Proteomics and the Trypanosoma brucei cytoskeleton: Advances and opportunities

Parasitology

Volumn 139, Issue 9, 2012, Pages 1168-1177

  Portman, Neil ^a   Gull, Keith ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Bilobe; cytoskeleton; flagella connector; flagellum; PFR; proteomic; Trypanosoma brucei

Indexed keywords

ADENYLATE KINASE; CALCIUM ION; CALPAIN;

ANIMAL EMBRYO; ARTICLE; AVIAN STOMACH; AXONEME; CHLAMYDOMONAS REINHARDTII; CHROMOSOME 8; CRITHIDIA; CRITHIDIA DEANEI; CYTOKINESIS; CYTOSKELETON; DAUGHTER CELL; DISEASE CARRIER; EMBRYO DEVELOPMENT; EPIMASTIGOTE; EUGLENA; EUGLENA GRACILLIS; EUKARYOTIC FLAGELLUM; HUMORAL IMMUNITY; KINETOPLASTIDA; LEISHMANIA; LYSOSOME; MICROBIAL DIVERSITY; NONHUMAN; PARAFLAGELLAR ROD; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEOMICS; SALIVARY GLAND; TRYPANOSOMA BRUCEI; TRYPOMASTIGOTE; TSETSE FLY;

ANIMALS; CYTOSKELETON; FLAGELLA; HUMANS; LIFE CYCLE STAGES; PROTEOMICS; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 84865034955     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012000443     Document Type: Article

References (61)

1. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Dore, G., Julkowska, D., Tavenet, A. and Bastin, P. (2008). Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Molecular Biology of the Cell 19, 929-944.
2. Absalon, S., Kohl, L., Branche, C., Blisnick, T., Toutirais, G., Rusconi, F., Cosson, J., Bonhivers, M., Robinson, D. and Bastin, P. (2007). Basal body positioning is controlled by flagellum formation in Trypanosoma brucei. Plos ONE 2(5), e437.
3. Barry, J. D. and McCulloch, R. (2001). Antigenic variation in trypanosomes: Enhanced phenotypic variation in a eukaryotic parasite. Advances in Parasitology 49, 1-70.
4. Bastin, P., Matthews, K. R. and Gull, K. (1996). The paraflagellar rod of 1kinetoplastida: Solved and unsolved questions. Parasitology Today 12, 302-307.
5. Bastin, P., Sherwin, T. and Gull, K. (1998). Paraflagellar rod is vital for trypanosome motility. Nature 391, 548.
6. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B., Bohme, U., Hannick, L., Aslett, M. A., Shallom, J., Marcello, L., Hou, L., Wickstead, B., Alsmark, U. C., Arrowsmith, C., Atkin, R. J., Barron, A. J., Bringaud, F., Brooks, K., Carrington, M., Cherevach, I., Chillingworth, T. J., Churcher, C., Clark, L. N., Corton, C. H., Cronin, A., Davies, R. M., Doggett, J., Djikeng, A., Feldblyum, T., Field, M. C., Fraser, A., Goodhead, I., Hance, Z., Harper, D., Harris, B. R., Hauser, H., Hostetler, J., Ivens, A., Jagels, K., Johnson, D., Johnson, J., Jones, K., Kerhornou, A. X., Koo, H., Larke, N., Landfear, S., Larkin, C., Leech, V., Line, A., Lord, A., Macleod, A., Mooney, P. J., Moule, S., Martin, D. M., Morgan, G.W., Mungall, K., Norbertczak, H., Ormond, D., Pai, G., Peacock, C. S., Peterson, J., Quail, M. A., Rabbinowitsch, E., Rajandream, M. A., Reitter, C., Salzberg, S. L., Sanders, M., Schobel, S., Sharp, S., Simmonds, M., Simpson, A. J., Tallon, L., Turner, C. M., Tait, A., Tivey, A. R., Van Aken, S., Walker, D., Wanless, D., Wang, S., White, B., White, O., Whitehead, S., Woodward, J., Wortman, J., Adams, M. D., Embley, T. M., Gull, K., Ullu, E., Barry, J. D., Fairlamb, A. H., Opperdoes, F., Barrell, B. G., Donelson, J. E., Hall, N., Fraser, C. M., and et al. (2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416-422.
7. Bonhivers, M., Nowacki, S., Landrein, N. and Robinson, D. R. (2008). Biogenesis of the trypanosome endo-exocytotic organelle is cytoskeleton mediated. Plos Biology 6(5), e105.
8. Brems, S., Guilbride, D. L., Gundlesdodjir-Planck, D., Busold, C., Luu, V. D., Schanne, M., Hoheisel, J. and Clayton, C. (2005). The transcriptomes of Trypanosoma brucei Lister 427 and TREU927 bloodstream and procyclic trypomastigotes. Molecular and Biochemical Parasitology 139, 163-172.
9. Briggs, L. J., McKean, P. G., Baines, A., Moreira-Leite, F., Davidge, J., Vaughan, S. and Gull, K. (2004). The flagella connector of Trypanosoma brucei: An unusual mobile transmembrane junction. Journal of Cell Science 117, 1641-1651.
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. and Gull, K. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227.
11. Davidge, J. A., Chambers, E., Dickinson, H. A., Towers, K., Ginger, M. L., McKean, P. G. and Gull, K. (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.
12. Fenn, K. and Matthews, K. R. (2007). The cell biology of Trypanosoma brucei differentiation. Current Opinions in Microbiology 10, 539-546.
13. Gadelha, C., Wickstead, B., De Souza, W., Gull, K. and Cunha-e-Silva, N. (2005). Cryptic paraflagellar rod in endosymbiontcontaining kinetoplastid protozoa. Eukaryotic Cell 4, 516-525.
14. Gull, K. (1999). The cytoskeleton of trypanosomatid parasites. Annual Review of Microbiology 53, 629-655.
15. He, C. Y., Pypaert, M. and Warren, G. (2005). Golgi duplication in Trypanosoma brucei requires Centrin2. Science 310, 1196-1198.
16. Henley, G. L., Lee, C. M. and Takeuchi, A. (1978). Electron microscopy observations on Trypanosoma brucei: Freeze-cleaving and thin-sectioning study of the apical part of the flagellar pocket. Zeitschrift für Parasitenkunde 55, 181-187.
