The GPI-phospholipase C of Trypanosoma brucei is non essential but influences parasitemia in mice

Journal of Cell Biology

Volumn 139, Issue 1, 1997, Pages 103-114

  Webb, Helena ^a   Carnall, Nicola ^a   Vanhamme, Luc ^b   Rolin, Sylvie ^b   Van Den Abbeele, Jakke ^c   Welburn, Sue ^d   Pays, Etienne ^b   Carrington, Mark ^a,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e Department of Biochemistry ^*  (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; PHOSPHOLIPASE C; VARIANT SURFACE GLYCOPROTEIN;

ANIMAL CELL; ANTIGENIC VARIATION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROLYSIS; MEMBRANE BINDING; MOUSE; MUTATION; NONHUMAN; PARASITEMIA; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI; TRYPANOSOMIASIS;

ANIMALS; DISEASE MODELS, ANIMAL; GLYCOSYLPHOSPHATIDYLINOSITOLS; MICE; MICE, INBRED STRAINS; MUTAGENESIS, INSERTIONAL; PARASITEMIA; PHENOTYPE; PHOSPHOLIPASE C; SEQUENCE DELETION; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMIASIS, AFRICAN;

EID: 0030763149     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.139.1.103     Document Type: Article

References (58)

1. Agur, Z., D. Abiri, and L.H.T. Van der Ploeg. 1989. Ordered appearance of antigenic variants of African trypanosomes explained in a mathematical model based on stochastic switch process and immune-selection against putative switch intermediates. Proc. Natl. Acad. Sci. USA. 86:9625-9630.
2. Askonas, B.A. 1985. Macrophages as mediators of immunosuppression in murine African trypanosomiasis. Curr. Top. Microbiol. Immunol. 117:119-127.
3. Barry, J.D., and C.M.R. Turner. 1991. The dynamics of antigenic variation and growth of African trypanosomes. Parasitol. Today. 7:207-211.
4. Berberof, M., L. Vanhamme, P. Tebabi, A. Pays, D. Jefferies, S. Welburn, and E. Pays. 1995. The 3′-terminal region of the mRNAs for VSG and procyclin expression in Trypanosoma brucei. EMBO (Eur. Mol. Biol. Organ.) J. 14: 2925-2934.
5. Blum, M.L., J.A. Down, A.M. Gurnett, M. Carrington, M.J. Turner, and D. Wiley. 1993. A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature (Lond.). 362:603-609.
6. Brun, R., and M. Schönenberger. 1979. Cultivation and in vitro cloning of procyclic culture forms of T. brucei in a semi-defined medium. Acta Trop. 36: 289-292.
7. Bülow, R., and P. Overath. 1985. Synthesis of a hydrolase for the membrane form variant surface glycoprotein is repressed during transformation of Trypanosoma brucei. FEBS (Fed. Eur. Biochem. Soc.) Lett. 187:105-110.
8. Bülow, R., and P. Overath. 1986. Purification and characterization of the membrane-form variant surface glycoprotein hydrolase of Trypanosoma brucei. J. Biol. Chem. 261:11918-11923.
9. Bülow, R., G. Griffiths, P. Webster, Y.-D. Stierhof, F. Opperdoes, and P. Overath. 1989a. Intracellular location of the glycosylphosphatidylinositol-specific phospholipase C of Trypanosoma brucei. J. Cell Sci. 93:233-240.
10. Bülow, R., C. Nonnengasser, and P. Overath. 1989b. The release of the variable surface glycoprotein on the transformation of Trypanosoma brucei from bloodstream to procyclic form. Mol. Biochem. Parasitol. 32:85-92.
11. Bütikofer, P., M. Boschung, U. Brodbeck, and A.K. Menon. 1996. Phosphatidylinositol hydrolysis by Trypanosoma brucei glycosylphosphatidylinositol phospholipase C. J. Biol. Chem. 271:15533-15541.
12. Cardoso de Almeida, M.L., and M.J. Turner. 1983. The membrane form of variant surface glycoproteins of Trypanosoma brucei. Nature (Lond.). 302:349-353.
13. Carrington, M., I. Roditi, and R.O. Williams. 1987. The structure and transcription of an element interspersed between tandem arrays of mini-exon donor RNA genes in Trypanosoma brucei. Nucleic. Acids Res. 15:10179-10198.
14. Carrington, M., R. Bülow, H. Reinke, and P. Overath. 1989. Sequence and expression of the glycosylphosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Mol. Biochem. Parasitol. 33:289-296.
15. Carrington, M., D. Walters, and H. Webb. 1991. The biology of the glycosylphosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Cell Biol. Int. Rep. 15:1101-1114.
16. Carroll, M., and P. McCrorie. 1986. Lipid composition of bloodstream forms of Trypanosoma brucei brucei. Comp. Biochem. Physiol. 83B:647-651.
