Assembly and function of complex flagellar structures illustrated by the paraflagellar rod of trypanosomes

Protist

Volumn 150, Issue 2, 1999, Pages 113-123

  Bastin, Philippe ^a   Gull, Keith ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; INVERTEBRATA; TRYPANOSOMA;

EID: 0033180543     PISSN: 14344610     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1434-4610(99)70015-5     Document Type: Article

References (75)

1. al-Shammary FJ, Shoukrey NM, al-Shewemi SE, Ibrahim EA, al-Zahrani MA, al-Tujwaijri AS (1995) Leishmania major: in vitro ultrastructural study of the paraxial rod of promastigotes. Int J Parasitol 25: 443-452
2. Baccetti B (1986) Evolutionary trends in sperm structure. Comp Biochem Physiol 85A: 29-36
3. Bastin P, Matthews KR, Gull K (1996a) The paraflagellar rod of Kinetoplastida: solved and unsolved questions. Parasitol Today 12: 302-307
4. Bastin P, Bagherzadeh A, Matthews KR, Gull K (1996b) A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol Biochem Parasitol 77: 235-239
5. Bastin P, Sherwin T, Gull K (1998) Paraflagellar rod is essential to trypanosome motility. Nature 391: 548
6. Bastin P, MacRae T, Francis SB, Matthews KR, Gull K (1999a) submitted
7. Bastin P, Ellis K, Kohl L, Gull K (1999b) submitted
8. Bastin P, Pullen T, Sherwin T, Gull K (1999c) submitted
9. Beard CA, Saborio JL, Tewari D, Krieglstein KG, Henschen AH, Mannings JE (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
10. Birkett CR, Parma AE, Gerke-Bonet R, Woodward R, Gull K (1992) Isolation of cDNA clones encoding proteins of complex structures: analysis of the Trypanosoma brucei cytoskeleton. Gene 110: 65-70
11. Bloch M, Johnson KA (1995) Identification of a molecular chaperone in the eukaryotic flagellum and its localization to the site of microtubule assembly. J Cell Sci 108: 3541-3545
12. Cachon J, Cachon M, Cosson MP, Cosson J (1988) The paraflagellar rod: a structure in search of a function. Biol Cell 63: 169-181
13. Cole D, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL (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
14. Cruz, AK, Titus R, Beverley SM (1991) Plasticity in chromosome number and testing of essential genes in Leishmania by targeting. Proc Natl Acad Sci USA 90: 1599-1603
15. Deflorin J, Rudolf M, 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
16. De Souza W, Souto-Padron T (1980) The paraxial structure of the flagellum of Trypanosomatidae. J Parasitol 66: 229-235
17. Eid J, Sollner-Webb B (1991) Stable integrative transformation of Trypanosoma brucei that occurs exclusively by homologous recombination. Proc Natl Acad Sci USA 88: 2118-2121
18. 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
19. Fok AK, Wang H, Katayama A, Aihira MS, Allen RD (1994) 22S axonemal dynein is preassembled and functional prior to being transported and attached on the axonemes. Cell Motil Cytoskeleton 29: 215-224
20. Fouts DL, Stryker GA, Gorski KS, Miller MJ, Nguyen TV, Wrightsman RA, Manning JE (1998) Evidence for four major distinct protein components for the paraflagellar rod of Trypanosoma cruzi. J Biol Chem 273: 21846-21855
21. Fuge H (1969) Electron microscopic studies on the intra-flagellar structures of trypanosomes. J Protozool 16: 460-466
22. Gallo JM, Schrevel J (1985) Homologies between paraflagellar rod proteins from trypanosomes and euglenoids revealed by a monoclonal antibody. Eur J Cell Biol 36: 163-168
23. Han JW, Park JH, Kim M, Lee J (1997) mRNAs for microtubule proteins are specifically colocalized during the sequential formation of basal body, flagella, and cytoskeletal microtubules in the differentiation of Naegleria gruben. J Cell Biol 137: 871-879
24. Hemphill A, Lawson D, Seebeck T (1991a) The cytoskeletal architecture of Trypanosoma brucei. J Parasitol 77: 603-612
