Terminal galactosylation of glycoconjugates in Plasmodium falciparum asexual blood stages and Trypanosoma brucei bloodstream trypomastigotes

Experimental Parasitology

Volumn 130, Issue 4, 2012, Pages 314-320

  Ramasamy, Ranjan ^a,b   Field, Mark C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITI BRUNEI DARUSSALAM   (Brunei Darussalam)

Author keywords

Bandeirea (Griffonia) simplicifolia B4 lectin 1; Galactosylation; Glycoconjugate; Plasmodium falciparum; Trypanosoma brucei

Indexed keywords

B4 LECTIN 1; GALACTOSE; GALACTOSYLTRANSFERASE; GLYCOLIPID; GLYCOPROTEIN; LECTIN; PROTOZOAL PROTEIN; TRITIUM; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE;

AMINO ACID SEQUENCE; ARTICLE; ASEXUAL REPRODUCTION; BANDEIREA SIMPLICIFOLIA; BINDING AFFINITY; CONTROLLED STUDY; DEVELOPMENTAL STAGE; GRIFFONIA; IN VITRO STUDY; LECTIN BINDING; MICROSOME; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; STRUCTURAL BIOINFORMATICS; TRYPANOSOMA BRUCEI; TRYPOMASTIGOTE;

FLUORESCEIN-5-ISOTHIOCYANATE; GALACTOSE; GALACTOSYLTRANSFERASES; GLYCOCONJUGATES; GLYCOLIPIDS; HUMANS; IMMUNE SERA; MICROSOMES; PLANT LECTINS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; TRITIUM; TRYPANOSOMA BRUCEI BRUCEI;

GRIFFONIA; PLASMODIUM FALCIPARUM; TRYPANOSOMA BRUCEI;

EID: 84859106882     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2012.02.017     Document Type: Article

References (55)

1. Almeida I.C., Ferguson M.A.J., Shenkman S., Travassos L.R. Lytic anti-α-galactosyl antibodies from patients with chronic Chagas' disease recognise novel O-linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma brucei. Biochemical Journal 1994, 304:793-802.
2. Atrih A., Richardson J.M., Prescott A.R., Ferguson M.A.J. Trypanosoma brucei glycoproteins contain novel giant poly-N-acetyllactosamine carbohydrate chains. Journal of Biological Chemistry 2005, 280(2):865-871.
3. Botte C., Saidani N., Mondragon R., Mondragon M., Isaac G., Mui E., McLeod R., Dubremetz J.F., Vial H., Welti R., Cesbron-Delauw M.F., Mercier C., Marechal E. Subcellular localisation and dynamics of a digalactoside-like epitope in Toxoplasma gondii. Journal of Lipid Research 2008, 49:746-762.
4. Buscaglia C.A., Campo V.A., Frasch A.C.C., Di Noia J.M. Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nature Reviews Microbiology 2006, 4:229-236.
5. Cartron J.P., Cartron J., Andreu G., Salmon Ch., Bird G.W.G. Selective deficiency of 3-β-D-galactosyltransferase (T-transferase) in Tn-polyagglutinable erythrocytes. The Lancet 1978, 856-857.
6. Christie W.W. Preparation of lipid extracts from tissues. Advances in Lipid Methodology, vol. 2 1993, 195-213. Oily Press, Dundee. W.W. Christie (Ed.).
7. Chung W.L., Leung K.F., Carrington M., Field M.C. Position-specific ubiquitylation is required for internalisation and degradation of trans-membrane surface proteins in trypanosomes. Traffic 2008, 9:1681-1697.
8. Couto A.S., Caffaro C., Uhrig M.L., Kimura E., Peres V.J., Merino E.F. Glycosphingolipids in Plasmodium falciparum. Presence of an active glucosylceramide synthase. European Journal of Biochemistry 2004, 271:2204-2214.
9. de Macedo C.S., Schwarz R.T., Todeschini A.R., Previato J.O., Mendonça-Previato L. Overlooked post-translational modifications of proteins in Plasmodium falciparum: N- and O-glycosylation - a review. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro. 2010, 105(8):949-956.
10. Delorenzi M., Sexton A., Shams-Eldin H., Schwarz R.T., Speed T., Schofield L. Genes for glycosylphosphatidylinositol toxin biosynthesis in Plasmodium falciparum. Infection and Immunity 2002, 70(8):4510-4522.
11. Ferguson M.A.J., Homans S.W., Dwek R.A., Rademacher T.W. Glycosyl-phosphatidylinositol moiety that anchors Trypanosoma brucei variant surface glycoprotein to the membrane. Science 1988, 239:753-759.
12. Ferguson M.A.J. The structure, biosynthesis and functions of glycosylphosphatidylinositols anchors, and the contributions of trypanosome research. Journal of Cell Science 1999, 112:2799-2809.
13. Foth B.J., McFadden G.I. The apicoplasts: a plastid in Plasmodium falciparum and other apicomplexan parasites. International Review of Cytology 2003, 224:57-110.
14. Gerold P., Dieckmann-Schuppert A., Schwarz R.T. Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malaria parasite, Plasmodium falciparum. Candidate for plasmodial glycosylphosphatidylinositols membrane anchor precursors and pathogenicity factors. Journal of Biological Chemistry 1994, 269:2597-2606.
15. Gerold P., Schwartz R.T. Biosynthesis of glycosphingolipids de-novo by the human malaria parasite Plasmodium falciparum. Molecular and Biochemical Parasitology 2001, 112:29-37.
16. Gilson P.R., Nebl T., Vukcevic D., Moritz R.L., Sargeant T., Speed T.P., Schofield L., Crabb B.S. Identification and stoichiometry of glycosylphosphatidylinositols anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Molecular and Cellular Proteomics 2006, 5:1286-1299.
17. Gowda D.C., Gupta P., Davidson E.A. Glycosylphosphatidylinositols represent the major carbohydrate modification in protein of intraerythrocytic stage Plasmodium falciparum. Journal of Biological Chemistry 1997, 272:6428-6439.
18. Grünfelder C.G., Engstler M., Weise F., Schwarz H., Stierhof Y.D., Boshart M., Overath P. Accumulation of a GPI-anchored protein at the cell surface requires sorting at multiple intracellular levels. Traffic 2002, 3(8):547-559.
19. Guther M.L., Prescott A.R., Ferguson M.A. Deletion of the GPIdeAc gene alters the location and fate of glycosylphosphatidylinositol precursors in Trypanosoma brucei. Biochemistry 2003, 42(49):14532-14540.
20. Hansen D.S., Siomos M.A., Buckingham L., Scalzo A.A., Schofield L. Regulation of murine cerebral malaria pathogenesis by CD-1d restricted NKT cells and the natural killer complex. Immunity 2003, 18:391-402.
21. Harwood J.L. Plant acyl lipids. The Biochemistry of Plants, vol. 4 1980, 1-55. Academic Press, New York. P.K. Stumpf (Ed.).
22. Holder A.A., Freeman R.R. The three major antigens on the surface of Plasmodium falciparum merozoites are derived from a single high molecular weight precursor. Journal of Experimental Medicine 1984, 160:624-629.
23. Jakobsen P.H., Theander T.G., Jensen J.B., Molbek K., Jepsen S. Soluble Plasmodium falciparum antigens contain carbohydrate moieties important for human reactivity. Journal of Clinical Microbiology 1987, 25(11):2075-2079.
24. Kirkeby S., Moe D. Binding of Griffonia simplicifolia 1 isolectin B4 (GS1 B4) to α-galactose antigens. Immunology and Cell Biology 2001, 79:121-127.
25. Krishnegowda G., Hajjar A.M., Zhu J., Douglass E.J., Uematsu S., Akira S., Woods A.S., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signalling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Journal of Biological Chemistry 2005, 280:8606-8616.
26. Landoni M., Duschak V.G., Peres V.J., Nonamid H., Erra-Balsells R., Katzin A.M., Couto A.S. Plasmodium falciparum biosynthesizes sulfoglycosphingolipids. Molecular and Biochemical Parasitology 2007, 154:22-29.
27. Marechal E., Azzouz N., de Macedo C.S., Block M.A., Feagin J.E., Schwartz R.T., Joyard J. Synthesis of chloroplast galactolipids in apicomplexan parasites. Eukaryotic Cell 2002, 1(4):653-656.