17. Clayton, C.E., J.P. Fueri, J.E. Itzhaki, V. Bellofatto, D.R. Sherman, S. Wisdom, S. Vijasarathy, and M.R. Mowatt. 1990. Transcription of the procyclic acidic repetitive protein genes of Trypanosoma brucei. Mol. Cell. Biol. 10:3036-3047.
18. Cruz, A., and S.M. Beverley. 1990. Gene replacement in parasitic protozoa. Nature (Lond.). 348:171-173.
19. Eid, J., and B. Sollner-Webb. 1991. Homologous recombination in the tandem calmodulin genes of Trypanosoma brucei yields multiple products: compensation for deleterious deletions by gene amplification. Genes Dev. 5:2024-2032.
20. Engstier, M., G. Reuter, and R. Schauer. 1992. Purification and characterisation of a novel sialidase found in procyclic culture forms of Trypanosoma brucei. Mol. Biochem. Parasitol. 54:21-30.
21. Esser, K.M., and M.J. Schoenbechler. 1985. Expression of two variant surface glycoprotein genes on two individual African trypanosomes during antigen switching. Science (Wash. DC). 229:190-192.
22. Ferguson, M.A.J., M.G. Low, and G.A.M. Cross. 1985. Glycosyl-sn-1,2-dimyristylphosphatidylinositol is covalently linked to Trypanosoma brucei variant surface glycoprotein. J. Biol. Chem. 260:14547-14555.
23. Ferguson, M.A.J., M. Duszenko, G.S. Lamont, P. Overath, and G.A.M. Cross. 1986. Biosynthesis of Trypanosoma brucei variant glycoprotein. J. Biol. Chem. 261:356-362.
24. Ferguson, M.A.J., S.W. Homans, R.A. Dwek, and T.W. Rademacher. 1988. Glycosylphosphatidylinositol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science (Wash. DC). 239:753-759.
25. Field, M.C., A.K. Menon, and G.A.M. Cross. 1991. A glycosylphosphatidylinositol protein anchor from procyclic stage Trypanosoma brucei: lipid structure and biosynthesis. EMBO (Eur. Mol. Biol. Organ.) J. 10:2731-2739.
26. Fox, J.A., M. Druszenko, M.A.J. Ferguson, M.G. Low, and G.A.M. Cross. 1986. Purification and characterization of a novel glycanphosphatidylinositol specific phospholipase C from Trypanosoma brucei. J. Biol. Chem. 261:15767-15771.
27. Güther, M.L.S., and M.A.J. Ferguson. 1995. The role of inositol acylation and inosotol deacylation in GPI biosynthesis in Trypanosoma brucei. EMBO (Eur. Mol. Biol. Organ.) J. 14:3080-3093.
28. Güther, M.L.S., W.J. Masterson, and M.A.J. Ferguson. 1994. The role of glycolipid C in the glycosylphosphatidylinositol biosynthetic pathway in Trypanosoma brucei bloodstream forms. Braz. J. Med. Biol. Res. 27:121-126.
29. Hereld, D., J.L. Krakow, J.D. Bangs, G.W. Hart, and P.T. Englund. 1986. A phospholipase C from Trypanosoma brucei which selectively cleaves the glycolipid on the variant surface glycoprotein. J. Biol. Chem. 261:13813-13818.
30. Holder, A.A., and G.A.M. Cross. 1981. Glycopeptides from variant surface glycoproteins of Trypanosoma brucei. C-terminal location of antigenically cross-reacting carbohydrate moitities. Mol. Biochem. Parasitol. 2:135-150.
31. Jackson, D.G., M.J. Owen, and H.P. Voorheis. 1985. A new method for the rapid purification of both the membrane-bound and released forms of the variant surface glycoprotein from Trypanosoma brucei. Biochem. J. 230:195-202.
32. Johnson, J.G., and G.A.M. Cross. 1979. Selective cleavage of variant surface glycoproteins from Trypanosoma brucei. Biochem. J. 178:689-697.
33. Lanham, S., and D. Godfrey. 1970. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp. Parsitol. 28:521-534.
34. Lee, M.G.-S., and L.H.T. Van der Ploeg. 1990. Homologous recombination and stable transfection in the parasitic protozoan Trypanosoma brucei. Science (Wash. DC). 250:1583-1587.
35. Masterson, W.J., and M.A.J. Ferguson. 1991. Phenylmethanesulphonyl fluoride inhibits GPI anchor biosynthesis in the African trypanosome. EMBO (Eur. Mol. Biol. Organ.) J. 10:2041-2045.
36. McConville, M.J., and M.A.J. Ferguson. 1993. The structure, biosynthesis and function of glycosylated phosphatidyinositols in the parasitic protozoa and higher eukaryotes. Biochem. J. 294:305-324.
37. Mensa-Wilmot, K., and P.T. Englund. 1992. Glycosyl phosphatidylinositol-specific phospholipase C of Trypanosoma brucei: expression in Escherichia coli. Mol Biochem. Parasitol. 56:311-322.
