Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 893272, 12 pages
http://dx.doi.org/10.1155/2014/893272
Research Article

Tracking the Biogenesis and Inheritance of Subpellicular Microtubule in Trypanosoma brucei with Inducible YFP-α-Tubulin

1Department of Biological Sciences, National University of Singapore, Singapore 117543
2Centre for BioImaging Sciences, National University of Singapore, Singapore 117546

Received 27 December 2013; Accepted 19 February 2014; Published 30 March 2014

Academic Editor: Wanderley de Souza

Copyright © 2014 Omar Sheriff et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. R. Robinson, T. Sherwin, A. Ploubidou, E. H. Byard, and K. Gull, “Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell cycle,” Journal of Cell Biology, vol. 128, no. 6, pp. 1163–1172, 1995. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Y. He, H. H. Ho, J. Malsam et al., “Golgi duplication in Trypanosoma brucei,” Journal of Cell Biology, vol. 165, no. 3, pp. 313–321, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Balaban and R. Goldman, “Isolation and characterization of a unique 15 kilodalton trypanosome subpellicular microtubule-associated protein,” Cell Motility and the Cytoskeleton, vol. 21, no. 2, pp. 138–146, 1992. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Woods, A. J. Baines, and K. Gull, “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, vol. 103, part 3, pp. 665–675, 1992. View at Google Scholar · View at Scopus
  5. E. Detmer, A. Hemphill, N. Müller, and T. Seebeck, “The Trypanosoma brucei autoantigen 1/6 is an internally repetitive cytoskeletal protein,” European Journal of Cell Biology, vol. 72, no. 4, pp. 378–384, 1997. View at Google Scholar · View at Scopus
  6. T. Sherwin and K. Gull, “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, vol. 323, no. 1218, pp. 573–588, 1989. View at Google Scholar · View at Scopus
  7. A. Hemphill, D. Lawson, and T. Seebeck, “The cytoskeletal architecture of Trypanosoma brucei,” Journal of Parasitology, vol. 77, no. 4, pp. 603–612, 1991. View at Google Scholar · View at Scopus
  8. V. Scott, T. Sherwin, and K. Gull, “γ-Tubulin in trypanosomes: molecular characterisation and localisation to multiple and diverse microtubule organising centres,” Journal of Cell Science, vol. 110, part 2, pp. 157–168, 1997. View at Google Scholar · View at Scopus
  9. P. G. McKean, A. Baines, S. Vaughan, and K. Gull, “γ-Tubulin functions in the nucleation of a discrete subset of microtubules in the eukaryotic flagellum,” Current Biology, vol. 13, no. 7, pp. 598–602, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Gull, “The cytoskeleton of trypanosomatid parasites,” Annual Review of Microbiology, vol. 53, pp. 629–655, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. H. Farr and K. Gull, “Cytokinesis in trypanosomes,” Cytoskeleton, vol. 69, pp. 931–941, 2012. View at Google Scholar
  12. Q. Zhou, B. Liu, Y. Sun, and C. Y. He, “A coiled-coil- and C2-domain-containing protein is required for FAZ assembly and cell morphology in Trypanosoma brucei,” Journal of Cell Science, vol. 124, no. 22, pp. 3848–3858, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. R. J. Wheeler, N. Scheumann, B. Wickstead, K. Gull, and S. Vaughan, “Cytokinesis in Trypanosoma brucei differs between bloodstream and tsetse trypomastigote forms: implications for microtubule-based morphogenesis and mutant analysis,” Molecular Microbiology, vol. 90, no. 6, pp. 1339–1355, 2013. View at Google Scholar
  14. J. V. Kilmartin, B. Wright, and C. Milstein, “Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line,” Journal of Cell Biology, vol. 93, no. 3, pp. 576–582, 1982. View at Google Scholar · View at Scopus
  15. T. Sherwin and K. Gull, “Visualization of detyrosination along single microtubules reveals novel mechanisms of assembly during cytoskeletal duplication in trypanosomes,” Cell, vol. 57, no. 2, pp. 211–221, 1989. View at Google Scholar · View at Scopus
  16. K. R. Matthews, T. Sherwin, and K. Gull, “Mitochondrial genome repositioning during the differentiation of the African trypanosome between life cycle forms is microtubule mediated,” Journal of Cell Science, vol. 108, no. 6, pp. 2231–2239, 1995. View at Google Scholar · View at Scopus
  17. J. Andre, L. Kerry, X. Qi et al., “An alternative model for the role of RP2 in flagellum assembly in the African trypanosome,” The Journal of Biological Chemistry, vol. 289, pp. 464–475, 2013. View at Google Scholar
