Polo-like kinase phosphorylation of bilobe-resident TbCentrin2 facilitates flagellar inheritance in Trypanosoma brucei

Molecular Biology of the Cell

Volumn 24, Issue 12, 2013, Pages 1947-1963

  De Graffenried, Christopher L ^a   Anrather, Dorothea ^a   Rauendorf, Freia Von ^b   Warren, Graham ^a,b  

^a UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CENTRIN; MALTOSE BINDING PROTEIN; POLO LIKE KINASE; SERINE; TBCENTRIN2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CELL GROWTH; CONTROLLED STUDY; CYTOSKELETON; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; EUKARYOTIC FLAGELLUM; IMMUNOFLUORESCENCE; IN VITRO STUDY; INHERITANCE; KINETOPLAST; KINETOSOME; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RAT; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CYTOSKELETON; FLAGELLA; MASS SPECTROMETRY; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTOZOAN PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

PROTISTA; TRYPANOSOMA BRUCEI;

EID: 84879571932     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-12-0911     Document Type: Article

References (58)

1. Araki Y, Gombos L, Migueleti SPS, Sivashanmugam L, Antony C, Schiebel E (2010). N-terminal regions of Mps1 kinase determine functional bifurcation. J Cell Biol 189, 41-56.
2. Bangs JD (2011). Replication of the ERES:Golgi junction in bloodstream-form African trypanosomes. Mol Microbiol 82, 1433-1443.
3. Barr FA, Silljé HHW, Nigg EA (2004). Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 5, 429-440. (Pubitemid 38745493)
4. Bonhivers M, Nowacki S, Landrein N, Robinson DR (2008). Biogenesis of the trypanosome endo-exocytotic organelle is cytoskeleton mediated. PLoS Biol 6, e105.
5. de Graffenried CL, Ho HH, Warren G (2008). Polo-like kinase is required for Golgi and bilobe biogenesis in Trypanosoma brucei. J Cell Biol 181, 431-438. (Pubitemid 351645033)
6. Dou Z, von Schubert C, Körner R, Santamaria A, Elowe S, Nigg EA (2011). Quantitative mass spectrometry analysis reveals similar substrate consensus motif for human Mps1 kinase and Plk1. PLoS One 6, e18793.
7. Elia AEH, Cantley LC, Yaffe MB (2003). Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 299, 1228-1231. (Pubitemid 36237463)
8. Esson HJ, Morriswood B, Yavuz S, Vidilaseris K, Dong G, Warren G (2012). Morphology of the trypanosome bilobe, a novel cytoskeletal structure. Eukaryotic Cell 11, 761-772.
9. Estévez AM, Kierszenbaum F, Wirtz E, Bringaud F, Grunstein J, Simpson L (1999). Knockout of the glutamate dehydrogenase gene in bloodstream Trypanosoma brucei in culture has no effect on editing of mitochondrial mRNAs. Mol Biochem Parasitol 100, 5-17. (Pubitemid 29206668)
10. Field MC, Carrington M (2009). The trypanosome flagellar pocket. Nat Rev Microbiol 7, 775-786.
11. Friedberg F (2006). Centrin isoforms in mammals. Relation to calmodulin. Mol Biol Rep 33, 243-252. (Pubitemid 44760393)
12. Gadelha C, Rothery S, Morphew M, McIntosh JR, Severs NJ, Gull K (2009). Membrane domains and flagellar pocket boundaries are influenced by the cytoskeleton in African trypanosomes. Proc Natl Acad Sci USA 106, 17425-17430.
13. Gheiratmand L, Brasseur A, Zhou Q, He CY (2013). Biochemical characterization of the bi-lobe reveals a continuous structural network linking the bi-lobe to other single-copied organelles in Trypanosoma brucei. J Biol Chem 288, 3489-3499.
14. Gull K (1999). The cytoskeleton of trypanosomatid parasites. Annu Rev Microbiol 53, 629-655. (Pubitemid 29503743)
15. Hammarton TC, Kramer S, Tetley L, Boshart M, Mottram JC (2007). Trypanosoma brucei Polo-like kinase is essential for basal body duplication, kDNA segregation and cytokinesis. Mol Microbiol 65, 1229-1248. (Pubitemid 47262827)
