Addition of α-O-GlcNAc to threonine residues define the post-translational modification of mucin-like molecules in Trypanosoma cruzi

Glycoconjugate Journal

Volumn 30, Issue 7, 2013, Pages 659-666

  Mendonça Previato, Lucia ^a   Penha, Luciana ^a   Garcez, Tatiana Cortes ^a   Jones, Christopher ^b   Previato, Jose Osvaldo ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Mucins; Posttranslational modification; pp GlcNAcT; trans sialidase; Trypanosoma cruzi

Indexed keywords

ALPHA O LINKED 2 N ACETAMIDO 2 DEOXY DEXTRO GLUCOPYRANOSE; BETA GALACTOFURANOSE; CARBOHYDRATE DERIVATIVE; MUCIN; OLIGOSACCHARIDE; SIALIDASE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CARBOHYDRATE ANALYSIS; CHAGAS DISEASE; CHEMICAL MODIFICATION; CONTROLLED STUDY; ENZYME ACTIVITY; GLYCOSYLATION; GOLGI COMPLEX; NONHUMAN; PARASITE TRANSMISSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIALYLATION; TRYPANOSOMA CRUZI;

MAMMALIA; PROTOZOA; TRYPANOSOMA CRUZI;

ACETYLGLUCOSAMINE; GLYCOSYLATION; MUCINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTOZOAN PROTEINS; THREONINE; TRYPANOSOMA CRUZI;

EID: 84884592083     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-013-9469-7     Document Type: Article

References (51)

