Tracking the biogenesis and inheritance of subpellicular microtubule in trypanosoma brucei with inducible YFP- α-tubulin

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Sheriff, Omar ^a   Lim, Li Fern ^a   He, Cynthia Y ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; FUNGAL PROTEIN; UNCLASSIFIED DRUG; YELLOW FLUORESCENCE PROTEIN ALPHA TUBULIN; HYBRID PROTEIN; PHOTOPROTEIN; TUBULIN;

ARTICLE; CELL DIVISION; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; CELL TRACKING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IN VIVO STUDY; KINETOPLAST; MICROTUBULE; MICROTUBULE ASSEMBLY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; START CODON; TRYPANOSOMA BRUCEI; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; REPORTER GENE; TRYPANOSOMA RHODESIENSE;

CELL LINE; GENES, REPORTER; LUMINESCENT PROTEINS; MICROTUBULES; RECOMBINANT FUSION PROTEINS; TRYPANOSOMA BRUCEI RHODESIENSE; TUBULIN;

EID: 84899570976     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/893272     Document Type: Article

References (55)

1. Robinson D. R., Sherwin T., Ploubidou A., Byard E. H., Gull K., Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell cycle. Journal of Cell Biology 1995 128 6 1163 1172 2-s2.0-0028935746 10.1083/jcb.128.6.1163
2. He C. Y., Ho H. H., Malsam J., Chalouni C., West C. M., Ullu E., Toomre D., Warren G., Golgi duplication in Trypanosoma brucei. Journal of Cell Biology 2004 165 3 313 321 2-s2.0-2442451357 10.1083/jcb.200311076
3. Balaban N., Goldman R., Isolation and characterization of a unique 15 kilodalton trypanosome subpellicular microtubule-associated protein. Cell Motility and the Cytoskeleton 1992 21 2 138 146 2-s2.0-0026683673 10.1002/cm.970210207
4. Woods A., Baines A. J., Gull K., A high molecular mass phosphoprotein defined by a novel monoclonal antibody is closely associated with the intermicrotubule cross bridges in the Trypanosoma brucei cytoskeleton. Journal of Cell Science 1992 103, part 3 665 675 2-s2.0-0027102657
5. Detmer E., Hemphill A., Müller N., Seebeck T., The Trypanosoma brucei autoantigen 1/6 is an internally repetitive cytoskeletal protein. European Journal of Cell Biology 1997 72 4 378 384 2-s2.0-0030895509
6. Sherwin T., Gull K., The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philosophical transactions of the Royal Society of London. B: Biological sciences 1989 323 1218 573 588 2-s2.0-0024967876
7. Hemphill A., Lawson D., Seebeck T., The cytoskeletal architecture of Trypanosoma brucei. Journal of Parasitology 1991 77 4 603 612 2-s2.0-0026005768
8. Scott V., Sherwin T., Gull K., γ -Tubulin in trypanosomes: molecular characterisation and localisation to multiple and diverse microtubule organising centres. Journal of Cell Science 1997 110, part 2 157 168 2-s2.0-0031049074
9. McKean P. G., Baines A., Vaughan S., Gull K., γ -Tubulin functions in the nucleation of a discrete subset of microtubules in the eukaryotic flagellum. Current Biology 2003 13 7 598 602 2-s2.0-0037380134 10.1016/S0960-9822(03)00174-X
10. Gull K., The cytoskeleton of trypanosomatid parasites. Annual Review of Microbiology 1999 53 629 655 2-s2.0-0032724638 10.1146/annurev.micro.53.1.629
11. Farr H., Gull K., Cytokinesis in trypanosomes. Cytoskeleton 2012 69 931 941
12. Zhou Q., Liu B., Sun Y., He C. Y., A coiled-coil- and C2-domain-containing protein is required for FAZ assembly and cell morphology in Trypanosoma brucei. Journal of Cell Science 2011 124 22 3848 3858 2-s2.0-84856808159 10.1242/jcs.087676
13. Wheeler R. J., Scheumann N., Wickstead B., Gull K., Vaughan S., Cytokinesis in Trypanosoma brucei differs between bloodstream and tsetse trypomastigote forms: implications for microtubule-based morphogenesis and mutant analysis. Molecular Microbiology 2013 90 6 1339 1355
14. Kilmartin J. V., Wright B., Milstein C., Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. Journal of Cell Biology 1982 93 3 576 582 2-s2.0-0020265993
15. Sherwin T., Gull K., Visualization of detyrosination along single microtubules reveals novel mechanisms of assembly during cytoskeletal duplication in trypanosomes. Cell 1989 57 2 211 221 2-s2.0-0024591582
16. Matthews K. R., Sherwin T., Gull K., Mitochondrial genome repositioning during the differentiation of the African trypanosome between life cycle forms is microtubule mediated. Journal of Cell Science 1995 108 6 2231 2239 2-s2.0-0029064231
