 187, 1117-1132.
38. Marshall, W. F., & Rosenbaum, J. L. (2001). Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. Journal of Cell Biology, 155, 405-414.
39. Morga, B., & Bastin, P. (2013). Getting to the heart of intraflagellar transport using Trypanosoma and Chlamydomonas models: the strength is in their differences. Cilia, 2, 16.
40. Oberholzer, M., Lopez, M. A., Ralston, K. S., & Hill, K. L. (2009). Approaches for functional analysis of flagellar proteins in African trypanosomes. Methods in Cell Biology, 93, 21-57.
41. Orozco, J. T., Wedaman, K. P., Signor, D., Brown, H., Rose, L., & Scholey, J. M. (1999). Movement of motor and cargo along cilia. Nature, 398, 674.
42. Perrault, I., Saunier, S., Hanein, S., Filhol, E., Bizet, A. A., Collins, F., et al. (2012). Mainzer-Saldino syndrome is a ciliopathy caused by IFT140 mutations. American Journal of Human Genetics, 90, 864-870.
43. Pigino, G., Geimer, S., Lanzavecchia, S., Paccagnini, E., Cantele, F., Diener, D. R., et al. (2009). Electron-tomographic analysis of intraflagellar transport particle trains in situ. Journal of Cell Biology, 187, 135-148.
44. Piperno, G., Siuda, E., Henderson, S., Segil, M., Vaananen, H., & Sassaroli, M. (1998). Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. Journal of Cell Biology, 143, 1591-1601.
45. Portman, N., & Gull, K. (2010). The paraflagellar rod of kinetoplastid parasites: from structure to components and function. International Journal of Parasitology, 40, 135-148.
46. Pradel, L. C., Bonhivers, M., Landrein, N., & Robinson, D. R. (2006). NIMA-related kinase TbNRKC is involved in basal body separation in Trypanosoma brucei. Journal of Cell Science, 119, 1852-1863.
47. Qin, H., Burnette, D. T., Bae, Y. K., Forscher, P., Barr, M. M., & Rosenbaum, J. L. (2005). Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Current Biology, 15, 1695-1699.
48. Qin, H., Wang, Z., Diener, D., & Rosenbaum, J. (2007). Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Current Biology, 17, 193-202.
49. Rosenbaum, J. L., Moulder, J. E., & Ringo, D. L. (1969). Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. Journal of Cell Biology, 41, 600-619.
50. Schwartz, G. (1978). Estimating the dimension of a model. Annals of Statistics, 6, 461-464.
51. Sherman, D. R., Janz, L., Hug, M., & Clayton, C. (1991). Anatomy of the parp gene promoter of Trypanosoma brucei. EMBO Journal, 10, 3379-3386.
52. Sherwin, T., & Gull, K. (1989). The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philosophical Transactions of the Royal Society Lond B: Biological Sciences, 323, 573-588.
53. Subota, I., Rotureau, B., Blisnick, T., Ngwabyt, S., Durand-Dubief, M., Engstler, M., & Bastin, P. (2011). ALBA proteins are stage regulated during trypanosome development in the tsetse fly and participate in differentiation. Molecular Biology of the Cell, 22, 4205-4219.
54. Wang, Z., Morris, J. C., Drew, M. E., & Englund, P. T. (2000). Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. Journal of Biological Chemistry, 275, 40174-40179.
55. Wirtz, E., & Clayton, C. (1995). Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science, 268, 1179-1183.
56. Wirtz, E., Leal, S., Ochatt, C., & Cross, G. A. (1999). A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Molecular and Biochemical Parasitology, 99, 89-101.
57. Zomerdijk, J. C., Kieft, R., & Borst, P. (1991). Efficient production of functional mRNA mediated by RNA polymerase I in Trypanosoma brucei. Nature, 353, 772-775.