1. WHO: Chagas disease (American trypanosomiasis). Fact sheet 340 (2010)
2. Machado, F.S., Jelicks, L.A., Kirchhoff, L.V., Shirani, J., Nagajyothi, F., Mukherjee, S., Nelson, R., Coyle, C.M., Spray, D.C., de Carvalho, A.C., Guan, F., Prado, C.M., Lisanti, M.P., Weiss, L.M., Montgomery, S.P., Tanowitz, H.B.: Chagas heart disease: report on recent developments. Cardiol. Rev. 20(2), 53-65 (2012)
3. Bellini, M.F., Silistino-Souza, R., Varella-Garcia, M., de Azeredo-Oliveira, M.T., Silva, A.E.: Biologic and genetics aspects of Chagas disease at endemic areas. J. Trop. Med. (2012). doi: 10.1155/2012/357948. Article ID 357948
4. Zingales, B., Andrade, S.G., Briones, M.R., Campbell, D.A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A.M., Machado, C.R., Miles, M.A., Romanha, A.J., Sturm, N.R., Tibayrenc, M., Schijman, A.G.: Second satellite meeting. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem. Inst. Oswaldo Cruz 104(7), 1051-1054 (2009)
5. Ramírez, J.D., Guhl, F., Rendón, L.M., Rosas, F., Marin-Neto, J.A., Morillo, C.A.: Chagas cardiomyopathy manifestations and Trypanosoma cruzi genotypes circulating in chronic Chagasic patients. PLoS Negl. Trop. Dis. 4(11), e899 (2010)
6. Guhl, F., Ramírez, J.D.: Trypanosoma cruzi I diversity: towards the need of genetic subdivision? Acta Trop. 119(1), 1-4 (2011)
7. Previato, J.O., Jones, C., Xavier, M.T., Wait, R., Travassos, L.R., Parodi, A.J., Mendonça-Previato, L.: Structural characterization of the major glycosylphosphatidylinositol membrane anchored glycoprotein of epimastigote forms of Trypanosoma cruzi Y-strain. J. Biol. Chem. 270(13), 7241-7250 (1995)
8. Previato, J.O., Jones, C., Gonçalves, L.P., Wait, R., Travassos, L.R., Mendonça-Previato, L.: O-Glycosidically linked N-acetylglucosamine- bound oligosaccharides from glycoproteins of Trypanosoma cruzi. Biochem. J. 301(Pt1), 151-159 (1994)
9. Di Noia, J.M., Pollevick, G.D., Xavier, M.T., Previato, J.O., Mendoça-Previato, L., Sánchez, D.O., Frasch, A.C.: High diversity in mucin genes and mucin molecules in Trypanosoma cruzi. J. Biol. Chem. 271(50), 32078-32083 (1996)
10. Mendonça-Previato, L., Todeschini, A.R., Heise, N., Agrellos, O.A., Previato, J.O.: Chemical structure of major glycoconjugates from parasites. Curr. Org. Chem. 12(11), 926-939 (2008)
11. Previato, J.O., Andrade, A.F.B., Pessolani, M.C.V., Mendonça Previato, L.: Incorporation of sialic acid into Trypanosoma cruzi macromolecules - a proposal for a new metabolic route. Mol. Biochem. Parasitol. 16(1), 85-96 (1985)
12. Mendonça-Previato, L., Todeschini, A.R., Freire de Lima, L., Previato, J.O.: The trans-Sialidase from Trypanosoma cruzi a Putative Target for Trypanocidal Agents. Open Parasitol. J. 4, 111-115 (2010)
13. Previato, J.O., Sola-Penna, M., Agrellos, O.A., Jones, C., Oeltmann, T., Travassos, L.R., Mendonça-Previato, L.: Biosynthesis of O-N-acetylglucosamine-linked glycans in Trypanosoma cruzi: characterisation of the novel uridine diphospho-N-acetylglucosamine:polypeptide N-acetyl- glucosaminyl transferase catalysing formation of the α-N- acetylglucosamine(1 → O)-threonine linkage. J. Biol. Chem. 273(24), 14982-14988 (1998)
14. Ten Hagen, K.G., Fritz, T.A., Tabak, L.A.: All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13(1), 1R-16R (2003)
15. North, S.J., Hitchen, P.G., Haslam, S.M., Dell, A.: Mass spectrometry in the analysis of N-linked and O-linked glycans. Curr. Opin. Struct. Biol. 19(5), 498-506 (2009)
16. Cullen, P.J.: Post-translational regulation of signaling mucins. Curr. Opin. Struct. Biol. 21(5), 590-596 (2011)
17. Todeschini, A.R., de Almeida, E.G., Agrellos, O.A., Jones, C., Previato, J.O., Mendonça-Previato, L.: Alpha-N-acetylglucosamine-linked O-glycans of sialoglycoproteins (Tc-mucins) from Trypanosoma cruzi Colombiana strain. Mem. Inst. Oswaldo Cruz 104(Suppl 1), 270-274 (2009)
