Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1

Journal of Cell Science

Volumn 112, Issue 21, 1999, Pages 3769-3777

  Bastin, Philippe ^a   Pullen, Timothy J ^a   Sherwin, Trevor ^a   Gull, Keith ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cytoskeleton; Flagellum; Intraflagellar transport; Paraflagellar rod; Trypanosome

Indexed keywords

DETERGENT; PROTEIN;

ARTICLE; AXONEME; CELL CYCLE; CELL DIVISION; CELL TRANSPORT; CYTOSKELETON; FLAGELLUM; GENETIC TRANSFORMATION; GROWTH; MUTANT; NONHUMAN; PARALYSIS; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN TRANSPORT; SEDIMENT; SUSPENSION; TRYPANOSOMA BRUCEI;

ANIMALS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL CYCLE; FLAGELLA; MEMBRANE PROTEINS; MOLECULAR MOTOR PROTEINS; MUTATION; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRYPANOSOMA BRUCEI BRUCEI;

PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0032693564     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (58)

1. Baccetti, B. (1986). Evolutionary trends in sperm structure. Comp. Biochem. Physiol. 85A, 29-36.
2. Bastin, P., Matthews, K. R. and Gull, K. (1996a). The paraflagellar rod of Kinetoplastida: solved and unsolved questions. Parasitol. Today 12, 302-307.
3. Bastin, P., Bagherzadeh, A., Matthews, K. R. and Gull, K. (1996b). A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 77, 235-239.
4. Bastin, P., Sherwin, T. and Gull, K. (1998). Paraflagellar rod is essential to trypanosome motility. Nature 391, 548.
5. Bastin, P. and Gull, K. (1999). Assembly and function of complex flagellar structures illustrated by the paraflagellar rod of trypanosomes. Protist 150, 113-123.
6. Beard, C. A., Saborio, J. L., Tewari, D., Krieglstein, K. G., Henschen, A. H. and Mannings J. E. (1992). Evidence for two distinct major protein components, PAR 1 and PAR 2, in the paraflagellar rod of Trypanosoma cruzi. J. Biol. Chem. 267, 21656-21662.
7. Beverley, S. M. and Clayton, C. E. (1993). Transfection of Leishmania and Trypanosoma brucei by electroporation. In Methods in Molecular Biology of Parasites (ed. E. Hyde), pp. 333-348. Humana Press Inc., Totowa, USA.
8. Birkett, C. R., Parma, A. E., Gerke-Bonet, R., Woodward, R. and Gull, K (1992). Isolation of cDNA clones encoding proteins of complex structures: analysis of the Trypanosoma brucei cytoskeleton. Gene 110, 65-70.
9. Cole, D., Diener, D. R., Himelblau, A. L., Beech, P. L., Fuster, J. C. and Rosenbaum, J. (1998). Chlamydomonas kinesin II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141, 993-1008.
10. Deflorin, J., Rudolf, M. and Seebeck, T. (1994). The major components of the paraflagellar rod of Trypanosoma brucei are two similar but distinct proteins which are encoded by two different gene loci. J. Biol. Chem. 269, 28745-28751.
11. Eid, J. and Sollner-Webb, B. (1991). Stable integrative transformation of Trypanosoma brucei that occurs exclusively by homologous recombination. Proc. Nat. Acad. Sci. USA 88, 2118-2121.
12. Farina, M., Attias, M., Souto-Padron, T., De Souza, W. (1986). Further studies on the organization of the paraxial rod of trypanosomatids. J. Protozool. 33, 552-557.
13. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. G. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
14. Fok, A. K., Wang, H., Katayama, A. M., Aihira, S. and Allen R. D. (1994). 22S axonemal dynein is preassembled and functional prior to being transported and attached on the axonemes. Cell Motil. Cytoskel. 29, 215-224.
15. Fouts, D. L., Stryker, G. A., Gorski, K. S., Miller, M. J., Nguyen, T. V., Whrightsman, R. A. and Manning, J. E. (1998). Evidence for four major distinct protein components for the parflagellar rod of Trypanosoma cruzi. J. Biol. Chem. 273, 21846-21855.
