Cytokinesis in trypanosoma brucei differs between bloodstream and tsetse trypomastigote forms: Implications for microtubule-based morphogenesis and mutant analysis

Molecular Microbiology

Volumn 90, Issue 6, 2013, Pages 1339-1355

  Wheeler, Richard J ^b   Scheumann, Nicole ^b   Wickstead, Bill ^c   Gull, Keith ^b   Vaughan, Sue ^a  

^a OXFORD BROOKES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; BINDING PROTEIN; UNCLASSIFIED DRUG; XMAP215 PROTEIN;

ARTICLE; CELL CYCLE; CONTROLLED STUDY; CYTOKINESIS; CYTOPLASM; CYTOSKELETON; FLAGELLUM; GLOSSINIDAE; LIFE CYCLE STAGE; MICROTUBULE; MORPHOGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SCANNING ELECTRON MICROSCOPY; TRYPANOSOMA BRUCEI; TRYPOMASTIGOTE; VIDEO MICROSCOPY;

EUKARYOTA; TRYPANOSOMA BRUCEI;

ANIMALS; CELL CYCLE; CYTOKINESIS; CYTOSKELETON; LIFE CYCLE STAGES; MICROSCOPY, ELECTRON, SCANNING; MICROTUBULES; MORPHOGENESIS; MUTATION; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI; TSETSE FLIES;

EID: 84890119143     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12436     Document Type: Article

References (64)

1. Absalon, S., Kohl, L., Branche, C., Blisnick, T., Toutirais, G., Rusconi, F., etal. (2007) Basal body positioning is controlled by flagellum formation in Trypanosoma brucei. PLoS ONE 2: e437.
2. Anderson, W.A., and Ellis, R.A. (1965) Ultrastructure of Trypanosoma lewisi: flagellum, microtubules, and the kinetoplast. J Eukaryot Microbiol 12: 483-499.
3. Asbury, C.L. (2008) XMAP215: a tip tracker that really moves. Cell 132: 19-20.
4. Baluska, F., Menzel, D., and Barlow, P.W. (2006) Cytokinesis in plant and animal cells: endosomes 'shut the door'. Dev Biol 294: 1-10.
5. Barr, F.A., and Gruneberg, U. (2007) Cytokinesis: placing and making the final cut. Cell 131: 847-860.
6. Branche, C., Kohl, L., Toutirais, G., Buisson, J., Cosson, J., and Bastin, P. (2006) Conserved and specific functions of axoneme components in trypanosome motility. J Cell Sci 119: 3443-3455.
7. 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. J Cell Sci 117: 1641-1651.
8. Broadhead, R., Dawe, H.R., Farr, H., Griffiths, S., Hart, S.R., Portman, N., etal. (2006) Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440: 224-227.
9. Bruce, D., Harvey, D., Hamerton, A.E., Davey, J.B., and Bruce, L. (1912) The morphology of Trypanosoma simiae, sp. nov. Proc R Soc Lond B 85: 477-481.
10. Brun, R., and Schönenberger, M. (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36: 289-292.
11. Daniels, J.-P., Gull, K., and Wickstead, B. (2012) The trypanosomatid-specific N terminus of RPA2 is required for RNA polymerase I assembly, localization, and function. Eukaryot Cell 11: 662-672.
12. 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. J Cell Sci 119: 3935-3943.
13. Engstler, M., Pfohl, T., Herminghaus, S., Boshart, M., Wiegertjes, G., Heddergott, N., and Overath, P. (2007) Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131: 505-515.
14. Farr, H., and Gull, K. (2009) Functional studies of an evolutionarily conserved, cytochrome b5 domain protein reveal a specific role in axonemal organisation and the general phenomenon of post-division axonemal growth in trypanosomes. Cell Motil Cytoskeleton 66: 24-35.
15. Farr, H., and Gull, K. (2012) Cytokinesis in trypanosomes. Cytoskeleton 69: 931-941.
16. Foth, B.J., Goedecke, M.C., and Soldati, D. (2006) New insights into myosin evolution and classification. Proc Natl Acad Sci USA 103: 3681-3686.
17. García-Salcedo, J.A., Pérez-Morga, D., Gijón, P., Dilbeck, V., Pays, E., and Nolan, D.P. (2004) A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J 23: 780-789.
18. Glotzer, M. (2009) The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 10: 9-20.
19. Greenbaum, M.P., Yan, W., Wu, M.-H., Lin, Y.-N., Agno, J.E., Sharma, M., etal. (2006) TEX14 is essential for intercellular bridges and fertility in male mice. Proc Natl Acad Sci USA 103: 4982-4987.
20. Gull, K. (1999) The cytoskeleton of trypanosomatid parasites. Annu Rev Microbiol 53: 629-655.
21. Hammarton, T.C., Clark, J., Douglas, F., Boshart, M., and Mottram, J.C. (2003) Stage-specific differences in cell cycle control in Trypanosoma brucei revealed by RNA interference of a mitotic cyclin. J Biol Chem 278: 22877-22886.
22. Hammarton, T.C., Monnerat, S., and Mottram, J.C. (2007) Cytokinesis in trypanosomatids. Curr Opin Microbiol 10: 520-527.
23. Hoare, C.A. (1972) The Trypanosomes of Mammals: A Zoological Monograph. Oxford and Edinburgh: Blackwell Scientific Publications.
24. Hoare, C.A., and Wallace, F.G. (1966) Developmental stages of trypanosomatid flagellates: a new terminology. Nature 212: 1385-1386.
25. Hughes, L., Towers, K., Starborg, T., Gull, K., and Vaughan, S. (2013) A cell body groove housing the new flagellum tip suggests an adaptation of cellular morphogenesis for parasitism in bloodstream form Trypanosoma brucei. J Cell Sci Epub ahead of print. doi: 10.1242/jcs.139139.
26. Kelly, S., Reed, J., Kramer, S., Ellis, L., Webb, H., Sunter, J., etal. (2007) Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Mol Biochem Parasitol 154: 103-109.
27. Kilmartin, J.V., Wright, B., and Milstein, C. (1982) Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J Cell Biol 93: 576-582.
28. Kohl, L., Sherwin, T., and Gull, K. (1999) Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J Eukaryot Microbiol 46: 105-109.
29. Kumar, P., and Wang, C.C. (2005) Depletion of anaphase-promoting complex or cyclosome (APC/C) subunit homolog APC1 or CDC27 of Trypanosoma brucei arrests the procyclic form in metaphase but the bloodstream form in anaphase. J Biol Chem 280: 31783-31791.
30. Lacomble, S., Vaughan, S., Gadelha, C., Morphew, M.K., Shaw, M.K., McIntosh, J.R., and Gull, K. (2009) Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J Cell Sci 122: 1081-1090.