  18. L. Ruben, C. Egwuagu, and C. L. Patton, “African trypanosomes contain calmodulin which is distinct from host calmodulin,” Biochimica et Biophysica Acta—General Subjects, vol. 758, no. 2, pp. 104–113, 1983. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Wirtz, S. Leal, C. Ochatt, and G. A. M. Cross, “A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 99, no. 1, pp. 89–101, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. Q. Zhou, L. Gheiratmand, Y. Chen et al., “A comparative proteomic analysis reveals a new bi-lobe protein required for bi-lobe duplication and cell division in Trypanosoma brucei,” PloS One, vol. 5, no. 3, article e9660, 2010. View at Google Scholar · View at Scopus
  21. J. D. Bangs, E. M. Brouch, D. M. Ransom, and J. L. Roggy, “A soluble secretory reporter system in Trypanosoma brucei. Studies on endoplasmic reticulum targeting,” The Journal of Biological Chemistry, vol. 271, no. 31, pp. 18387–18393, 1996. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Morriswood, C. Y. He, M. Sealey-Cardona, J. Yelinek, M. Pypaert, and G. Warren, “The bilobe structure of Trypanosoma brucei contains a MORN-repeat protein,” Molecular and Biochemical Parasitology, vol. 167, no. 2, pp. 95–103, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Redmond, J. Vadivelu, and M. C. Field, “RNAit: an automated web-based tool for the selection of RNAi targets in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 128, no. 1, pp. 115–118, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Wickstead, K. Ersfeld, and K. Gull, “Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 125, no. 1-2, pp. 211–216, 2002. View at Google Scholar · View at Scopus
  25. L. Kohl, T. Sherwin, and K. Gull, “Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle,” Journal of Eukaryotic Microbiology, vol. 46, no. 2, pp. 105–109, 1999. View at Google Scholar · View at Scopus
  26. R. Ismach, C. M. Cianci, J. P. Caulfield, P. J. Langer, A. Hein, and D. McMahon-Pratt, “Flagellar membrane and paraxial rod proteins of Leishmania: characterization employing monoclonal antibodies,” Journal of Protozoology, vol. 36, no. 6, pp. 617–624, 1989. View at Google Scholar · View at Scopus
  27. L. Gheiratmand, A. Brasseur, Q. Zhou, and C. Y. He, “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, vol. 288, pp. 3489–3499, 2013. View at Google Scholar
  28. E. Meijering, O. Dzyubachyk, and I. Smal, “Methods for cell and particle tracking,” Methods in Enzymology, vol. 504, pp. 183–200, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Seebeck, P. A. Whittaker, M. A. Imboden, N. Hardman, and R. Braun, “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, vol. 80, no. 15, pp. 4634–4638, 1983. View at Google Scholar · View at Scopus
  30. S. Sather and N. Agabian, “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, vol. 82, no. 17, pp. 5695–5699, 1985. View at Google Scholar · View at Scopus
  31. B. E. Kimmel, S. Samson, J. Wu, R. Hirschberg, and L. R. Yarbrough, “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, vol. 35, no. 3, pp. 237–248, 1985. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Carminati and T. Stearns, “Microtubules orient the mitotic spindle in yeast through dynein- dependent interactions with the cell cortex,” Journal of Cell Biology, vol. 138, no. 3, pp. 629–641, 1997. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Weinstein and F. Solomon, “Phenotypic consequences of tubulin overproduction in Saccharomyces cerevisiae: differences between alpha-tubulin and beta-tubulin,” Molecular and Cellular Biology, vol. 10, no. 10, pp. 5295–5304, 1990. View at Google Scholar · View at Scopus
  34. M. Andresen, R. Schmitz-Salue, and S. Jakobs, “Short tetracysteine tags to β-tubulin demonstrate the significance of small labels for live cell imaging,” Molecular Biology of the Cell, vol. 15, no. 12, pp. 5616–5622, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. N. M. Rusan, C. J. Fagerstrom, A.-M. C. Yvon, and P. Wadsworth, “Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-α tubulin,” Molecular Biology of the Cell, vol. 12, no. 4, pp. 971–980, 2001. View at Google Scholar · View at Scopus