25. Hemphill A, Seebeck T, Lawson D (1991b) The Trypanosoma brucei cytoskeleton: ultrastructure and localization of microtubule-associated and spectrin-like proteins using quick-freeze deep-etch, immunogold electron microscopy. J Struct Biol 107: 211-220
26. Holwill MEJ (1965) The motion of Strigomonas oncopelti. J Exp Biol 42: 125-137
27. Hunger-Glaser I, Seebeck T (1997) Deletion of the genes for the paraflagellar rod protein PFR-A in Trypanosoma brucei is probably lethal. Mol Biochem Parasitol 90: 347-351
28. Hyams J (1982) The Euglena paraflagellar rod: structure, relationship to other flagellar components and preliminary biochemical characterization. J Cell Sci 55: 199-210
29. Imboden M, Muller N, Hemphill A, Mattioli R, Seebeck T (1995) Repetitive proteins from the flagellar cytoskeleton of African trypanosomes are diagnostically useful antigens. Parasitology 110: 249-258
30. Ismach R, Cianci CM, Caulfield JP, Langer PJ, Hein A, McMahon-Pratt D (1989) Flagellar membrane and paraxial rod proteins of Leishmania: characterization employing monoclonal antibodies. J Protozool 36: 617-624
31. Johnson KA, Rosenbaum JL (1992) Polarity of flagellar assembly in Chlamydomonas. J Cell Biol 119: 1605-1611
32. Johnson KA, Rosenbaum JL (1993) Flagellar regeneration in Chlamydomonas: a model system for studying organelle assembly. Trends Cell Biol 3: 156-161
33. Kohl L, Gull K (1998) Molecular architecture of the trypanosome cytoskeleton. Mol Biochem Parasitol 93: 1-9
34. Kohl L, Sherwin T, Gull K (1999) Assembly of the paraflagellar rod and of the flagellum attachement zone complex in Trypanosoma brucei. J Euk Microbiol 46: 105-109
35. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90: 5519-5523
36. Kozminski KG, Beech P, Rosenbaum JL (1995) The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131: 1517-1527
37. Lee MGS, Van der Ploeg LHT (1990) Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei. Science 250: 1583-1587
38. Lindemann CB (1994) Functional significance of the outer dense fibers of mammalian sperm examined by computer simulations with the geometric clutch model. Cell Motil Cytoskeleton 34: 258-270
39. Lupas A (1996) Prediction and analysis of coiled-coil structures. Meth Enzymol 266: 513-525
40. Marszalek J, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LSB (1999) Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96: 5043-5048
41. Meyer P (1968) The fine structure of the flagellum and kinetoplast-chondriome of Trypanosoma (Schizotrypanum) cruzi in tissue culture. J Protozool 15: 614-621
42. Miller MJ, Wrightsman RA, Stryker GA, Manning JE (1997) Protection of mice against Trypanosoma cruzi by immunization with paraflagellar rod proteins requires T cell, but not B cell, function. J Immunol 158: 5330-5337
43. Moore L, Santrich C, LeBowitz JH (1996) Stage-specific expression of the Leishmania mexicana paraflagellar rod protein PFR-2. Mol Biochem Parasitol 80: 125-135
44. Morris RL, Scholey JM (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
45. Nonaka S., Tanaka Y, Okada Y, Takeda S, Harada A, Kania Y, Kido M, 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
46. Ngo HM, Bouck GB (1998) Heterogeneity and a coiled-coil prediction of trypanosomatid-like flagellar rod proteins in Euglena J Euk Microbiol 45: 323-333
47. Pazour GJ, Wilkerson CG, Witman GB (1998) A dynein light chain is essential for the retrograde particle movement of intraflagellar transport. J Cell Biol 141: 979-992
48. Pazour GJ, Dickert BL, Witman GB (1999) The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J Cell Biol 144: 473-481
49. Piperno G, Huang B, Luck D (1977) Two dimensional analysis of flagellar proteins from wild-type and paralyzed mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 74: 1600-1604