18. Miles, M.A., Souza, A., Povoa, M., Shaw, J.J., Lainson, R., Toye, P.J.: Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature (London) 272, 819-821 (1978)
19. Slawson, C., Hart, G.W.: O-GlcNAc signalling: implications for cancer cell biology. Nat. Rev. Cancer 11(9), 678-684 (2011)
20. Zachara, N.E., Vosseller, K., Hart, G.W.: Detection and analysis of proteins modified by O-linked N-acetylglucosamine. Curr. Protoc. Protein Sci. 66(12.8), 1-12 (2011)
21. Morgado-Díaz, J.A., Nakamura, C.V., Agrellos, O.A., Dias, W.B., Previato, J.O., Mendonça-Previato, L., De Souza, W.: Isolation and characterization of the Golgi complex of the protozoan Trypanosoma cruzi. Parasitology 123(Pt1), 33-43 (2001)
22. Haltiwanger, R.S., Holt, G.D., Hart, G.W.: Enzymatic addition of O-GlcNAc to nuclear and cytoplasmic proteins - identification of uridine diphospho-N-acetylglucosamine peptide β-N-acetylglucosaminyltransferase. J. Biol. Chem. 265(5), 2563-2568 (1990)
23. Heise, N., Singh, D., van der Wel, H., Sassi, S.O., Johnson, J.M., Feasley, C.L., Koeller, C.M., Previato, J.O., Mendonça-Previato, L., West, C.M.: Molecular analysis of a UDP-GlcNAc:polypeptide alpha-N- acetylglucosaminyltransferase implicated in the initiation of mucin-type O-glycosylation in Trypanosoma cruzi. Glycobiology 19(8), 918-933 (2009)
24. Wang, F., Metcalf, T., van der Wel, H., West, C.M.: Initiation of mucin-type O-glycosylation in dictyostelium is homologous to the corresponding step in animals and is important for spore coat function. J. Biol. Chem. 278(51), 51395-51407 (2003)
25. West, C.M., Van Der Wel, H., Sassi, S., Gaucher, E.: Cytoplasmic glycosylation of protein-hydroxyproline and its relationship to other glycosylation pathways. Biochem. Biophys. Acta 1673(1-2), 29-44 (2004)
26. Chiribao, M.L., Libisch, M.G., Osinaga, E., Parodi-Talice, A., RobelloCloning, C.: Localization and differential expression of the Trypanosoma cruzi TcOGNT-2 glycosyl transferase. Gene 498(2), 147-154 (2012)
27. Jones, C., Todeschini, A.R., Agrellos, O.A., Previato, J.O., Mendonça-Previato, L.: Heterogeneity in the biosynthesis of mucin O-glycans from Trypanosoma cruzi Tulahuen strain with the expression of novel galactofuranosyl-containing α-O-GlcNAc-linked oligosaccharides. Biochemistry 43(37), 11889-11897 (2004)
28. Agrellos, O.A., Jones, C., Previato, J.O., Mendonça-Previato, L.: A novel sialylated and galactofuranose-containing O-linked glycan, Neu5Acα2 → Galpβ1 → 6(Galfβ1 → 4)GlcNAc, is expressed on the sialoglycoprotein of Trypanosoma cruzi Dm28c. Mol. Biochem. Parasitol. 126(1), 93-96 (2003)
29. Todeschini, A.R., Xavier da Silveira, E., Jones, C., Wait, R., Previato, J.O., Mendonça-Previato, L.: Structures of O-Glycosidically linked oligosaccharides from glycoproteins of Trypanosoma cruzi CL-Brener strain: Evidence for the presence of O-linked sialyloligosaccharides. Glycobiology 11(1), 47-55 (2001)
30. Almeida, I.C., Ferguson, M.A.J., Schenkman, S., Travassos, L.R.: Lytic anti-α-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosylphosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem. J. 304(3), 793-802 (1994)
31. Pereira-Chioccola, V.L., Acosta-Serrano, A., Almeida, I.C., Ferguson, M.A., Souto-Padron, T., Rodrigues, M.M., Travassos, L.R., Schenkman, S.: Mucin-like molecules form a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-alpha-galactosyl antibodies. J. Cell Sci. 113(7), 1299-1307 (2000)
32. Mendonça-Previato, L., Gorin, P.A., Braga, A.F., Scharfstein, J., Previato, J.O.: Chemical structure and antigenic aspects of complexes obtained from epimastigotes of Trypanosoma cruzi. Biochemistry 22(21), 4980-4987 (1983)
33. Agustí, R., Giorgi, M.E., Mendoza, V.M., Gallo-Rodriguez, C., de Lederkremer, R.M.: Comparative rates of sialylation by recombinant trans-sialidase and inhibitor properties of synthetic oligosaccharides from Trypanosoma cruzi mucins-containing galactofuranose and galactopyranose. Bioorg. Med. Chem. 15(7), 2611-2616 (2007)