16. Fowkes, M. E. and Mitchell, D. R. (1998). The role of preasssembled cytoplasmic complexes in the assembly of flagellum dynein. Mol. Biol. Cell 9, 2337-2347.
17. Gallo, J. M. and Schrevel, J. (1985). Homologies between paraflagellar rod proteins from trypanosomes and euglenoids revealed by a monoclonal antibody. Eur. J. Cell Biol. 36, 163-168.
18. Johnson, K. A. and Rosenbaum, J. L. (1992). Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 119, 1605-1611.
19. r 8, 000 light chain. J. Biol. Chem. 271, 19358-19366.
20. Kohl, L. and Gull, K. (1998). Molecular architecture of the trypanosome cytoskeleton. Mol. Biochem. Parasitol. 93, 1-9.
21. Kohl, L., Sherwin, T. and Gull, K. (1999). Assembly of the paraflagellar rod and of the flagellum attachement zone complex in Trypanosoma brucei. J. Euk. Microbiol. 46, 105-109.
22. Kozminski, K. G., Johnson, K. A., Forscher, P. and Rosenbaum, J. L. (1993). A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Nat. Acad. Sci. USA 90, 5519-5523.
23. Kozminski, K. G., Beech, P. and Rosenbaum, J. L. (1995). The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131, 1517-1527.
24. Lee, M. G. S. and Van der Ploeg, L. H. T. (1990). Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei. Science 250, 1583-1587.
25. Marszalek, J., Ruiz-Lozano, P., Roberts, E., Chien, K. R. and Goldstein, L. S. B. (1999). Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Nat. Acad. Sci. USA 96, 5043-5048.
26. Moore, L., Santrich, C. and LeBowitz, J. H. (1996). Stage-specific expression of the Leishmania mexicana paraflagellar rod protein PFR-2. Mol. Biochem. Parasitol. 80, 125-135.
27. Morris, R. L. and Scholey, J. M. (1997). Heterotrimeric kinesin II is required for the assembly of motile 9+2 ciliary axonemes on sea urchin embryo. J. Cell Biol. 138, 1009-1022.
28. Ngo, H. M. and Bouck, G. B. (1998). Heterogeneity and a coiled-coil prediction of trypanosomatid-like flagellar rod proteins in Euglena. J. Euk. Microbiol. 45, 323-333.
29. Ngo, H. M., Tschudi, C., Gull, K. and Ullu, E. (1998). Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Nat. Acad. Sci. USA 95, 14687-14692.
30. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998). Randomization of left-right asymmetry due to loss of a nodal cilia regenerating leftward flow of extraembryonic fluid in mice lacking KIF-3B motor protein. Cell 95, 829-837.
31. Pazour, G. J., Wilkerson, C. G. and Witman, G. B. (1998). A dynein light chain is essential for the retrograde particle movement of intraflagellar transport. J. Cell Biol. 141, 979-992.
32. Pazour G. J., Dickert, B. L. and Witman, G. B. (1999). The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144, 473-481.
33. Piperno, G., Huang, B. and Luck, D. (1977). Two dimensional analysis of flagellar proteins from wild-type and paralyzed mutants of Chlamydomonas reinhardtii. Proc. Nat. Acad, Sci. USA 74, 1600-1604.
34. fla10 to reach the distal part of the flagella in Chlamydamonas. J. Cell Biol. 133, 371-379.
35. Porter, M. E., Bower, R., Knott, J. A., Byrd, P. and Dentler, W. (1999). Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell 10, 693-712.
36. Robinson, D. R. and Gull, K. (1991). Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature 352, 731-733.
37. Rosenbaum, J. L., Moulder, J. E. and Ringo, D. L. (1969). Flagellar elongation and shortening in Chlamydomonas. J. Cell Biol. 41, 600-619.
38. Rosenbaum, J. L., Cole, D. G. and Diener, D. R. (1999). Intraflagellar transport: the eyes have it. J. Cell Biol. 144, 385-388.
39. Russell, D. G. Newsham, R. J., Palmer, G. C. and Gull, K. (1983). Structural and biochemical characterization of the paraflagellar rod structure of Crithidia fasciculata. Eur. J. Cell Biol. 30, 137-143.
