Cell lysis induces redistribution of the GPI-anchored variant surface glycoprotein on both faces of the plasma membrane of Trypanosoma brucei

Journal of Cell Science

Volumn 112, Issue 23, 1999, Pages 4461-4473

  De Almeida, M Lucia Cardoso ^a,b   Geuskens, Maurice ^a   Pays, Etienne ^a  

^a FREE UNIVERSITY OF BRUSSELS   (Belgium)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Glycosylphosphatidylinositol (GPI); Phospholipase C; Protein asymmetry; Trypanosome; VSG

Indexed keywords

BENZENESULFONIC ACID DERIVATIVE; GLYCOPROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; MEMBRANE PROTEIN; PHOSPHOLIPASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOLYSIS; MEMBRANE FUSION; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN VARIANT; TEMPERATURE; TRYPANOSOMA BRUCEI;

ANIMALS; CELL MEMBRANE; CYTOPLASM; GENE DELETION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HYPOTONIC SOLUTIONS; MICROTUBULES; PHOSPHATIDYLINOSITOL DIACYLGLYCEROL-LYASE; PHOSPHOLIPASE C; TRYPANOSOMA BRUCEI BRUCEI; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA;

ANIMALIA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0033492446     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Armah, D. A. and Mensa-Wilmot, K. (1999). S-Myristoylation of a glycosylphosphatidylinositol-specific phospholipase C in Trypanosoma brucei. J. Biol. Chem. 274, 5931-5938.
2. Bangs, J. D., Doering, T. L., Englund, P. T. and Hart, G. W. (1988). Biosynthesis of a variant surface glycoprotein of Trypanosoma brucei: processing of the glycolipid membrane anchor and N-linked oligosaccharides. J. Biol. Chem. 263, 17697-17705.
3. Barry, J. D. (1979). Capping of variable antigen on Trypanosoma brucei and its inimunological and biological significance. J. Cell Sci. 37, 287-302.
4. Black, S. J., Hewett, R. S. and Sendashonga, C. N. (1982). Trypanosoma brucei variable surface antigen is released by degenerating parasites but not by actively dividing parasites. Parasite Immunol. 4, 233-244.
5. Blum, M. L., Down, A., Gurnett, A. M., Carrington, M., Turner, M. J. and Wiley, D. C. (1993). A structural motif in the variant surface glycoproteins of Trypanosoma brucei. Nature 362, 603-609.
6. Borst, P. and Fairlamb, A. H. (1998). Surface receptors and transporters of Trypanosoma brucei. Annu. Rev. Microbiol. 52, 745-778.
7. 2+ FEBS Lett. 139, 17-21.
8. Bülow, R. and Overath, P. (1985). Synthesis of a hydrolase for the membrane form variant surface glycoprotein is repressed during transformation of Trypanosoma brucei. FEBS Lett. 187, 105-110.
9. Bülow, R. and Overath, P. (1986). Purification and characterization of the membrane-form variant surface glycoprotein hydrolase of Trypanosoma brucei. J. Biol. Chem. 261, 11918-11923.
10. Bülom, R., Overath, P. and Davoust, J. (1988). Rapid lateral diffusion of the variant surface glycoprotein in the coat of Trypanosoma brucei. Biochemistry 27, 2384-2388.
11. Bülow, R., Griffiths, G., Webster, P., Stierhof, Y.-D., Opperdoes, F. and Overath, P. (1989). Intracellular location of the glycosylphosphatidylinositol-speeitic phospholipase C of Trypanosoma brucei. J. Cell Sci. 93, 233-240.
12. Bütikofer, P., Boschung, M., Brodbeck, U. and Menon, A. K. (1996). Phosphatidylinositol hydrolysis by Trypanosoma brucei glycosylphosphatidylnositol phospholipase C. J. Biol. Chem. 271, 15533-15541.