50. Fla10 to reach the distal part of the flagella in Chlamydomonas. J Cell Biol 133: 371-379
51. Piperno G, Mead K (1997) Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagellum. Proc Natl Acad Sci USA 94: 4457-4462
52. Porter ME, Bower R, Knott JA, Byrd P, Dentier W (1999) Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell 10: 693-712
53. Rosenbaum JL, Child FM (1967) Flagellar regeneration in protozoan flagellates. J Cell Biol 34: 345-364
54. Rosenbaum JL, Cole DG, Diener DR (1999) Intraflagellar transport: the eyes have it. J Cell Biol 144: 385-388
55. Ruben L, Patton CL (1986) Calmodulin from Trypanosoma brucei: immunological analysis and genomic organization. Meth Enzymol 139: 262-276
56. Russell, DG Newsham RJ, Palmer GC, Gull K (1983) Structural and biochemical characterization of the paraflagellar rod structure of Crithidia fasciculata. Eur J Cell Biol 30: 137-143
57. Saborio JL, Hernandes JM, Narayanswami S, Wrightsman R, Palmer E, Manning JE (1989) Isolation and characterization of paraflagellar proteins from Trypanosoma cruzi. J Biol Chem 264: 4071-4075
58. Santrich C, Moore L, Bastin P, Sherwin T, Brokaw C, Gull K, Lebowitz JH (1997) A motility function for the paraflagellar rod in Leishmania parasites revealed by PFR-2 gene knockouts. Mol Biochem Parasitol 90: 95-109
59. Schlaeppi K, Deflorin J, 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
60. Shakir MA, Fukushige T, Yasuda H, Miwa J, Siddiqui SS (1993) C. elegans osm-3 gene mediating osmotic avoidance behaviour encodes a kinesin-like protein. Neuroreport 4: 891-894
61. Sherwin T, Gull K (1989a) 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
62. Sherwin T, Gull K (1989b) Visualization of detyrosination along single microtubules reveals novel mechanisms of assembly during cytoskeletal duplication in trypanosomes. Cell 57: 211-221
63. Snapp EL, Landfear SM (1997) Cytoskeletal association is important for differential targeting of glucose transporter isoforms in Leishmania. J Cell Biol 139: 1775-1783
64. Stephens RE (1994) Tubulin and tektin in sea urchin embryonic cilia: pathways of protein incorporation during turnover and regeneration. J Cell Sci 107: 683-692
65. Tabish M, Siddiqui ZK, Nishikawa K, Siddiqui SS (1995) Exclusive expression of C.elegans osm-3 kinesin gene in chemosensory neurons open to external environment. J Mol Biol 247: 377-389
66. ten Asbroek ALMA, Ouellette M, Borst P (1990) Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 348: 174-175
67. Vickerman K (1962) The mechanism of cyclical development in trypanosomes of the Trypanosoma brucei subgroup: a hypothesis based on ultrastructural observations. Trans R Soc Trop Med Hyg 56: 487-495
68. Vickerman K, Preston TM (1976) Comparative Cell Biology of the Trypanosomatids. In Lumsden WHR, Evans DA (eds) Biology of the Kinetoplastida, Vol. 1, Academic Press, London, pp 35-130
69. Walker PJ (1961) Organisation and function of the trypanosome flagella. Nature 189: 1017-1018
70. Westhoff D, Kamp G (1997) Glyceraldehyde-3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J Cell Sci 110: 1821-1829
71. Wirtz LE, Clayton CE (1995) Inducible gene expression in trypanosomes mediated by a procaryotic repressor. Science 268: 1179-1183
72. Woods A, Sherwin T, Sasse R, MacRae TH, Baines A, 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
73. Woodward R, Carden MJ, Gull K (1994) Molecular characterisation of a novel, repetitive protein of the paraflagellar rod in Trypanosoma brucei. Mol Biochem Parasitol 67: 31-39
74. Woodward R, Carden MJ, 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
75. Wrightsman RA, Miller MJ, Saborio JL, Manning JE (1995) Pure paraflagellar rod protein protects mice against Trypanosoma cruzi infection. Infect Immun 63: 122-125