A Trypanosoma brucei Protein Required for Maintenance of the Flagellum Attachment Zone and Flagellar Pocket ER Domains

Protist

Volumn 163, Issue 4, 2012, Pages 602-615

  Lacomble, Sylvain ^a   Vaughan, Sue ^b   Deghelt, Michaël ^a,c   Moreira Leite, Flávia Fernandes ^a   Gull, Keith ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF NAMUR   (Belgium)

Author keywords

Cellular electron tomography; Endoplasmic reticulum; Flagellar proteome; Flagellum attachment zone; Trypanosoma brucei; VAMP associated protein.

Indexed keywords

CYTOSKELETON PROTEIN; MEMBRANE PROTEIN; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; ELECTRON TOMOGRAPHY; ENDOPLASMIC RETICULUM; FLAGELLUM; GENE SILENCING; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RNA INTERFERENCE; THREE DIMENSIONAL IMAGING; TRYPANOSOMA BRUCEI; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; CYTOSKELETAL PROTEINS; ELECTRON MICROSCOPE TOMOGRAPHY; ENDOPLASMIC RETICULUM; FLAGELLA; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMAGING, THREE-DIMENSIONAL; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 84861331710     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2011.10.010     Document Type: Article

References (52)

1. 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. J Cell Sci 2008, 121:3704-3716.
2. Alsford S., Turner D.J., Obado S.O., Sanchez-Flores A., Glover L., Berriman M., Hertz-Fowler C., Horn D. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 2011, 21:915-924.
3. Amarilio R., Ramachandran S., Sabanay H., Lev S. Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J Biol Chem 2005, 280:5934-5944.
4. Bastin P., Bagherzadeh Z., Matthews K.R., Gull K. A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol Biochem Parasitol 1996, 77:235-239.
5. Brickner J.H., Walter P. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol 2004, 2:e342.
6. 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.
7. 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.
8. Field M.C., Sergeenko T., Wang Y.N., Bohm S., Carrington M. Chaperone requirements for biosynthesis of the trypanosome variant surface glycoprotein. PLoS One 2010, 5:e8468.
9. Griffiths S., Portman N., Taylor P.R., Gordon S., Ginger M.L., Gull K. RNA interference mutant induction in vivo demonstrates the essential nature of trypanosome flagellar function during mammalian infection. Eukaryot Cell 2007, 6:1248-1250.
10. Izquierdo L., Schulz B.L., Rodrigues J.A., Guther M.L., Procter J.B., Barton G.J., Aebi M., Ferguson M.A. Distinct donor and acceptor specificities of Trypanosoma brucei oligosaccharyltransferases. EMBO J 2009, 28:2650-2661.
11. Kagiwada S., Zen R. Role of the yeast VAP homolog, Scs2p, in INO1 expression and phospholipid metabolism. J Biochem 2003, 133:515-522.
12. Kagiwada S., Hosaka K., Murata M., Nikawa J., Takatsuki A. The Saccharomyces cerevisiae SCS2 gene product, a homolog of a synaptobrevin-associated protein, is an integral membrane protein of the endoplasmic reticulum and is required for inositol metabolism. J Bacteriol 1998, 180:1700-1708.
13. Kall L., Krogh A., Sonnhammer E.L. A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004, 338:1027-1036.
14. Kanekura K., Nishimoto I., Aiso S., Matsuoka M. Characterization of amyotrophic lateral sclerosis-linked P56S mutation of vesicle-associated membrane protein-associated protein B (VAPB/ALS8). J Biol Chem 2006, 281:30223-30233.
15. Katoh K., Asimenos G., Toh H. Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 2009, 537:39-64.
16. Kawano M., Kumagai K., Nishijima M., Hanada K. Efficient trafficking of ceramide from the endoplasmic reticulum to the Golgi apparatus requires a VAMP-associated protein-interacting FFAT motif of CERT. J Biol Chem 2006, 281:30279-30288.
17. Kelly S., Reed J., Kramer S., Ellis L., Webb H., Sunter J., Salje J., Marinsek N., Gull K., Wickstead B., Carrington M. Functional genomics in Trypanosoma brucei: a collection of vectors for the expression of tagged proteins from endogenous and ectopic gene loci. Mol Biochem Parasitol 2007, 154:103-109.
18. Kohl L., Robinson D., Bastin P. Novel roles for the flagellum in cell morphogenesis and cytokinesis of trypanosomes. EMBO J 2003, 22:5336-5346.
19. 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.
20. Koumandou V.L., Natesan S.K., Sergeenko T., Field M.C. The trypanosome transcriptome is remodelled during differentiation but displays limited responsiveness within life stages. BMC Genomics 2008, 9:298.
21. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 1996, 116:71-76.
22. Lacomble S., Gadelha C., Vaughan S., 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. J Cell Sci 2009, 122:1081-1090.
23. Lacomble S., Portman N., Gull K. A protein-protein interaction map of the Trypanosoma brucei paraflagellar rod. PLoS One 2009, 4:e7685.
24. Lacomble S., Vaughan S., Gadelha C., Morphew M.K., Shaw M.K., McIntosh J.R., Gull K. Basal body movements orchestrate membrane organelle division and cell morphogenesis in Trypanosoma brucei. J Cell Sci 2010, 123:2884-2891.
25. 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.
26. Lev S., Ben Halevy D., Peretti D., Dahan N. The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol 2008, 18:282-290.
27. Loewen C.J., Young B.P., Tavassoli S., Levine T.P. Inheritance of cortical ER in yeast is required for normal septin organization. J Cell Biol 2007, 179:467-483.
28. Nikawa J., Murakami A., Esumi E., Hosaka K. Cloning and sequence of the SCS2 gene, which can suppress the defect of INO1 expression in an inositol auxotrophic mutant of Saccharomyces cerevisiae. J Biochem 1995, 118:39-45.
29. Nishimura A.L., Al-Chalabi A., Zatz M. A common founder for amyotrophic lateral sclerosis type 8 (ALS8) in the Brazilian population. Hum Genet 2005, 118:499-500.
30. Nishimura A.L., Mitne-Neto M., Silva H.C., Richieri-Costa A., Middleton S., Cascio D., Kok F., Oliveira J.R., Gillingwater T., Webb J., Skehel P., Zatz M. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am J Hum Genet 2004, 75:822-831.
31. Nishimura Y., Hayashi M., Inada H., Tanaka T. Molecular cloning and characterization of mammalian homologues of vesicle-associated membrane protein-associated (VAMP-associated) proteins. Biochem Biophys Res Commun 1999, 254:21-26.
32. 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.
33. Ogbadoyi E.O., Robinson D.R., Gull K. A high-order trans-membrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol Biol Cell 2003, 14:1769-1779.
34. Pennetta G., Hiesinger P.R., Fabian-Fine R., Meinertzhagen I.A., Bellen H.J. Drosophila VAP-33A directs bouton formation at neuromuscular junctions in a dosage-dependent manner. Neuron 2002, 35:291-306.
35. Portman N., Gull K. The paraflagellar rod of kinetoplastid parasites: from structure to components and function. Int J Parasitol 2010, 40:135-148.
36. Prosser D.C., Tran D., Gougeon P.Y., Verly C., Ngsee J.K. FFAT rescues VAPA-mediated inhibition of ER-to-Golgi transport and VAPB-mediated ER aggregation. J Cell Sci 2008, 121:3052-3061.
37. Ralston K.S., Kisalu N.K., Hill K.L. Structure-function analysis of dynein light chain 1 identifies viable motility mutants in bloodstream-form Trypanosoma brucei. Eukaryot Cell 2011, 10:884-894.
38. Roberts T.M., Stewart M. Nematode sperm locomotion. Curr Opin Cell Biol 1995, 7:13-17.
39. Robinson D.R., Gull K. Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature 1991, 352:731-733.
40. 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.
41. Rocha G.M., Brandao B.A., Mortara R.A., Attias M., de Souza W., Carvalho T.M. The flagellar attachment zone of Trypanosoma cruzi epimastigote forms. J Struct Biol 2006, 154:89-99.
42. Sevova E.S., Bangs J.D. Streamlined architecture and glycosylphosphatidylinositol-dependent trafficking in the early secretory pathway of African trypanosomes. Mol Biol Cell 2009, 20:4739-4750.
43. 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.
44. Signorell A., Rauch M., Jelk J., Ferguson M.A., Butikofer P. Phosphatidylethanolamine in Trypanosoma brucei is organized in two separate pools and is synthesized exclusively by the Kennedy pathway. J Biol Chem 2008, 283:23636-23644.
45. Skehel P.A., Fabian-Fine R., Kandel E.R. Mouse VAP33 is associated with the endoplasmic reticulum and microtubules. Proc Natl Acad Sci USA 2000, 97:1101-1106.
46. Skehel P.A., Martin K.C., Kandel E.R., Bartsch D. A VAMP-binding protein from Aplysia required for neurotransmitter release. Science 1995, 269:1580-1583.
47. Taylor A.E., Godfrey D.G. A new organelle of bloodstream salivarian trypanosomes. J Protozool 1969, 16:466-470.
48. Tetley L., Vickerman K. Differentiation in Trypanosoma brucei: host-parasite cell junctions and their persistence during acquisition of the variable antigen coat. J Cell Sci 1985, 74:1-19.
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. Woodward R., Gull K. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J Cell Sci 1990, 95:49-57.