16. He CY, Pypaert M, Warren G (2005). Golgi duplication in Trypanosoma brucei requires Centrin2. Science 310, 1196-1198. (Pubitemid 41681748)
17. Hill KL (2010). Parasites in motion: Flagellum-driven cell motility in African trypanosomes. Curr Opin Microbiol 13, 459-465.
18. Ikeda KN, de Graffenried CL (2012). Polo-like kinase is necessary for flagellum inheritance in Trypanosoma brucei. J Cell Sci 125, 3173-3184.
19. Klotz C, Garreau de Loubresse N, Ruiz F, Beisson J (1997). Genetic evidence for a role of centrin-associated proteins in the organization and dynamics of the infraciliary lattice in Paramecium. Cell Motil Cytoskeleton 38, 172-186. (Pubitemid 27430423)
20. Kohl L, Robinson D, Bastin P (2003). Novel roles for the flagellum in cell morphogenesis and cytokinesis of trypanosomes. EMBO J 22, 5336-5346. (Pubitemid 37279944)
21. Kohl L, Sherwin T, 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. (Pubitemid 29263302)
22. Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, 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.
23. Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, Gull K (2010). Basal body movements orchestrate membrane organelle division and cell morphogenesis in Trypanosoma brucei. J Cell Sci 123, 2884-2891.
24. LaCount DJ, Barrett B, Donelson JE (2002). Trypanosoma brucei FLA1 is required for flagellum attachment and cytokinesis. J Biol Chem 277, 17580-17588. (Pubitemid 34967560)
25. Li S, Sandercock AM, Conduit P, Robinson CV, Williams RL, Kilmartin JV (2006). Structural role of Sfi1p-centrin filaments in budding yeast spindle pole body duplication. J Cell Biol 173, 867-877.
26. Li Z, Umeyama T, Li Z, Wang CC (2010). Polo-like kinase guides cytokinesis in Trypanosoma brucei through an indirect means. Eukaryot Cell 9, 705-716.
27. Lutz W, Lingle WL, McCormick D, Greenwood TM, Salisbury JL (2001). Phosphorylation of centrin during the cell cycle and its role in centriole separation preceding centrosome duplication. J Biol Chem 276, 20774-20780.
28. Martindale VE, Salisbury JL (1990). Phosphorylation of algal centrin is rapidly responsive to changes in the external milieu. J Cell Sci 96, 395-402.
29. Mazanek M, Mituloviae G, Herzog F, Stingl C, Hutchins JRA, Peters J-M, Mechtler K (2007). Titanium dioxide as a chemo-affinity solid phase in offline phosphopeptide chromatography prior to HPLC-MS/MS analysis. Nat Protoc 2, 1059-1069. (Pubitemid 46901287)
30. Mok J et al. (2010). Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci Signal 3, ra12.
31. Morriswood B et al. (2013). Novel bilobe components in Trypanosoma brucei identified using proximity-dependent biotinylation. Eukaryot Cell 12, 356-367.
32. Morriswood B, He CY, Sealey-Cardona M, Yelinek J, Pypaert M, Warren G (2009). The bilobe structure of Trypanosoma brucei contains a MORN-repeat protein. Mol Biochem Parasitol 167, 95-103.
33. Nett IRE, Davidson L, Lamont D, Ferguson MAJ (2009a). Identification and specific localization of tyrosine-phosphorylated proteins in Trypanosoma brucei. Eukaryot Cell 8, 617-626.
34. Nett IRE, Martin DMA, Miranda-Saavedra D, Lamont D, Barber JD, Mehlert A, Ferguson MAJ (2009b). The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol Cell Proteomics 8, 1527-1538.
35. Portman N, Gull K (2012). Proteomics and the Trypanosoma brucei cytoskeleton: Advances and opportunities. Parasitology 139, 1168-1177.
36. Robinson DR, Gull K (1991). Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature 352, 731-733. (Pubitemid 21912419)
37. Robinson DR, Sherwin T, Ploubidou A, Byard EH, 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.