17. Andre J., Kerry L., Qi X., An alternative model for the role of RP2 in flagellum assembly in the African trypanosome. The Journal of Biological Chemistry 2013 289 464 475
18. Ruben L., Egwuagu C., Patton C. L., African trypanosomes contain calmodulin which is distinct from host calmodulin. Biochimica et Biophysica Acta-General Subjects 1983 758 2 104 113 2-s2.0-0020959336 10.1016/0304-4165(83) 90290-8
19. Wirtz E., Leal S., Ochatt C., Cross G. A. M., A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Molecular and Biochemical Parasitology 1999 99 1 89 101 2-s2.0-0033525524 10.1016/S0166-6851(99)00002-X
20. Zhou Q., Gheiratmand L., Chen Y., Lim T. K., Zhang J., Li S., Xia N., Liu B., Lin Q., He C. Y., A comparative proteomic analysis reveals a new bi-lobe protein required for bi-lobe duplication and cell division in Trypanosoma brucei. PloS One 2010 5 3, article e9660 2-s2.0-79952116623
21. Bangs J. D., Brouch E. M., Ransom D. M., Roggy J. L., A soluble secretory reporter system in Trypanosoma brucei. Studies on endoplasmic reticulum targeting. The Journal of Biological Chemistry 1996 271 31 18387 18393 2-s2.0-0029764290 10.1074/jbc.271.31.18387
22. Morriswood B., He C. Y., Sealey-Cardona M., Yelinek J., Pypaert M., Warren G., The bilobe structure of Trypanosoma brucei contains a MORN-repeat protein. Molecular and Biochemical Parasitology 2009 167 2 95 103 2-s2.0-67649359323 10.1016/j.molbiopara.2009.05.001
23. Redmond S., Vadivelu J., Field M. C., RNAit: an automated web-based tool for the selection of RNAi targets in Trypanosoma brucei. Molecular and Biochemical Parasitology 2003 128 1 115 118 2-s2.0-0037466382 10.1016/S0166-6851(03)00045-8
24. Wickstead B., Ersfeld K., Gull K., Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Molecular and Biochemical Parasitology 2002 125 1-2 211 216 2-s2.0-0036860235
25. Kohl L., Sherwin T., Gull K., Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. Journal of Eukaryotic Microbiology 1999 46 2 105 109 2-s2.0-0033105686
26. Ismach R., Cianci C. M., Caulfield J. P., Langer P. J., Hein A., McMahon-Pratt D., Flagellar membrane and paraxial rod proteins of Leishmania: characterization employing monoclonal antibodies. Journal of Protozoology 1989 36 6 617 624 2-s2.0-0024763154
27. Gheiratmand L., Brasseur A., Zhou Q., He C. Y., Biochemical characterization of the bi-lobe reveals a continuous structural network linking the bi-lobe to other single-copied organelles in Trypanosoma brucei. The Journal of Biological Chemistry 2013 288 3489 3499
28. Meijering E., Dzyubachyk O., Smal I., Methods for cell and particle tracking. Methods in Enzymology 2012 504 183 200 2-s2.0-84855958004 10.1016/B978-0-12-391857-4.00009-4
29. Seebeck T., Whittaker P. A., Imboden M. A., Hardman N., Braun R., Tubulin genes of Trypanosoma brucei: a tightly clustered family of alternating genes. Proceedings of the National Academy of Sciences of the United States of America 1983 80 15 4634 4638 2-s2.0-0020803222
30. Sather S., Agabian N., A 5′ spliced leader is added in trans to both α-and β -tubulin transcripts in Trypanosoma brucei. Proceedings of the National Academy of Sciences of the United States of America 1985 82 17 5695 5699 2-s2.0-0022339563
31. Kimmel B. E., Samson S., Wu J., Hirschberg R., Yarbrough L. R., Tubulin genes of the African trypanosome Trypanosoma brucei rhodesiense: nucleotide sequence of a 3.7-kb fragment containing genes for alpha and beta tubulins. Gene 1985 35 3 237 248 2-s2.0-0022257583 10.1016/0378-1119(85)90002-2
32. Carminati J. L., Stearns T., Microtubules orient the mitotic spindle in yeast through dynein- dependent interactions with the cell cortex. Journal of Cell Biology 1997 138 3 629 641 2-s2.0-0030750203 10.1083/jcb.138.3.629
33. Weinstein B., Solomon F., Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: differences between alpha-tubulin and beta-tubulin. Molecular and Cellular Biology 1990 10 10 5295 5304 2-s2.0-0025075301
34. Andresen M., Schmitz-Salue R., Jakobs S., Short tetracysteine tags to β -tubulin demonstrate the significance of small labels for live cell imaging. Molecular Biology of the Cell 2004 15 12 5616 5622 2-s2.0-9444247617 10.1091/mbc.E04-06-0454
35. Rusan N. M., Fagerstrom C. J., Yvon A.-M. C., Wadsworth P., Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein- α tubulin. Molecular Biology of the Cell 2001 12 4 971 980 2-s2.0-0035168410
