Calmodulin is Required for Paraflagellar Rod Assembly and Flagellum-Cell Body Attachment in Trypanosomes

Protist

Volumn 164, Issue 4, 2013, Pages 528-540

  Ginger, Michael L ^a   Collingridge, Peter W ^b   Brown, Robert W B ^a   Sproat, Rhona ^b   Shaw, Michael K ^b   Gull, Keith ^b  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cell morphogenesis; Flagellum assembly; Flagellum function; Paraflagellar rod Trypanosoma brucei; Trypanosomatid.

Indexed keywords

CHLAMYDOMONAS; CHLOROPHYTA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 84879511644     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2013.05.002     Document Type: Article

References (57)

1. Aslett M., Aurrecoechea C., Berriman M., Brestelli J., Brunk B.P., Carrington M., Depledge D.P., Fischer S., Gajria B., Gao X., Gardner M.J., Gingle A., Grant G., Harb O.S., Heiges M., Hertz-Fowler C., Houston R., Innamorato F., Iodice J., Kissinger J.C., Kraemer E., Li W., Logan F.J., Miller J.A., Mitra S., Myler P.J., Nayak V., Pennington C., Phan I., Pinney D.F., Ramasamy G., Rogers M.B., Roos D.S., Ross C., Sivam D., Smith D.F., Srinivasamoorthy G., Stoeckert C.J., Subramanian S., Thibodeau R., Tivey A., Treatman C., Velarde G., Wang H. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 2010, 38:D457-D462.
2. Bastin P., Matthews K.R., Gull K. The paraflagellar rod of Kinetoplastida: solved and unsolved questions. Parasitol Today 1996, 12:302-307.
3. Bastin P., Sherwin T., Gull K. Paraflagellar rod is vital for trypanosome motility. Nature 1998, 391:548.
4. Bastin P., Ellis K., Kohl L., Gull K. Flagellum ontogeny in trypanosomes studied via an inherited and regulated RNA interference system. J Cell Sci 2000, 113:3321-3328.
5. Bastin P., Pullen T.J., Sherwin T., Gull K. Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J Cell Sci 1999, 112:3769-3777.
6. Branche C., Kohl L., Toutirais G., Buisson J., Cosson J., Bastin P. Conserved and specific functions of axoneme components in trypanosome motility. J Cell Sci 2006, 119:3443-3455.
7. 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, 440:224-227.
8. Brun R., Schönenberger M. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 1979, 36:289-292.
9. Casey D.M., Inaba K., Pazour G.J., Takada S., Wakabayashi K., Wilkerson C.G., Kamiya R., Witman GB DC3, the 21-kDa subunit of the outer dynein arm-docking complex (ODA-DC), is a novel EF-hand protein important for assembly of both the outer arm and the ODA-DC. Mol Biol Cell 2003, 14:3650-3663.
10. Chin D., Means A.R. Calmodulin: a prototypical calcium sensor. Trends Cell Biol 2000, 10:322-328.
11. Davidge J.A., Chambers E., Dickinson H.A., Towers K., Ginger M.L., McKean P.G., Gull K. Trypanosome IFT mutants provide insight into the motor location for mobility of the flagella connector and flagellar membrane formation. J Cell Sci 2006, 119:3935-3943.
12. Demonchy R., Blisnick T., Deprez C., Toutirais G., Loussert C., Marande W., Grellier P., Bastin P., Kohl L. Kinesin 9 family members perform separate functions in the trypanosome flagellum. J Cell Biol 2009, 187:615-622.
13. DiPetrillo C.G., Smith E.F. Pcdp1 is a central apparatus protein that binds Ca2+-calmodulin and regulates ciliary motility. J Cell Biol 2010, 189:601-612.
14. Dymek E.E., Smith E.F. A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity. J Cell Biol 2007, 179:515-526.
15. Eid J.E., Sollner-Webb B. Homologous recombination in the tandem calmodulin genes of Trypanosoma brucei yields multiple products: compensation for deleterious deletions by gene amplification. Genes Dev 1991, 5:2024-2032.