38. Salisbury JL (1995). Centrin, centrosomes, and mitotic spindle poles. Curr Opin Cell Biol 7, 39-45.
39. Salisbury JL, Baron A, Surek B, Melkonian M (1984). Striated flagellar roots: Isolation and partial characterization of a calcium-modulated contractile organelle. J Cell Biol 99, 962-970. (Pubitemid 14043354)
40. Sanders MA, Salisbury JL (1994). Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J Cell Biol 124, 795-805. (Pubitemid 24085787)
41. Selvapandiyan A, Duncan R, Debrabant A, Bertholet S, Sreenivas G, Negi NS, Salotra P, Nakhasi HL (2001). Expression of a mutant form of Leishmania donovani centrin reduces the growth of the parasite. J Biol Chem 276, 43253-43261.
42. Selvapandiyan A, Kumar P, Morris JC, Salisbury JL, Wang CC, Nakhasi HL (2007). Centrin1 is required for organelle segregation and cytokinesis in Trypanosoma brucei. Mol Biol Cell 18, 3290-3301. (Pubitemid 47378671)
43. Sheehan JH, Bunick CG, Hu H, Fagan PA, Meyn SM, Chazin WJ (2006). Structure of the N-terminal calcium sensor domain of centrin reveals the biochemical basis for domain-specific function. J Biol Chem 281, 2876-2881. (Pubitemid 43845753)
44. Sherwin T, Gull K (1989). 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.
45. Shi J, Franklin JB, Yelinek JT, Ebersberger I, Warren G, He CY (2008). Centrin4 coordinates cell and nuclear division in T. brucei. J Cell Sci 121, 3062-3070.
46. Szöör B (2010). Trypanosomatid protein phosphatases. Mol Biochem Parasitol 173, 53-63.
47. Szöör B, Wilson J, McElhinney H, Tabernero L, Matthews KR (2006). Protein tyrosine phosphatase TbPTP1: A molecular switch controlling life cycle differentiation in trypanosomes. J Cell Biol 175, 293-303. (Pubitemid 44631423)
48. Thingholm TE, Jørgensen TJD, Jensen ON, Larsen MR (2006). Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nat Protoc 1, 1929-1935. (Pubitemid 46773313)
49. Thompson JR, Ryan ZC, Salisbury JL, Kumar R (2006). The structure of the human centrin 2-xeroderma pigmentosum group C protein complex. J Biol Chem 281, 18746-18752. (Pubitemid 44035535)
50. Trojan P, Rausch S, Giessl A, Klemm C, Krause E, Pulvermüller A, Wolfrum U (2008). Light-dependent CK2-mediated phosphorylation of centrins regulates complex formation with visual G-protein. Biochim Biophys Acta 1783, 1248-1260.
51. Vaughan S (2010). Assembly of the flagellum and its role in cell morphogenesis in Trypanosoma brucei. Curr Opin Microbiol 13, 453-458.
52. Vaughan S, Kohl L, Ngai I, Wheeler RJ, Gull K (2008). A repetitive protein essential for the flagellum attachment zone filament structure and function in Trypanosoma brucei. Protist 159, 127-136. (Pubitemid 350213528)
53. Vickerman K (1969). On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci 5, 163-193.
54. Wang M, Gheiratmand L, He CY (2012). An interplay between Centrin2 and Centrin4 on the bi-lobed structure in Trypanosoma brucei. Mol Microbiol 83, 1153-1161.
55. Wirtz E, Leal S, Ochatt C, Cross GA (1999). A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99, 89-101. (Pubitemid 29127189)
56. Yang A, Miron S, Duchambon P, Assairi L, Blouquit Y, Craescu CT (2006). The N-terminal domain of human centrin 2 has a closed structure, binds calcium with a very low affinity, and plays a role in the protein self-assembly. Biochemistry 45, 880-889. (Pubitemid 43122252)
57. Yang C-H, Kasbek C, Majumder S, Yusof AM, Fisk HA (2010). Mps1 phosphorylation sites regulate the function of centrin 2 in centriole assembly. Mol Biol Cell 21, 4361-4372.
58. Yu Z, Liu Y, Li Z (2012). Structure-function relationship of the Polo-like kinase in Trypanosoma brucei. J Cell Sci 125, 1519-1530.