T rypanosoma cruzi trans-sialidase as a multifunctional enzyme in chagas' disease

Cellular Microbiology

Volumn 14, Issue 10, 2012, Pages 1522-1530

  Dc Rubin, Sergio S C ^a,b   Schenkman, Sergio ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b CNIB   (Bolivia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INOSITOL; SIALIDASE; TRANS SIALIDASE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL INVASION; CELL VACUOLE; CHAGAS DISEASE; COXIELLA BURNETII; CYTOSOL; DRUG TARGETING; ENZYME SUBSTRATE COMPLEX; HOST CELL; HOST PARASITE INTERACTION; IMMUNE SYSTEM; INFECTION CONTROL; KINETICS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIALYLATION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; X RAY DIFFRACTION;

CHAGAS DISEASE; GLYCOPROTEINS; HUMANS; NEURAMINIDASE; PROTEIN CONFORMATION; TRYPANOSOMA CRUZI; VIRULENCE FACTORS;

TRYPANOSOMA CRUZI;

EID: 84866314328     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01831.x     Document Type: Article

References (77)

1. Abuin, G., Freitas-Junior, L.H.G., Colli, W., Alves, M.J., and Schenkman, S. (1999) Expression of trans-sialidase and 85kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J Biol Chem 274: 13041-13047.
2. Acosta-Serrano, A., Almeida, I.C., Freitas-Junior, L.H., Yoshida, N., and Schenkman, S. (2001) The mucin-like glycoprotein super-family ofTrypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol 114: 143-150.
3. Agusti, R., Paris, G., Ratier, L., Frasch, A.C., and de Lederkremer, R.M. (2004) Lactose derivatives are inhibitors of Trypanosoma cruzi trans-sialidase activity toward conventional substrates in vitro and in vivo Glycobiology 14: 659-670.
4. Albertti, L.A., Macedo, A.M., Chiari, E., Andrews, N.W., and Andrade, L.O. (2010) Role of host lysosomal associated membrane protein (LAMP) in Trypanosoma cruzi invasion and intracellular development. Microbes Infect 12: 784-789.
5. Alvarez, P., Leguizamon, M.S., Buscaglia, C.A., Pitcovsky, T.A., and Campetella, O. (2001) Multiple overlapping epitopes in the repetitive unit of the shed acute-phase antigen from Trypanosoma cruzi enhance its immunogenic properties. Infect Immun 69: 7946-7949.
6. Alves, C.R., Albuquerque-Cunha, J.M., Mello, C.B., Garcia, E.S., Nogueira, N.F., Bourguingnon, S.C., etal. (2007) Trypanosoma cruzi: attachment to perimicrovillar membrane glycoproteins of Rhodnius prolixus Exp Parasitol 116: 44-52.
7. Andrade, L.O., and Andrews, N.W. (2005) The Trypanosoma cruzi-host-cell interplay: location, invasion, retention. Nat Rev Microbiol 3: 819-823.
8. Andreoli, W.K., