Identification of glycoproteins targeted by Trypanosoma cruzi trans-sialidase, a virulence factor that disturbs lymphocyte glycosylation

Glycobiology

Volumn 20, Issue 7, 2010, Pages 833-842

  Muiá, Romina P ^a   Yu, Hai ^b   Prescher, Jennifer A ^c   Hellman, Ulf ^d   Chen, Xi ^b   Bertozzi, Carolyn R ^c   Campetella, Oscar ^a  

^a UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

Author keywords

Azido sugars; CD45; Integrals; Parasite host interactions; Sialylation

Indexed keywords

CD45 ANTIGEN; GLYCOPROTEIN; INTEGRIN; MUCIN; SIALIC ACID; SIALIDASE; SUGAR; PROTOZOAL PROTEIN; TRANS-SIALIDASE; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL POPULATION; CONTROLLED STUDY; CYTOARCHITECTURE; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; LEUKOCYTE; LYMPHOCYTE; MASS SPECTROMETRY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; SPLEEN CELL; THYMOCYTE; TRYPANOSOMA CRUZI; TRYPANOSOMIASIS; ANIMAL; C57BL MOUSE; CHEMISTRY; ENZYMOLOGY; HOST PARASITE INTERACTION; JURKAT CELL LINE; METABOLISM; PATHOGENICITY;

MAMMALIA; TRYPANOSOMA CRUZI;

ANIMALS; GLYCOPROTEINS; GLYCOSYLATION; HOST-PARASITE INTERACTIONS; HUMANS; JURKAT CELLS; LYMPHOCYTES; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; NEURAMINIDASE; PROTOZOAN PROTEINS; TRYPANOSOMA CRUZI; VIRULENCE FACTORS;

EID: 77956266766     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwq037     Document Type: Article

References (56)