17. Hertz-Fowler, C., Ersfeld, K. and Gull, K. (2001). CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. Molecular and Biochemical Parasitology 116, 25-34.
18. Hirokawa, N., Tanaka, Y., Okada, Y. and Takeda, S. (2006). Nodal flow and the generation of left-right asymmetry. Cell 125, 33-45.
19. Horn, D. and McCulloch, R. (2010). Molecular mechanisms underlying the control of antigenic variation in African trypanosomes. Current Opinion in Microbiology 13, 700-705.
20. Hyams, J. S. (1982). The Euglena paraflagellar rod: Structure, relationship to other flagellar components and preliminary biochemical characterization. Journal of Cell Science 55, 199-210.
21. Jensen, B. C., Sivam, D., Kifer, C. T., Myler, P. J. and Parsons, M. (2009). Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10, 482.
22. Kabani, S., Fenn, K., Ross, A., Ivens, A., Smith, T. K., Ghazal, P. and Matthews, K. (2009). Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10, 427.
23. Koumandou, V. L., Natesan, S. K., Sergeenko, T. and Field, M. C. (2008). The trypanosome transcriptome is remodelled during differentiation but displays limited responsiveness within life stages.BMCGenomics 9, 298.
24. Kozminski, K. G., Johnson, K. A., Forscher, P. and Rosenbaum, J. L. (1993). A motility in the eukaryotic flagellum unrelated to flagellar beating. Proceedings of the National Academy of Sciences, USA 90, 5519-5523.
25. Lacomble, S., Portman, N. and Gull, K. (2009a). A protein-protein interaction map of the Trypanosoma brucei paraflagellar rod. Plos One 4 (11), e7685.
26. Lacomble, S., Vaughan, S., Gadelha, C., Morphew, M. K., Shaw, M. K., McIntosh, J. R. and Gull, K. (2009b). Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. Journal of Cell Science 122, 1081-1090.
27. LaCount, D. J., Barrett, B. and Donelson, J. E. (2002). Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. Journal of Biological Chemistry 277, 17580-17588.
28. Landfear, S. M. and Ignatushchenko, M. (2001). The flagellum and flagellar pocket of trypanosomatids. Molecular and Biochemical Parasitology 115, 1-17.
29. Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E. N., Rux, J. J., Speicher, D.W. and Pierce, E. A. (2007). The proteome of the mouse photoreceptor sensory cilium complex. Molecular and Cellular Proteomics 6, 1299-1317.
30. Matthews, K. R. and Gull, K. (1994). Evidence for an interplay between cell cycle progression and the initiation of differentiation between life cycle forms of African trypanosomes. Journal of Cell Biololgy 125, 1147-1156.
31. McGhee, R. B. and Cosgrove,W. B. (1980). Biology and physiology of the lower Trypanosomatidae. Microbiological Reviews 44, 140-173.
32. Moreira-Leite, F. F., Sherwin, T., Kohl, L. and Gull, K. (2001). A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science 294, 610-612.
33. Morriswood, B., He, C. Y., Sealey-Cardona, M., Yelinek, J., Pypaert, M. and Warren, G. (2009). The bilobe structure of Trypanosoma brucei contains a MORN-repeat protein. Molecular and Biochemical Parasitology 167, 95-103.
34. Nozaki, T., Haynes, P. A. and Cross, G. A. (1996). Characterization of the Trypanosoma brucei homologue of a Trypanosoma cruzi flagellum-adhesion glycoprotein. Molecular and Biochemical Parasitology 82, 245-255.
35. Oberholzer, M., Langousis, G., Nguyen, H. T., Saada, E. A., Shimogawa, M. M., Jonsson, Z. O., Nguyen, S. M., Wohlschlegel, J. A. and Hill, K. L. (2011). Independent analysis of the flagellum surface and matrix proteomes provides insight into flagellum signaling in mammalian-infectious Trypanosoma brucei. Molecular and Cellular Proteomics 10, M111.010538.
36. Ogbadoyi, E. O., Robinson, D. R. and Gull, K. (2003). A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Molecular Biology of the Cell 14, 1769-1779.
37. Olego-Fernandez, S., Vaughan, S., Shaw, M. K., Gull, K. and Ginger, M. L. (2009). Cell morphogenesis of Trypanosoma brucei requires the paralogous, differentially expressed calpain-related proteins CAP5.5 and CAP5.5 V. Protist 160, 576-590.
38. Ono, Y. and Sorimachi, H. (2012). Calpains - An elaborate proteolytic system. Biochimica et Biophysica Acta 1824, 224-236.
39. 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. Molecular and Cellular Proteomics 1, 451-465.