13. Cardoso de Almeida, M. L. and Turner, M. J. (1983). The membrane form of variant surface glycoproteins of Trypanosoma brucei. Nature 302, 349-352.
14. Carnall, N., Webb, H. and Carrington, M. (1997). Mutagenesis study of the glycosylphosphatidylinositol phospholipase C of Trypanosoma brucei. Mol. Biochem. Parasitol. 90, 423-432.
15. Carrington, M., Bülow, R., Reinke, H. and Overath, P. (1989). Sequence and expression of the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Mol. Biochem. Parasitol. 33, 289-296.
16. Carrington, M., Miller, N., Blum, M., Roditi, I. and Wiley, D. (1991). Variant specific glycoprotein of Trypanosoma brucei consists of two domains each having an independently conserved pattern of cysteine residues. J. Mol. Biol. 221, 823-835.
17. Carrington, M., Carnall, N., Crow, M. S., Gaud, A., Redpath, M. B., Wasunna, C. L. and Webb, H. (1998). The properties and function of the glycosylphosphatidylinositol-phospholipase C in Trypanosoma brucei. Mol. Biochem. Parasitol. 91, 153-164.
18. Cross, G. A. M. (1990). Cellular and genetic aspects of antigenic variation in trypanosomes. Annu. Rev. Immunol. 8, 83-110.
19. Devaux, P. F. (1991). Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163-1173.
20. Englund, P. T. (1993). The structure and biosynthesis of glycosylphosphatidylinositol protein anchors. Annu. Rev. Biochem. 62, 121-138.
21. Esser, K. M. and Schoenbechler, M. J. (1985). Expression of two variant surface glycoproteins on individual African trypanoosomes during antigen switching. Science 229, 190-193.
22. Ferguson, M. A. J., Homans, S. W., Dwek, R. A. and Rademacher, T. W. (1988). Glycosylphosphatidylinosilol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science 239, 753-759.
23. Field, M. C., Menon, A. K. and Cross, G. A. M. (1991). A glycosylphosphatidylnositol protein anchor from procyclic stage Trypanosoma brucei: lipid structure and biosynthesis. EMBO J. 10, 2731-2739.
24. Fox, J. A., Duszenko, M., Ferguson, M. A. J., Low, M. G. and Cross, G. A. M. (1986). Purification and characterization of a novel glycanphosphatidylinositol-specific phospholipase C from Trypanosoma brucei. J. Biol. Chem. 261, 15767-15771.
25. Frevert, U., Herzberg, F., Reinwald, E. and Risse, M. J. (1986). Morphological changes in Trypanosoma congolense after proteolytic removal of the surface coat. J. Ultrastruct. Mol. Struct. Res. 94, 140-148.
26. Garg, N., Tarleton, R. L. and Mensa-Wilmot, K. (1997). Proteins with glycosylphosphatidylinositol (GPI) signal sequences have divergent fates during a GPI deficiency. J. Biol. Chem. 272, 12482-12491.
27. Gurnett, A. M., Raper, J., Ward, J. and Turner, M. J. (1986). Purification and characterization of membrane form VSG of Trypanosoma brucei. Mol. Biochem. Parasitol. 20, 1-13.
28. Güther, M. L. S., Cardoso de Almeida, M. L., Rosenberry, T. L. and Ferguson, M. A. J. (1994). The detection of phospholipase-resistant and sensitive glycosylphosphatidylinositol membrane anchors by western blotting. Anal. Biochem. 219, 249-255.
29. Hereld, D., Krakow, J. L., Bangs, J. D., Hart, G. W. and Englund, P. T. (1986). A phospholipase C from Trypanosoma brucei which selectively cleaves the glycolipid on the variant surface glycoprotein. J. Biol. Chem. 261, 13813-13819.
30. Hereld, D., Hart, G. W. and Englund, P. T. (1988). cDNA encoding the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Proc. Nat. Acad. Sci. USA 85, 8914-8918.
31. Jokiranta, T. S., Jokipii, L. and Meri, S. (1995). Complement resistance of parasites. Scand. J. Immunol. 42, 9-20.
32. Lanham, S. M. and Godfrey, D. G. (1970). Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp. Parasitol. 28, 521-534.
33. Lasic, D. D. (1988). The mechanism of vesicle formation. Biochem. J. 256, 1-11.
34. Magez, S., Stijlemans, B., Radwanska, M., Pays, E., Ferguson, M. A. J. and De Baetselier, P. (1998). The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. J. Immunol. 160, 1949-1956.
35. Martin, I., Turco, S. J., Epand, R. M. and Ruysschaert, J.-M. (1998). Lipophosphoglycan of Leishmania donovani inhibits lipid vesicle fusion induced by the N-terminal extremity of viral fusogenic SIV protein. Eur. J. Biochem. 258, 150-156.
36. Melikyan, G. B., White, J. M. and Cohen, F. S. (1995). GPI-anchored influenza haemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131, 679-691.
37. Menon, A. K. (1995). Flippases. Trends Cell Biol. 5, 355-360.
38. Mensa-Wilmot, K., LeBowitz, J. H., Chang, K.-P., Al-Qahtani, A., McGwire, B. S., Tucker, S. and Morris, J. C. (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.
39. Morris, J. C., Ping-Sheng, L., Shen, T.-Y. and Mensa-Wilmot, K. (1995). Glycan requirements of glycosylphosphatidylinositol phospholipase C from Trypanosoma brucei. J. Biol. Chem. 270, 2517-2524.
40. Mũoz-Jordán, J., Davies, K. P. and Cross, G. A. M. (1996). Stable expression of mosaic coats of variant surface glycoproteins in Trypanosoma brucei. Science 272, 1745-1797.
41. Nolan, D. P., Rolin, S., Rodriguez, J. R., Van Den Abeele and Pays, E.. (1999). Slender and stumpy bloodstream forms of Trypanosoma brucei display a differential response to extracellular acidic and proteolytic stress. Eur. J. Biochemistry (in press).
42. Overath, P., Stierhof, Y.-D. and Wiese, M. (1997). Endocytosis and secretion in trypanosomatid parasites - tumultuous traffic in a pocket. Trends Cell Biol. 7, 27-33.
43. Pays, E., Vanhamme, L. and Berberof, M. (1994). Genetic controls for the expression of surface proteins in African trypanosomes. Annu. Rev. Microbiol. 48, 25-52.
44. Rehaber, P., Staudacher, N., Seckler, R., Bülow, R., Overath, P. and Jaenicke, R. (1990). Stability and reconstitution of the soluble variant surface glycoprotein (sVSG) from Trypanosoma brucei. Biochemistry 29, 8217-8223.
45. Reynolds, E. S. (1963). The use of lead citrate at high pH as electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-213.
46. Robinson, D., Beattie, P., Sherwin, T. and Gull, K. (1991). Microtubules, tubulin and microtubule-associated proteins of trypanosomes. Meth. Enzymol. 196, 285-299.
47. Rolin, S., Hanocq-Quertier, J., Paturiaux-Hanocq, F., Nolan, D., Salmon, D., Webb, H., Carrington, M., Voorheis, P. and Pays, E. (1996) Simultaneous but independent activation of adenylate cyclase and glycosylphosphatidylinositol-phospholipase C under stress conditions in Trypanosoma brucei. J. Biol. Chem. 271, 10844-10852.
48. Ross, C., Cardoso de Almeida, M. L. and Turner, M. J. (1987). Variant surface glycoproteins of Trypanasoma congolense bloodstream and metacyclic forms are anchored by a glycolipid tail. Mol. Biochem. Parasitoi. 22, 153-158.
49. Russo, D. C. W., Grab, D. J., Lonsdale-Eccles, J. D., Shaw, M. K. and Williams, D. J. L. (1993). Directional movement of variable surface glycoprotein antibody complexes in Trypanosoma brucei. Eur. J. Cell Biol. 62, 432-441.