16. Gadelha C., Wickstead B., de Souza W., Gull K., Cunha-e-Silva N. Cryptic paraflagellar rod in endosymbiont-containing kinetoplastid protozoa. Eukaryot Cell 2005, 4:516-525.
17. Gadelha C., Wickstead B., Gull K. Flagellar and ciliary beating in trypanosome motility. Cytoskeleton 2007, 64:629-643.
18. Ginger M.L., Portman N., McKean P.G. Swimming with protists: perception, motility and flagellum assembly. Nature Rev Microbiol 2008, 6:838-850.
19. Griffiths S., Portman N., Taylor P.R., Gordon S., Ginger M.L., Gull K. RNAi mutant induction in vivo demonstrates the essential nature of trypanosome flagellar function during mammalian infection. Eukaryot Cell 2007, 6:148-1250.
20. Holwill M.E., McGregor J.L. Effects of calcium on flagellar movement in the trypanosome Crithidia oncopelti. J Exp Biol 1976, 65:229-242.
21. Höög J.L., Bouchet-Marquis C., McIntosh J.R., Hoenger A., Gull K. Cryo-electron tomography and 3-D analysis of the intact flagellum in Trypanosoma brucei. J Struct Biol 2012, 178:189-198.
22. Hughes L.C., Ralston K.S., Hill K.L., Zhou Z.H. Three-dimensional structure of the trypanosome flagellum suggests that the paraflagellar rod functions as a biomechanical spring. Plos One 2012, 7:e25700.
23. Hunger-Glaser I., Seebeck T. Deletion of the genes for the paraflagellar rod protein PFR-A in Trypanosoma brucei is probably lethal. Mol Biochem Parasitol 1997, 90:347-351.
24. Kohl L., Sherwin T., Gull K. Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J Eukaryot Microbiol 1999, 46:105-109.
25. Koyfman A.Y., Schmid M.F., Gheiratmand L., Fu C.J., Khant H.A., Huang D., He C.Y., Chiu W. Structure of Trypanosoma brucei flagellum accounts for its bihelical motion. Proc Natl Acad Sci USA 2011, 108:11105-11108.
26. Lacomble S., Portman N., Gull K. A protein-protein interaction map of the Trypanosoma brucei paraflagellar rod. PLoS One 2009, 4:e7685.
27. LaCount D.J., Barrett B., Donelson J.E. Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. J Biol Chem 2002, 277:17580-17588.
28. Lye L.-F., Owens K., Shi H., Murta S.M.F., Vieira A.C., Turco S.J., Tschudi C., Ullu E., Beverley S.M. Retention and Loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathogens 2010, 6:e1001161.
29. Maga J.A., Sherwin T., Francis S., Gull K., LeBowitz J.H. Genetic dissection of the Leishmania paraflagellar rod, a unique flagellar cytoskeleton structure. J Cell Sci 1999, 112:2753-2763.
30. McCulloch R., Vassella E., Burton P., Boshart M., Barry J.D. Transformation of monomorphic and pleomorphic Trypanosoma brucei. Methods Mol Biol 2004, 262:53-86.
31. Moreira-Leite FF (2002) PhD thesis, University of Manchester, UK.
32. Moreira-Leite F.F., Sherwin T., Kohl L., Gull K. A trypanosome structure involved in transmitting cytoplasmic information during cell division. Science 2001, 294:610-612.
33. Nozaki T., Haynes P.A., Cross G.A. Characterization of the Trypanosoma brucei homologue of a Trypanosoma cruzi flagellum-adhesion glycoprotein. Mol Biochem Parasitol 1996, 82:245-255.
34. Oberholzer M., Marti G., Baresic M., Kunz S., Hemphill A., Seebeck T. The Trypanosoma brucei cAMP phosphodiesterases TbPDEB1 and TbPDEB2: flagellar enzymes that are essential for parasite virulence. FASEB J 2007, 21:720-731.
35. Ploubidou A., Robinson D.R., Docherty R.C., Ogbadoyi E.O., Gull K. Evidence for novel cell cycle checkpoints in trypanosomes: kinetoplast segregation and cytokinesis in the absence of mitosis. J Cell Sci 1999, 112:4641-4650.