34. Serrano, A.A., Schenkman, S., Yoshida, N., Mehlert, A., Richardson, J.M., Ferguson, M.A.J.: The lipid structure of the glycosylphosphatidylinositol- anchored mucin-like sialic-acid acceptors of Trypanosoma cruzi changes during parasite differentiation from epimastigotes to infective metacyclic trypomastigote forms. J. Biol. Chem. 270(45), 27244-27253 (1995)
35. Vandekerckhove, F., Schenkman, S., Pontes de Carvalho, L., Tomlinson, S., Kiso, M., Yoshida, M., Hasegawa, A., Nussenzweig, V.: Substrate specificity of the Trypanosoma cruzi trans-sialidase. Glycobiology 2(6), 541-548 (1992)
36. Scudder, P., Doom, J.P., Chuenkoval, M., Manger, I.D., Pereira, M.E.A.: Enzymatic characterization of beta-D-galactoside alpha 2,3-trans-sialidase from Trypanosoma cruzi. J. Biol. Chem. 268(13), 9886-9891 (1993)
37. Schenkman, S., Ferguson, M.A.J., Heise, N., de Almeida, M.L., Mortara, R.A., Yoshida, N.: Mucin-like glycoproteins linked to the membrane by glycosylphosphatidylinositol anchor are the major acceptors of sialic acid in a reaction catalyzed by trans-sialidase in metacyclic forms of Trypanosoma cruzi. Mol. Biochem. Parasitol. 59(2), 293-303 (1993)
38. Schenkman, S., Eichinger, D.: Trypanosoma cruzi trans-sialidase and cell invasion. Parasitol. Today 6(6), 218-222 (1993)
39. Tomlinson, S., Pontes de Carvalho, L.C., Vandekerckhove, F., Nussenzweig, V.: Role of sialic acid in the resistance of Trypanosoma cruzi trypomastigotes to complement. J. Immunol. 153(7), 3141-3147 (1994)
40. Buscaglia, C.A., Campo, V.A., Frasch, A.C.C., Di Noia, J.M.: Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat. Rev. Microbiol. 4(3), 229-236 (2006)
41. Salazar, N.A., Mondragon, A., Kelly, J.M.: Mucin-like glycoprotein genes are closely linked to members of the trans-sialidase super-family at multiple sites in the Trypanosoma cruzi genome. Mol. Biochem. Parasitol. 78(1-2), 127-136 (1996)
42. Schenkman, S., Jiang, M.S., Hart, G.W., Nussenzweig, V.: A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65(7), 1117-1125 (1991)
43. Brener, Z.: Biology of Trypanosoma cruzi. Annu. Rev. Microbiol. 27, 347-382 (1973)
44. Yoshida, N.: Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An. Acad. Bras. Cienc. 78(1), 87-111 (2006)
45. Fernandes, M.C., Andrews, N.W.: Host cell invasion by Trypanosoma cruzi: a unique strategy that promotes persistence. FEMS Microbiol. Rev. 36(3), 734-747 (2012)
46. Camargo, M.M., Almeida, I.C., Pereira, M.E., Ferguson, M.A.J., Travassos, L.R.: Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes initiate the synthesis of proinflammatory cytokines by macrophages. J. Immunol. 158(12), 5890-5901 (1997)
47. Yoshida, N., Dorta, M.L., Ferreira, A.T., Oshiro, M.E., Mortara, R.A., Acosta-Serrano, A., Favoreto Júnior, S.: Removal of sialic acid from mucin-like surface molecules of Trypanosoma cruzi metacyclic trypomastigotes enhances parasite-host cell interaction. Mol. Biochem. Parasitol. 84(1), 57-67 (1997)
48. Ruiz, R.C., Rigoni, V.L., Gonzalez, J., Yoshida, N.: The 35/50 kDa surface antigen of Trypanosoma cruzi metacyclic trypomastigotes, an adhesion molecule involved in host cell invasion. Parasite Immunol. 15(2), 121-125 (1993)
49. Yoshida, N., Mortara, R.A., Araguth, M.F., Gonzalez, J.C., Russo, M.: Metacyclic neutralizing effect of monoclonal antibody 10D8 directed to the 35- and 50-kilodalton surface glycoconjugates of Trypanosoma cruzi. Infect. Immun. 57(6), 1663-1667 (1989)
50. Ruiz, R.C., Favoreto Jr., S., Dorta, M.L., Oshiro, M.E., Ferreira, A.T., Manque, P.M., Yoshida, N.: Infectivity of Trypanosoma cruzi strains is associated with differential expression of surface glycoproteins with differential Ca2+ signaling activity. Biochem. J. 330(1), 505-511 (1998)
51. Mortara, R.A., Silva, S., Araguth, M.F., Blanco, S.A., Yoshida, N.: Glycoconjugates of Trypanosoma cruzi metacyclic trypomastigotes. Infect. Immun. 60(11), 4673-4678 (1992)