50. Salmon, D., Geuskens, M., Hanocq, F., Hanocq-Quertier, J., Nolan, D., Ruben, L. and Pays, E. (1994). A novel heterodimeric transferrin receptor encoded by a pair of VSG expression site-associated genes in Trypanosoma brucei. Cell 78, 75-86.
51. Sanders, II C. R. and Schwonek, J. P. (1992). Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31, 8898-8905.
52. Sanders, II C. R. and Landis, G. C. (1995). Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 43, 4030-4040.
53. Seyfang, A., Mecke, D. and Duszenko, M. (1990). Degradation, recycling and shedding of Trypanosoma brucei variant surface glycoprotein. J. Protozol. 37, 546-552.
54. Shakibaei, M. and Frevert, U. (1992). Cell surface interactions between Trypanosoma congolense and macrophages during phagocytosis in vitro. J. Protozol. 39, 224-235.
55. Shapiro, S. Z. (1986). Trypanosoma brucie: release of variant surface glycoprotein during the parasite life cycle. Exp. Parasitol. 61, 432-437.
56. Steverding, D., Stierhof, Y., Chaudhri, M., Ligtenberg, M., Schell, D. A., Beck-Sickinger, F. and Overath, P. (1994). BSAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur. J. Cell Biol. 64, 78-87.
57. Tetley, L., Vickerman, K. and Moloo, S. K. (1981). Absence of a surface coat from metacyclic Trypanosoma vivax: possible implications for vaccination against vivax trypanosomiasis. Trans. R. Soc. Trop. Med. Hyg. 75, 409-414.
58. Turner, M. J., Cardoso de Almeida, M. L., Gurnett, A. M., Raper, J. and Ward, J. (1985). Biosynthesis, attachment and release of variant surface glycoproteins of the African trypanosome. Curr. Topics Microbiol. Immunol. 117, 23-55.
59. van Gelderen, I. L., van Meer, G., Slot, J. W., Geuze, M. J. and Voorhout, W. F. (1991). Subcellular localization of Forssman glycolipid in epithelial MDCK cells by immuno-electronmicroscopy after freeze-substitution. J. Cell Biol. 115, 1009-1019.
60. Vidugiriene, J. and Menon, A. K. (1994). The GPI anchor of cell-surface proteins is synthesized on the cytoplasmic face of the endoplasmic reticulum. J. Cell Biol. 127, 333-341.
61. Vieira, L. L. (1998). pH and volume homeostasis in trypanosomatids: current views and perspectives. Bioch. Biophys. Acta 1376, 221-241.
62. Voorheis, P. H., Gale, J. S., Owen, M. J. and Edwards, W. (1979). The isolation and partial characterisation of the plasma membrane from Trypanosoma brucei. Biochem. J. 180, 11-24.
63. Webb, H., Carnall, N., Vanhamme, L., Rolin, S., Van Den Abbeele, J., Welburn, S., Pays, E. and Carrington, M. (1997). The GPI-phospholipase C of Trypanosoma brucei is nonessential but influences parasitemia in mice. J. Cell Biol. 139, 103-114.
64. Webster, P. and Grab, D. J. (1988). Intracellular colocalization of variant surface glycoprotein and transferrin-gold in Trypanosoma brucei. J. Cell Biol. 106, 279-288.
65. White, J. M. (1992). Membrane fusion. Science 258, 917-923.
66. Wright, K. A. and Hales, H. (1970). Cytochemistry of the pellicle of bloodstream forms of Trypanosoma (Trypanosoma) brucei. J. Parasitol. 56, 671-683.
67. Zamze, S. E., Ferguson, M. A. J., Collins, R., Dwek, R. A. and Rademacher, T. W. (1988). Characterization of the cross-reacting determinant (CRD) of the glycosyl-phosphatidylinositol membrane anchor of Trypanosoma brucei variant surface glycoprotein. Eur. J. Biochem. 176, 527-534.