36. Poon S.K., Peacock L., Gibson W., Gull K., Kelly S. A modular and optimised single marker system for generating Trypanosoma brucei cell lines expressing T7 RNA polymerase and the tetracycline repressor. Open Biol 2012, 2:120033.
37. Portman N., Gull K. The paraflagellar rod of kinetoplastid parasites: from structure to components and function. Int J Parasitol 2010, 40:135-148.
38. Portman N., Lacomble S., Thomas B., McKean P.G., Gull K. Combining RNA interference mutants and comparative proteomics to identify protein components and dependences in a eukaryotic flagellum. J Biol Chem 2009, 284:5610-5619.
39. Pullen T.J., Ginger M.L., Gaskell S.J., Gull K. Protein targeting of an unusual, evolutionarily conserved adenylate kinase to a eukaryotic flagellum. Mol Biol Cell 2004, 15:3257-3265.
40. Ralston K.S., Lerner A.G., Diener D.R., Hill K.L. Flagellar motility contributes to cytokinesis in Trypanosoma brucei and is modulated by an evolutionarily conserved dynein regulatory system. Eukaryot Cell 2006, 5:696-711.
41. Ridgley E., Webster P., Patton C., Ruben L. Calmodulin-binding properties of the paraflagellar rod complex from Trypanosoma brucei. Mol Biochem Parasitol 2000, 109:195-201.
42. 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. J Cell Biol 1995, 128:1163-1172.
43. Rusconi F., Durand-Dubief M., Bastin P. Functional complementation of RNA interference mutants in trypanosomes. BMC Biotechnol 2005, 5:6.
44. Santrich C., Moore L., Sherwin T., Bastin P., Brokaw C., Gull K., LeBowitz J.H. A motility function for the paraflagellar rod of Leishmania parasites revealed by PFR-2 gene knockouts. Mol Biochem Parasitol 1997, 90:95-109.
45. Sherwin T., Gull K. The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philos Trans R Soc Lond B Biol Sci 1989, 323:573-588.
46. Smith E.F. Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol Biol Cell 2002, 13:3303-3313.
47. Sun Y., Wang C., Yuan Y.A., He C.Y. An intra-cellular membrane junction mediated by flagellum adhesion glycoproteins links flagellum biogenesis to cell morphogenesis in Trypanosoma brucei. J Cell Sci 2013, 126:520-531.
48. Turnock D.C., Izquierdo L., Ferguson M.A. The de novo synthesis of GDP-fucose is essential for flagellar adhesion and cell growth in Trypanosoma brucei. J Biol Chem 2007, 282:28853-28863.
49. Vaughan S. Assembly of the flagellum and its role in cell morphogenesis in Trypanosoma brucei. Curr Opin Microbiol 2010, 13:453-458.
50. Vaughan S., Kohl L., Ngai I., Wheeler R.J., Gull K. A repetitive protein essential for the flagellum attachment zone filament structure and function in Trypanosoma brucei. Protist 2008, 159:127-136.
51. Vickerman K. On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci 1969, 5:163-193.
52. Wang Z., Morris J.C., Drew M.E., Englund P.T. Inhibition of Trypanosoma brucei gene expression by RNAi interference using an integratable vector with opposing T7 promoters. J Biol Chem 2000, 275:40174-40179.
53. Wickstead B., Ersfeld K., Gull K. Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol 2002, 125:211-216.
54. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 1999, 99:89-101.
55. Yang P., Yang C., Sale W.S. Flagellar radial spoke protein 2 is a calmodulin binding protein required for motility in Chlamydomonas reinhardtii. Eukaryot Cell 2004, 3:72-81.
56. Yang P., Diener D.R., Rosenbaum J.L., Sale W.S. Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J Cell Biol 2001, 153:1315-1326.
57. 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. J Cell Sci 2011, 124:3848-3858.