31. Li, Z., Lee, J.H., Chu, F., Burlingame, A.L., Günzl, A., and Wang, C.C. (2008a) Identification of a novel chromosomal passenger complex and its unique localization during cytokinesis in Trypanosoma brucei. PLoS ONE 3: e2354.
32. Li, Z., Umeyama, T., and Wang, C.C. (2008b) The chromosomal passenger complex and a mitotic kinesin interact with the Tousled-like kinase in trypanosomes to regulate mitosis and cytokinesis. PLoS ONE 3: e3814.
33. Magie, C.R., Meyer, M.R., Gorsuch, M.S., and Parkhurst, S.M. (1999) Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126: 5353-5364.
34. 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.
35. Müller, S., Wright, A.J., and Smith, L.G. (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19: 180-188.
36. Oh, Y., and Bi, E. (2011) Septin structure and function in yeast and beyond. Trends Cell Biol 21: 141-148.
37. Ormerod, W., and Venkatesan, S. (1971) An amastigote phase of the sleeping sickness trypanosome. Trans R Soc Trop Med Hyg 65: 736-741.
38. Ormerod, W.E., and Killick-Kendrick, R. (1956) Developmental forms of Trypanosoma lewisi in the vasa recta of the kidney. Trans R Soc Trop Med Hyg 50: 4.
39. Ploubidou, A., Robinson, D.R., Docherty, R.C., Ogbadoyi, E.O., and Gull, K. (1999) Evidence for novel cell cycle checkpoints in trypanosomes: kinetoplast segregation and cytokinesis in the absence of mitosis. J Cell Sci 112 (Pt 24): 4641-4650.
40. Pollard, T.D., and Wu, J.-Q. (2010) Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 11: 149-155.
41. Ralston, K.S., Lerner, A.G., Diener, D.R., and Hill, K.L. (2006) Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell 5: 696-711.
42. Richards, T.A., and Cavalier-Smith, T. (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436: 1113-1118.
43. 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. J Cell Biol 128: 1163-1172.
44. Rothberg, K.G., Burdette, D.L., Pfannstiel, J., Jetton, N., Singh, R., and Ruben, L. (2006) The RACK1 homologue from Trypanosoma brucei is required for the onset and progression of cytokinesis. J Biol Chem 281: 9781-9790.
45. Sanger, J.M., Pochapin, M.B., and Sanger, J.W. (1985) Midbody sealing after cytokinesis in embryos of the sea urchin Arabacia punctulata. Cell Tissue Res 240: 287-292.
46. 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.
47. 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.
48. Sherwin, T., and Gull, K. (1989b) The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philos Trans R Soc Lond B Biol Sci 323: 573-588.
49. Sherwin, T., Schneider, A., Sasse, R., Seebeck, T., and Gull, K. (1987) Distinct localization and cell cycle dependence of COOH terminally tyrosinolated alpha-tubulin in the microtubules of Trypanosoma brucei brucei. J Cell Biol 104: 439-446.
50. Soltys, M.A., and Woo, P. (1969) Multiplication of Trypanosoma brucei and Trypanosoma congolense in vertebrate hosts. Trans R Soc Trop Med Hyg 63: 490-494.
51. Steigemann, P., and Gerlich, D.W. (2009) Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol 19: 606-616.
52. Stephan, A., Vaughan, S., Shaw, M.K., Gull, K., and McKean, P.G. (2007) An essential quality control mechanism at the eukaryotic basal body prior to intraflagellar transport. Traffic 8: 1323-1330.
53. Steverding, D. (2008) The history of African trypanosomiasis. Parasit Vectors 1: 3.
54. Taylor, A.E., and Godfrey, D.G. (1969) A new organelle of bloodstream salivarian trypanosomes. J Protozool 16: 466-470.
55. Tu, X., and Wang, C.C. (2004) The involvement of two cdc2-related kinases (CRKs) in Trypanosoma brucei cell cycle regulation and the distinctive stage-specific phenotypes caused by CRK3 depletion. J Biol Chem 279: 20519-20528.
56. Tyler, K.M., Matthews, K.R., and Gull, K. (2001) Anisomorphic cell division by African trypanosomes. Protist 152: 367-378.
57. Van Damme, D. (2009) Division plane determination during plant somatic cytokinesis. Curr Opin Plant Biol 12: 745-751.
58. 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.
59. Vickerman, K. (1962) The mechanism of cyclical development in trypanosomes of the Trypanosoma brucei sub-group: an hypothesis based on ultrastructural observations. Trans R Soc Trop Med Hyg 56: 487-495.
60. Vickerman, K. (1969) The fine structure of Trypanosoma congolense in its bloodstream phase. J Eukaryot Microbiol 16: 54-69.
61. Wenyon, C.M. (1926) Protozoology: A Manual for Medical Men, Veterinarians and Zoologists. London: Baillière, Tindall and Cox.
62. Wheeler, R.J., Gluenz, E., and Gull, K. (2011) The cell cycle of Leishmania: morphogenetic events and their implications for parasite biology. Mol Microbiol 79: 647-662.
63. Wolcott, G.B. (1952) Mitosis in Trypanosoma lewisi. J Morphol 90: 189-199.
64. 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.