40. Pazour, G. J., Agrin, N., Leszyk, J. and Witman, G. B. (2005). Proteomic analysis of a eukaryotic cilium. Journal of Cell Biology 170, 103-113.
41. Portman, N. and Gull, K. (2010). The paraflagellar rod of kinetoplastid parasites: From structure to components and function. International Journal for Parasitology 40, 135-148.
42. Portman, N., Lacomble, S., Thomas, B., McKean, P. G. and Gull, K. (2009). Combining RNA interference mutants and comparative proteomics to identify protein components and dependences in a eukaryotic flagellum. Journal of Biological Chemistry 284, 5610-5619.
43. Pullen, T. J., Ginger, M. L., Gaskell, S. J. and Gull, K. (2004). Protein targeting of an unusual, evolutionarily conserved adenylate kinase to a eukaryotic flagellum. Molecular Biology of the Cell 15, 3257-3265.
44. 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.
45. Robinson, D. R., Sherwin, T., Ploubidou, A., Byard, E. H. and Gull, K. (1995). Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell cycle. Journal of Cell Biology 128, 1163-1172.
46. Rotureau, B., Subota, I. and Bastin, P. (2011). Molecular bases of cytoskeleton plasticity during the Trypanosoma brucei parasite cycle. Cellular Microbiology 13, 705-716.
47. Russell, D. G., Newsam, R. J., Palmer, G. C. and Gull, K. (1983). Structural and biochemical characterisation of the paraflagellar rod of Crithidia fasciculata. European Journal of Cell Biology 30, 137-143.
48. Santrich, C., Moore, L., Sherwin, T., Bastin, P., Brokaw, C., Gull, K. and LeBowitz, J. H. (1997). A motility function for the paraflagellar rod of Leishmania parasites revealed by PFR-2 gene knockouts. Molecular and Biochemical Parasitology 90, 95-109.
49. Sharma, R., Gluenz, E., Peacock, L., Gibson, W., Gull, K. and Carrington, M. (2009). The heart of darkness: Growth and form of Trypanosoma brucei in the tsetse fly. Trends in Parasitology 25, 517-524.
50. Sharma, R., Peacock, L., Gluenz, E., Gull, K., Gibson, W. and Carrington, M. (2008). Asymmetric cell division as a route to reduction in cell length and change in cell morphology in trypanosomes. Protist 159, 137-151.
51. Sherwin, T. and Gull, K. (1989). The cell division cycle of Trypanosoma brucei brucei: Timing of event markers and cytoskeletal modulations. Philosophical Transactions of the Royal Society B: Biological Sciences 323, 573-588.
52. Siegel, T. N., Hekstra, D. R., Wang, X., Dewell, S. and Cross, G. A. (2010). Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Research 38, 4946-4957.
53. 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. Journal of Proteome Research 4, 909-919.
54. Taylor, J. E. and Rudenko, G. (2006). Switching trypanosome coats: What,s in the wardrobe? Trends in Genetics 22, 614-620.
55. Tetley, L. and Vickerman, K. (1985). Differentiation in Trypanosoma brucei: Host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. Journal of Cell Science 74, 1-19.
56. Vaughan, S., Kohl, L., Ngai, I., Wheeler, R. J. and Gull, K. (2008). A repetitive protein essential for the flagellum attachment zone filament structure and function in Trypanosoma brucei. Protist 159, 127-136.
57. Vedrenne, C., Giroud, C., Robinson, D. R., Besteiro, S., Bosc, C., Bringaud, F. and Baltz, T. (2002). Two related subpellicular cytoskeletonassociated proteins in Trypanosoma brucei stabilize microtubules. Molecular Biology of the Cell 13, 1058-1070.
58. Vickerman, K. (1969). On the surface coat and flagellar adhesion in trypanosomes. Journal of Cell Science 5, 163-193.
59. Vickerman, K. (1985). Developmental cycles and biology of pathogenic trypanosomes. British Medical Bulletin 41, 105-114.
60. Woods, A., Sherwin, T., Sasse, R., MacRae, T. H., Baines, A. J. and Gull, K. (1989). Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. Journal of Cell Science 93, 491-500.
61. Zhou, Q., Gheiratmand, L., Chen, Y., Lim, T. K., Zhang, J., Li, S., Xia, N., Liu, B., Lin, Q. and He, C. Y. (2010). A comparative proteomic analysis reveals a new bi-lobe protein required for bi-lobe duplication and cell division in Trypanosoma brucei. Plos One 5(3), e9660.