40. Santrich, C., Moore, L., Bastin, P., Sherwin, T., Brokaw, C., Gull, K. and Lebowitz, J. H. (1997). A motility function for the paraflagellar rod in Leishmania parasites revealed by PFR-2 gene knockoutş. Mol. Biochem. Parasitol. 90, 95-109.
41. Schlaeppi, K., Deflorin, J. and Seebeck, T. (1989). The major component of the paraflagellar rod of Trypanosoma brucei is a helical protein that is encoded by two identical, tandemly linked genes. J. Cell Biol. 109, 1695-1709.
42. Scott, V., Sherwin, T. and Gull, K. (1997). γ-Tubulin in trypanosomes: molecular characterisation and localisation to multiple and diverse microtubule organising centres. J. Cell Sci. 110, 157-168.
43. Shakir, M. A., Fukushige, T., Yasuda, H., Miwa, J. and Siddiqui, S. S. (1993). C. elegans osm-3 gene mediating osmotic avoidance behaviour encodes a kinesin-like protein. Neuroreport 4, 891-894.
44. Sherman, D. R., Janz, L., Hug., M. and Clayton, C. E. (1991). Anatomy of the parp gene promoter of Trypanosoma brucei. EMBO J. 10, 3379-3386.
45. Sherwin, T., Schneider, A., Sasse, R., Seebeck, T. and Gull, K. (1987). Distinct localisation and cell cycle dependence of COOH terminally tyrosinolated α-tubulin in the microtubules of Trypanosoma brucei. J. Cell Biol. 104, 439-446.
46. Sherwin, T. and Gull, K. (1989a). Visualization of detyrosination along single microtubules reveals novel mechanisms of assembly during cytoskeletal duplication in trypanosomes. Cell 57, 211-221.
47. Sherwin, T. and Gull, K. (1989b). The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeleton modifications. Phil. Trans. R. Soc. London Ser. B 323, 575-588.
48. Tabish, M., Siddiqui, Z. K., Nishikawa, K. and Siddiqui, S. S. (1995). Exclusive expression of C. elegans osm-3 kinesin gene in chemosensory neurons open to external environment. J. Mol. Biol. 247, 377-389.
49. ten Asbroek, A. L. M. A., Ouellette, M. and Borst, P. (1990). Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 348, 174-175.
50. Vickerman, K. (1962). The mechanism of cyclical development in trypanosomes of the Trypanosoma brucei subgroup: a hypothesis based on ultrastruetural observations. Trans. R. Soc. Trop. Med. Hyg. 56, 487-495.
51. Vickerman, K. and Preston, T. M. (1976). Comparative cell biology of the Trypanosomatids. In Biology of the Kinetoplastida, vol. 1 (ed. W. H. R. Lumsden and D. A. Evans), pp. 35-130. Academic Press.
52. Witman, G. B. (1975). The site of in vivo assembly of flagellar microtubules. Ann. NY Acad. Sci. 253, 178-191.
53. Woods, A., Sherwin, T., Sasse, R., MacRae, T. H., Baines, A. and Gull, K. (1989). Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93, 491-500.
54. Woodward, R. and Gull, K. (1990). Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J. Cell Sci. 95, 49-57.
55. Woodward, R., Carden, M. J. and Gull, K. (1994). Molecular characterisation of a novel, repetitive protein of the paraflagellar rod in Trypanosoma brucei. Mol. Biochem. Parasitol. 67, 31-39.
56. Woodward, R., Carden, M. J. and Gull, K. (1995). Immunological characterization of cytoskeletal proteins associated with the basal body, axoneme and flagellum attachment zone of Trypanosoma brucei. Parasitology 111, 77-85.
57. Wu, Y. M., Haghighat, N. G and Ruben, L. (1992). The predominant calcimedins from Trypanosoma brucei comprise a family of flagellar EF-hand calcium-binding proteins Biochem J. 287, 187-193.
58. Wu, Y. M., Deford, J., Benjamin, R., Lee, M. G. S. and Ruben, L. (1994). The gene family of EF-hand calcium binding proteins from the flagellum of Trypanosoma brucei. Biochem J. 304, 833-841.