  36. H. V. Goodson, J. S. Dzurisin, and P. Wadsworth, “Methods for expressing and analyzing GFP-tubulin and GFP-microtubule-associated proteins,” Cold Spring Harbor Protocols, vol. 5, no. 9, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Bastin, A. Bagherzadeh, K. R. Matthews, and K. Gull, “A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 77, no. 2, pp. 235–239, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Schneider, U. Plessmann, and K. Weber, “Subpellicular and flagellar microtubules of Trypanosoma brucei are extensively glutamylated,” Journal of Cell Science, vol. 110, part 4, pp. 431–437, 1997. View at Google Scholar · View at Scopus
  39. P. Bastin, T. H. MacRae, S. B. Francis, K. R. Matthews, and K. Gull, “Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of trypanosomes,” Molecular and Cellular Biology, vol. 19, no. 12, pp. 8191–8200, 1999. View at Google Scholar · View at Scopus
  40. R. Sasse and K. Gull, “Tubulin post-translational modifications and the construction of microtubular organelles in Trypanosoma brucei,” Journal of Cell Science, vol. 90, part 4, pp. 577–589, 1988. View at Google Scholar · View at Scopus
  41. W. Bu and L.-K. Su, “Characterization of functional domains of human EB1 family proteins,” The Journal of Biological Chemistry, vol. 278, no. 50, pp. 49721–49731, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Honnappa, C. M. John, D. Kostrewa, F. K. Winkler, and M. O. Steinmetz, “Structural insights into the EB1-APC interaction,” EMBO Journal, vol. 24, no. 2, pp. 261–269, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Honnappa, S. M. Gouveia, A. Weisbrich et al., “An EB1-binding motif acts as a microtubule tip localization signal,” Cell, vol. 138, no. 2, pp. 366–376, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. B. Skube, J. M. Chaverri, and H. V. Goodson, “Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo,” Cytoskeleton, vol. 67, no. 1, pp. 1–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. R. N. Gunawardane, O. C. Martin, K. Cao et al., “Characterization and reconstitution of Drosophila γ-tubulin ring complex subunits,” Journal of Cell Biology, vol. 151, no. 7, pp. 1513–1524, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Zimmerman and F. Chang, “Effects of γ-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast,” Molecular Biology of the Cell, vol. 16, no. 6, pp. 2719–2733, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Cuschieri, R. Miller, and J. Vogel, “γ-Tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast,” Molecular Biology of the Cell, vol. 17, no. 10, pp. 4420–4434, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Y. Sun, C. Wang, Y. A. Yuan, and C. Y. He, “An intracellular membrane junction consisting of flagellum adhesion glycoproteins links flagellum biogenesis to cell morphogenesis in Trypanosoma brucei,” Journal of Cell Science, vol. 126, part 2, pp. 520–531, 2013. View at Google Scholar
  49. D. J. Lacount, B. Barrett, and J. E. Donelson, “Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis,” The Journal of Biological Chemistry, vol. 277, no. 20, pp. 17580–17588, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. D. R. Robinson and K. Gull, “Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle,” Nature, vol. 352, no. 6337, pp. 731–733, 1991. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Absalon, L. Kohl, C. Branche et al., “Basal body positioning is controlled by flagellum formation in Trypanosoma brucei,” PLoS ONE, vol. 2, no. 5, article e437, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. H. R. Dawe, H. Farr, N. Portman, M. K. Shaw, and K. Gull, “The Parkin co-regulated gene product, PACRG, is an evolutionarily conserved axonemal protein that functions in outer-doublet microtubule morphogenesis,” Journal of Cell Science, vol. 118, no. 23, pp. 5421–5430, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Broadhead, H. R. Dawe, H. Farr et al., “Flagellar motility is required for the viability of the bloodstream trypanosome,” Nature, vol. 440, no. 7081, pp. 224–227, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Absalon, T. Blisnick, M. Bonhivers et al., “Flagellum elongation is required for correct structure, orientation and function of the flagellar pocket in Trypanosoma brucei,” Journal of Cell Science, vol. 121, no. 22, pp. 3704–3716, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Lacomble, S. Vaughan, C. Gadelha et al., “Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography,” Journal of Cell Science, vol. 122, no. 8, pp. 1081–1090, 2009. View at Publisher · View at Google Scholar · View at Scopus