1. Acosta-Serrano A, Almeida IC, Freitas-Junior LH, Yoshida N, Schenkman S. 2001. The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol. 114: 143-150.
2. Almeida IC, Ferguson MA, Schenkman S, Travassos LR. 1994. Lytic anti-alpha-galactosyl antibodies from patients with chronic Chagas' disease recognize novel O-linked oligosaccharides on mucin-like glycosyl- phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem J. 304: 793-802.
3. Alvarez P, Buscaglia CA, Campetella O. 2004. Improving protein pharmaco-kinetics by genetic fusion to simple amino acid sequences. J Biol Chem. 279: 3375-3381.
4. Buscaglia CA, Alfonso J, Campetella O, Frasch AC. 1999. Tandem amino acid repeats from Trypanosoma cruzi shed antigens increase the half-life of proteins in blood. Blood. 93: 2025-2032.
5. Buscaglia CA, Campo VA, Frasch AC, Di Noia JM. 2006. Trypanosoma cruzi surface mucins: Host-dependent coat diversity. Nat Rev Microbiol. 4: 229-236.
6. Buschiazzo A, Frasch AC, Campetella O. 1996. Medium scale production and purification to homogeneity of a recombinant trans-sialidase from Trypanosoma cruzi. Cell Mol Biol (Noisy-le-grand). 42: 703-710.
7. Campetella OE, Uttaro AD, Parodi AJ, Frasch AC. 1994. A recombinant Trypanosoma cruzi trans-sialidase lacking the amino acid repeats retains the enzymatic activity. Mol Biochem Parasitol. 64: 337-340.
8. Cotta-de-Almeida V, Bonomo A, Mendes-da-Cruz DA, Riederer I, De Meis J, Lima-Quaresma KR, Vieira-de-Abreu A, Villa-Verde DM, Savino W. 2003. Trypanosoma cruzi infection modulates intrathymic contents of extracellular matrix ligands and receptors and alters thymocyte migration. Eur J Immunol. 33: 2439-2448.
9. Cremona ML, Campetella O, Sanchez DO, Frasch AC. 1999. Enzymically inactive members of the trans-sialidase family from Trypanosoma cruzi display beta-galactose binding activity. Glycobiology. 9: 581 -587.
10. Crisa L, Cirulli V, Ellisman MH, Ishii JK, Elices MJ, Salomon DR. 1996. Cell adhesion and migration are regulated at distinct stages of thymic T cell development: the roles of fibronectin, VLA4, and VLA5. J Exp Med. 184: 215-228.
11. Dalton P, Christian HC, Redman CW, Sargent IL, Boyd CA. 2007. Membrane trafficking of CD98 and its ligand galectin 3 in BeWo cells-implication for placental cell fusion. FEBS J. 274: 2715-2727.
12. Daniels MA, Devine L, Miller JD, Moser JM, Lukacher AE, Altman JD, Kavathas P, Hogquist KA, Jameson SC. 2001. CD8 binding to MHC class I molecules is influenced by T cell maturation and glycosylation. Immunity. 15: 1051-1061.
13. Daniels MA, Hogquist KA, Jameson SC. 2002. Sweet 'n' sour: the impact of differential glycosylation on T cell responses. Nat Immunol. 3: 903-910.
14. de Titto EH, Araujo FG. 1988. Serum neuraminidase activity and hematological alterations in acute human Chagas' disease. Clin Immunol Immunopathol. 46: 157-161.
15. Dube DH, Bertozzi CR. 2003. Metabolic oligosaccharide engineering as a tool for glycobiology. Curr Opin Chem Biol. 7: 616-625.
16. Earl LA, Baum LG. 2008. CD45 glycosylation controls T-cell life and death. Immunol Cell Biol. 86: 608-615.
17. Ferrero-Garcia MA, Trombetta SE, Sanchez DO, Reglero A, Frasch AC, Parodi AJ. 1993. The action of Trypanosoma cruzi trans-sialidase on glycolipids and glycoproteins. Eur J Biochem. 213: 765-771.
18. Hellman U. 2002. Peptide mapping using MALDI-TOFMS. In Silbering J and Ekman R, editors. Mass Spectrometry and Hyphenated Techniques in Neuropeptide Research. New York: John Wiley & Sons, Inc. p. 259-275.
19. Hernandez JD, Baum LG. 2002. Ah, sweet mystery of death! Galectins and control of cell fate. Glycobiology. 12: 127R-136R.
20. Kierszenbaum F, Sztein MB. 1990. Mechanisms underlying immunosuppression induced by Trypanosoma cruzi. Parasitol Today. 6: 261-264.
21. Laughlin ST, Agard NJ, Baskin JM, Carrico IS, Chang PV, Ganguli AS, Hangauer MJ, Lo A, Prescher JA, Bertozzi CR. 2006. Metabolic labeling of glycans with azido sugars for visualization and glycoproteomics. Methods Enzymol. 415: 230-250.
22. Leguizamon MS, Campetella OE, González Cappa SM, Frasch AC. 1994. Mice infected with Trypanosoma cruzi produce antibodies against the enzymatic domain of trans-sialidase that inhibit its activity. Infect Immun. 62: 3441-3446.
23. Leguizamón MS, Mocetti E, Garcia Rivello H, Argibay P, Campetella O. 1999. Trans-sialidase from Trypanosoma cruzi induces apoptosis in cells from the immune system in vivo. J Infect Dis. 180: 1398-1402.
24. Lowe JB. 2001. Glycosylation, immunity, and autoimmunity. Cell. 104: 809-812.
25. MacKinnon AC, Farnworth SL, Hodkinson PS, Henderson NC, Atkinson KM, Leffler H, Nilsson UJ, Haslett C, Forbes SJ, Sethi T. 2008. Regulation of alternative macrophage activation by galectin-3. J Immunol. 180: 2650-2658.
26. Minoprio P, Itohara S, Heusser C, Tonegawa S, Coutinho A. 1989. Immunobiology of murine T cruzi infection: the predominance of parasite-nonspecific responses and the activation of TCRI T cells. Immunol Rev. 112: 183-207.
27. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL. 2001. Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell. 107: 501-512.
28. Moody AM, North SJ, Reinhold B, Van Dyken SJ, Rogers ME, Panico M, Dell A, Morris HR, Marth JD, Reinherz EL. 2003. Sialic acid capping of CD8b core 1-O-glycans controls thymocyte-major histocompatibility complex Class I interaction. J Biol Chem. 278: 7240-7246.