38. Mensa-Wilmot, K., D. Hereld, and P.T. Englund. 1990. Genomic organisation chromosomal localisation, and developmentally regulated expression of the glycosylphosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Mol. Cell. Biol. 10:720-726.
39. Mensa-Wilmot, K., J.H. LeBowitz, K.-P. Chang, A. Al-Qahtani, B.S. McGwire, S. Tucker, and J.C. Morris. 1994. A glycosylphosphatidylinositol (GPI)-negative phenotype produced in Leishmania major by GPI phospholipase C from Trypanosoma brucei: topography of two GPI pathways. J. Cell Biol. 124:935-947.
40. Miller, E.N., and M.J. Turner. 1981. Analysis of antigenic types appearing in first relapse populations of clones of Trypanosoma brucei. Parasitology. 82: 63-80.
41. Overath, P., J. Czichos, and C. Haas. 1986. The effect of citrate/cis-aconitate on oxidative metabolism during transformation of Trypanosoma brucei. Eur. J. Biochem. 113:223-227.
42. Roditi, I., H. Schwartz, T.W. Pearson, R.P. Beecroft, M.K. Liu, J.P. Richardson, H.-J. Bühring, J. Pleiss, R. Bülow, R.O. Williams, and P. Overath. 1989. Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J. Cell Biol. 108:737-746.
43. Rolin, S., P. Paindavoine, J. Hanocq-Quertier, F. Hanocq, Y. Claes, D. Le Ray, P. Overath, and E. Pays. 1993. Transient adenylate cyclase activation accompanies differentiation of Trypanosoma brucei from bloodstream to procyclic forms. Mol. Biol. Parasitol. 61:115-126.
44. Rolin, S., J. Hanocq-Quertier, F. Paturiaux-Hanocq, D. Nolan, D. Salmon, H. Webb, M. Carrington, P. Voorheis, and E. Pays. 1996. Simultaneous but independent activation of adenylate cyclase and glycosylphosphatidylinositol-phospholipase C under stress conditions in Trypanosoma brucei. J. Biol. Chem. 271:10844-10852.
45. Seyfang, A., D. Mecke, and M. Duszenko. 1990. Degradation, recycling, and shedding of Trypanosoma brucei variant surface glycoprotein. J. Protozool. 37:546-552.
46. ten Asbroek, A.L.M.A., M. Ouellette, and P. Borst. 1990. Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature (Lond.). 348:174-175.
47. ten Asbroek, A.L.M.A., C.A.A.M. Mol, R. Kieft, and P. Borst. 1993. Stable transformation of Trypanosoma brucei. Mol. Bioch. Parasitol. 59:133-142.
48. Turner, C.M.R. 1990. The use of experimental artefacts in African trypanosome research Parasitol. Today. 6:14-17.
49. Turner, C.M.R., N. Aslam, and C. Dye. 1995. Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology. 111:289-300.
50. Van Meirvenne, N., P. Jansen, and E. Magnus. 1975. Antigenic variation in syringe-passaged populations of Trypanosoma (Trypanozoon) brucei. Ann. Soc. Belge Med. Trop. 55:1-23.
51. Vidugiriene, J., and A.K. Menon. 1993. Early lipid intermediates in glycosylphosphatidylinositol anchor assembly are synthesised in the ER and location in the cytoplasmic leaflet of the ER membrane bilayer. J. Cell Biol. 121:987-990.
52. Vidugiriene, J., and A.K. Menon. 1994. The GPI anchor of cell-surface protein is synthesized on the cytoplasmic face of the endoplasmic reticulum. J. Cell Biol. 127:333-341.
53. Voorheis, H.P., and B.R. Martin. 1980. "Swell dialysis" demonstrates that adonylate cyclase in Trypanosoma brucei is regulated by calcium ions. Eur. Biochem. 113:223-227.
54. Voorheis, H.P., D.J. Bowles, and G.A. Smith. 1982. Characteristics of the nuclease of the surface coat protein from bloodstream forms of Trypanosoma brucei. J. Biol. Chem. 257:2300-2304.
55. Zamze, S.E., M.A.J. Ferguson, R. Collins, R.A. Dwek, and T.W. Rademacher 1988. Characterisation of the cross-reacting determinant (CRD) of the glycosyl-phosphatidylinositol membrane anchor of Trypanosoma brucei variation surface glycoprotein. Eur. J. Biochem. 176:527-534.
56. Ziegelbauer, K., M. Quinten, H. Schwartz, T. Pearson, and P. Overath. 1990. Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur. J. Biochem. 192:373-378.
57. Ziegelbauer, K., B. Stahl, M. Karas, Y.-D. Stierhof, and P. Overath. 1993. Proteolytic release of cell surface proteins during differentiation of Trypanosoma brucei. Biochemistry. 32:3737-3742.
58. Zimmerman, U. 1982. Electric field mediated fusion and related electrical phanomena Biochem. Biophys. Acta. 694:227-277.