28. Masterson W.J., Raper J., Doerling T.L., Hart G.W., Englund P.T. Fatty acid remodelling: a novel reaction sequence in the biosynthesis of trypanosome glycosyl phosphatidylinositol membrane anchors. Cell 1990, 62:73-80.
29. Mayor S., Menon A.K., Cross G.A.M. Galactose-containing glycosylphosphatidylinositols in Trypanosoma brucei. Journal of Biological Chemistry 1992, 267:754-761.
30. McConville M.J., Ferguson M.A.J. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochemical Journal 1993, 294:305-324.
31. Mehlert A., Richardson J.M., Ferguson M.A.J. Structure of the glycophosphatidyl inositol membrane anchor of a class-2 variant surface glycoprotein of Trypanosoma brucei. Journal of Molecular Biology 1988, 277:370-392.
32. Mehlert A., Ferguson M.A.J. Structure of the glycosylphosphatidylinositol anchor of the Trypanosoma brucei transferrin receptor. Molecular and Biochemical Parasitology 2007, 151(2):220-223.
33. Mendonc-Previato L., Todeschini A.R., Heise N., Previato J.O. Protozoan parasite-specific carbohydrate structures. Current Opinion in Structural Biology 2009, 15:499-505.
34. Mya M.M., Roy A., Saxena R.K., Roy K.B. Isolation, part characterisation, immunogenicity and specificity study of Plasmodium falciparum culture supernatant. Japan Journal of Infectious Diseases 2002, 55:150-156.
35. Naik R.S., Branch O.L.H., Woods A.S., Vijaykumar M., Perkins D.J., Lal A.A., Cotter R.J., Costello C.E., Ockenhouse C.F., Davidson E.A., Gowda D.C. Glycophosphatidyl anchors of Plasmodium falciparum: molecular characterisation and naturally elicited antibody response that may provide immunity to malaria pathogenesis. Journal of Experimental Medicine 2000, 192(11):1563-1575.
36. Naus C.W.A., Jones F.M., Satti M.Z., Joseph S., Riley E.M., Kimani G., Mwatha J.K., Kariuki C.H., Ouma J.H., Kabatereine N.B., Vennervald B.J., Dunne D.W. Serological responses among individuals in areas where both schistosomaisis and malaria are endemic: cross-reactivity between Schistosoma mansoni and Plasmodium falciparum. Journal of Infectious Diseases 2003, 187:1272-1282.
37. Pingel S., Field R.A., Guther M.L.S., Duszenko M., Ferguson M.A.J. The hydrophobic mannoside Man αl-6 Man α-S-(CH2)7-CH3 acts as an acceptor for the UDP-Gal:glycosylphosphatidylinositol anchor alpha 1,3-galactosyltransferase of Trypanosoma brucei. Biochemical Journal 1995, 309:877-882.
38. Pingel S., Rheinweiler U., Kolb V., Duszenko M. Purification and characterisation of an α-galactosyl transferase from Trypanosoma brucei. Biochemical Journal 1999, 338:545-551.
39. Ramasamy R., Rajakaruna R. Association of malaria with 1-3 galactosyl transferase inactivation in catarrhines. Biochimica et Biophysica Acta 1997, 1360:241-246.
40. Ramasamy R., Reese R.T. A role for carobohydrate moieties in the immune response to malaria. Journal of Immunology 1985, 134:1952-1955.
41. Ramasamy R., Reese R.T. Terminal galactose residues and the antigenicity of Plasmodium falciparum glycoproteins. Molecular and Biochemical Parasitology 1986, 19:91-101.
42. Ravindran B., Satapathy A.K., Das M.K. Naturally-occurring anti-α-galactosyl antibodies in human Plasmodium falciparum infections - a possible role for autoantibodies in malaria. Immunology Letters 1988, 19:137-142.
43. Samuelson J., Banerjee S., Magnell P., Cui J., Kelleher J., Gilmore R., Robbins P.W. The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proceedings of the National Academy of Sciences USA 2005, 102(5):1548-1553.
44. Schofield L., Hewitt M.C., Evans K., Slomos M.A., Seeburgher P.H. Synthetic GPI as candidate anti-toxic vaccine in model of malaria. Nature 2002, 418:785-789.
45. Schofield L., McConville M.J., Hansen D., Campbell A.S., Fraser-Reid B., Grusby M.J., Tachado S.D. CD1d-restricted immunoglobulin G formation to GPI-anchored antigens mediated by NKT cells. Science 1999, 283:225-228.
46. Tachado S.D., Gerold P., McConville M.J., Baldwin T., Quilici D., Schwarz R.T., Schofield L. Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase C-dependent signalling pathway. Journal of Immunology 1996, 156:1897-1907.
47. Trager W., Jensen J.B. Human malaria parasites in continuous culture. Science 1976, 193:673-675.
48. Tupin E., Kinjo Y., Kronenberg M. The unique role of natural killer T cells in the immune response to microorganisms. Nature Reviews Microbiology 2007, 5:405-417.
49. Uemura A., Watarai S., Kushi Y., Kasama T., Ohnishi Y., Kodama H. Analysis of neutral glycosphingolipids from Trypanosoma brucei. Veterinary Parasitology 2006, 140(3-4):264-272.
50. Vivas L., O' Dea K.P., Noya O., Pabon R., Magres M., Botto C., Holder A.A., Brown K.N. Hyper reactive malarial splenomegaly is associated with low levels of antibodies against red blood cell and Plasmodium falciparum derived glycolipids in Yanomami Amerindians from Venezuela. Acta Tropica 2008, 105:207-214.
51. von Itzstein M., Plebanski M., Cooke B.M., Coppel R.L. Hot, sticky and sweet: the glycobiology of Plasmodium falciparum. Trends in Parasitology 2008, 24(5):211-218.
52. World Health Organisation 2010a. Fact sheet No. 94 Malaria. Genève.
53. World Health Organisation 2010b. Fact sheet No 259 African trypanosomiasis (sleeping sickness). Genève.
54. Zamze S.E., Ashford D.A., Wooten E.W., Rademacher T.W., Dwek R.A. Structural characterization of the asparagine-linked oligosaccharides from Trypanosoma brucei type II and type III variant surface glycoproteins. Journal of Biological Chemistry 1991, 266(30):20244-20261.
55. Ziegelbauer K., Overath P. Organization of two invariant surface glycoproteins in the surface coat of Trypanosoma brucei. Infection and Immunity 1993, 61(11):4540-4545.