29. Mucci J, Hidalgo A, Mocetti E, Argibay PF, Leguizamón MS, Campetella O. 2002. Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc Natl Acad Sci USA. 99: 3896-3901.
30. Mucci J, Mocetti E, Leguizamon MS, Campetella O. 2005. A sexual dimorphism in intrathymic sialylation survey is revealed by the trans-sialidase from Trypanosoma cruzi. J Immunol. 174: 4545-4550.
31. Mucci J, Risso MG, Leguizamón MS, Frasch AC, Campetella O. 2006. The trans-sialidase from Trypanosoma cruzi triggers apoptosis by target cell sialylation. Cell Microbiol. 8: 1086-1095.
32. Paessens LC, Singh SK, Fernandes RJ, van Kooyk Y. 2008. Vascular cell adhesion molecule-1 (VCAM-1) and intercellular adhesion molecule-1 (ICAM-1) provide co-stimulation in positive selection along with survival of selected thymocytes. Mol Immunol. 45: 42-48.
33. Pereira ME. 1983. A developmentally regulated neuraminidase activity in Trypanosoma cruzi. Science. 219: 1444-1446.
34. Pereira-Chioccola VL, Acosta-Serrano A, Correia de Almeida I, Ferguson MA, Souto-Padron T, Rodrigues MM, Travassos LR, Schenkman S. 2000. 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: 1299-1307.
35. Prescher JA, Dube DH, Bertozzi CR. 2004. Chemical remodelling of cell surfaces in living animals. Nature. 430: 873-877.
36. Risso MG, Garbarino GB, Mocetti E, Campetella O, González Cappa SM, Buscaglia CA, Leguizamon MS. 2004. Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. J Infect Dis. 189: 2250-2259.
37. Risso MG, Pitcovsky TA, Caccuri RL, Campetella O, Leguizamon MS. 2007. Immune system pathogenesis is prevented by the neutralization of the systemic trans-sialidase from Trypanosoma cruzi during severe infections. Parasitology. 134: 503-510.
38. Salomon DR, Mojcik CF, Chang AC, Wadsworth S, Adams DH, Coligan JE, Shevach EM. 1994. Constitutive activation of integrin alpha 4 beta 1 defines a unique stage ofhuman thymocyte development. J Exp Med. 179: 1573-1584.
39. Savino W. 2006. The thymus is a common target organ in infectious diseases. PLoS Pathog. 2: e62.
40. Savino W, Mendes-Da-Cruz DA, Smaniotto S, Silva-Monteiro E, Villa-Verde DM. 2004. Molecular mechanisms governing thymocyte migration: combined role of chemokines and extracellular matrix. J Leukoc Biol. 75: 951-961.
41. Schenkman S, Jiang MS, Hart GW, Nussenzweig V. 1991. A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell. 65: 1117-1125.
42. Schenkman S, Pontes de Carvalho L, Nussenzweig V. 1992. Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. J Exp Med. 175: 567-575.
43. Seales EC, Shaikh FM, Woodard-Grice AV, Aggarwal P, McBrayer AC, Hennessy KM, Bellis SL. 2005. A protein kinase C/Ras/ERK signaling pathway activates myeloid fibronectin receptors by altering beta1 integrin sialylation. J Biol Chem. 280: 37610-37615.
44. Semel AC, Seales EC, Singhal A, Eklund EA, Colley KJ, Bellis SL. 2002. Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem. 277: 32830-32836.
45. Serrano AA, Schenkman S, Yoshida N, Mehlert A, Richardson JM, Ferguson MA. 1995. The lipid structure of the glycosylphosphatidylinositol-an-chored mucin-like sialic acid acceptors of Trypanosoma cruzi changes during parasite differentiation from epimastigotes to infective metacyclic trypomastigote forms. J Biol Chem. 270: 27244-27253.
46. Silva-Monteiro E, Reis Lorenzato L, Kenji Nihei O, Junqueira M, Rabinovich GA, Hsu DK, Liu FT, Savino W, Chammas R, Villa-Verde DM. 2007. Altered expression of galectin-3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanosoma cruzi infection. Am J Pathol. 170: 546-556.
47. Starr TK, Daniels MA, Lucido MM, Jameson SC, Hogquist KA. 2003. Thymocyte sensitivity and supramolecular activation cluster formation are developmentally regulateD: A partial role for sialylation. J Immunol. 171: 4512-4520.
48. Taliaferro WH, Pizzi T. 1955. Connective tissue reactions in normal and immunized mice to a reticulotropic strain of Trypanosoma cruzi. J Infect Dis. 96: 199-226.
49. Todeschini AR, Girard MF, Wieruszeski JM, Nunes MP, DosReis GA, Mendonca-Previato L, Previato JO. 2002. Trans-Sialidase from Trypanosoma cruzi binds host T-lymphocytes in a lectin manner. J Biol Chem. 277: 45962-45968.
50. Todeschini AR, Nunes MP, Pires RS, Lopes MF, Previato JO, Mendonca-Previato L, DosReis GA. 2002. Costimulation of host T lymphocytes by a trypanosomal trans-sialidase: involvement of CD43 signaling. J Immunol. 168: 5192-5198.
51. Tomlinson S, Pontes de Carvalho LC, Vandekerckhove F, Nussenzweig V. 1994. Role of sialic acid in the resistance of Trypanosoma cruzi trypomas- tigotes to complement. J Immunol. 153: 3141-3147.
52. Tribulatti MV, Mucci J, Van Rooijen N, Leguizamon MS, Campetella O. 2005. The trans-sialidase from Trypanosoma cruzi induces thrombocytopenia during acute Chagas' disease by reducing the platelet sialic acid contents. Infect Immun. 73: 201-207.
53. Varki A, Schauer R. 2009. Sialic acids. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW and Etzler ME, editors. Essentials of Glycobiology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p. 199-217.
54. Yu H, Chokhawala H, Karpel R, Wu B, Zhang J, Zhang Y, Jia Q, Chen X. 2005. A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries. J Am Chem Soc. 127: 17618-17619.
55. Zamoyska R. 2007. Why is there so much CD45 on T cells? Immunity. 27: 421-423.
56. Zamoyska R, Basson A, Filby A, Legname G, Lovatt M, Seddon B. 2003. The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol Rev. 191: 107-118.