36. Goodson H. V., Dzurisin J. S., Wadsworth P., Methods for expressing and analyzing GFP-tubulin and GFP-microtubule-associated proteins. Cold Spring Harbor Protocols 2010 5 9 2-s2.0-77958089300 10.1101/pdb.top85
37. Bastin P., Bagherzadeh A., Matthews K. R., Gull K., A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Molecular and Biochemical Parasitology 1996 77 2 235 239 2-s2.0-0029894292 10.1016/0166-6851(96)02598-4
38. Schneider A., Plessmann U., Weber K., Subpellicular and flagellar microtubules of Trypanosoma brucei are extensively glutamylated. Journal of Cell Science 1997 110, part 4 431 437 2-s2.0-0031049174
39. Bastin P., MacRae T. H., Francis S. B., Matthews K. R., Gull K., Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of trypanosomes. Molecular and Cellular Biology 1999 19 12 8191 8200 2-s2.0-0033500153
40. Sasse R., Gull K., Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei. Journal of Cell Science 1988 90, part 4 577 589 2-s2.0-0024065220
41. Bu W., Su L.-K., Characterization of functional domains of human EB1 family proteins. The Journal of Biological Chemistry 2003 278 50 49721 49731 2-s2.0-0346749538 10.1074/jbc.M306194200
42. Honnappa S., John C. M., Kostrewa D., Winkler F. K., Steinmetz M. O., Structural insights into the EB1-APC interaction. EMBO Journal 2005 24 2 261 269 2-s2.0-13444267357 10.1038/sj.emboj.7600529
43. Honnappa S., Gouveia S. M., Weisbrich A., Damberger F. F., Bhavesh N. S., Jawhari H., Grigoriev I., van Rijssel F. J. A., Buey R. M., Lawera A., Jelesarov I., Winkler F. K., Wüthrich K., Akhmanova A., Steinmetz M. O., An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009 138 2 366 376 2-s2.0-67650627616 10.1016/j.cell.2009.04.065
44. Skube S. B., Chaverri J. M., Goodson H. V., Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo. Cytoskeleton 2010 67 1 1 12 2-s2.0-77649086983 10.1002/cm.20409
45. Gunawardane R. N., Martin O. C., Cao K., Zhang L., Dej K., Iwamatsu A., Zheng Y., Characterization and reconstitution of Drosophila γ -tubulin ring complex subunits. Journal of Cell Biology 2000 151 7 1513 1524 2-s2.0-0034739840 10.1083/jcb.151.7.1513
46. Zimmerman S., Chang F., Effects of γ -tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Molecular Biology of the Cell 2005 16 6 2719 2733 2-s2.0-19644364761 10.1091/mbc.E04-08-0676
47. Cuschieri L., Miller R., Vogel J., γ -Tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast. Molecular Biology of the Cell 2006 17 10 4420 4434 2-s2.0-33749472453 10.1091/mbc.E06-03-0245
48. Sun S. Y., Wang C., Yuan Y. A., He C. Y., An intracellular membrane junction consisting of flagellum adhesion glycoproteins links flagellum biogenesis to cell morphogenesis in Trypanosoma brucei. Journal of Cell Science 2013 126, part 2 520 531
49. Lacount D. J., Barrett B., Donelson J. E., Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. The Journal of Biological Chemistry 2002 277 20 17580 17588 2-s2.0-0037124117 10.1074/jbc.M200873200
50. Robinson D. R., Gull K., Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature 1991 352 6337 731 733 2-s2.0-0025773091 10.1038/352731a0
51. Absalon S., Kohl L., Branche C., Blisnick T., Toutirais G., Rusconi F., Cosson J., Bonhivers M., Robinson D., Bastin P., Basal body positioning is controlled by flagellum formation in Trypanosoma brucei. PLoS ONE 2007 2 5, article e437 2-s2.0-55849123576 10.1371/journal.pone.0000437
52. Dawe H. R., Farr H., Portman N., Shaw M. K., Gull K., The Parkin co-regulated gene product, PACRG, is an evolutionarily conserved axonemal protein that functions in outer-doublet microtubule morphogenesis. Journal of Cell Science 2005 118 23 5421 5430 2-s2.0-30544436017 10.1242/jcs.02659
53. 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., Gull K., Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 2006 440 7081 224 227 2-s2.0-33644858832 10.1038/nature04541
54. Absalon S., Blisnick T., Bonhivers M., Kohl L., Cayet N., Toutirais G., Buisson J., Robinson D., Bastin P., Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei. Journal of Cell Science 2008 121 22 3704 3716 2-s2.0-59549102746 10.1242/jcs.035626
55. Lacomble S., Vaughan S., Gadelha C., Morphew M. K., Shaw M. K., McIntosh J. R., Gull K., Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. Journal of Cell Science 2009 122 8 1081 1090 2-s2.0-66849128079 10.1242/jcs.045740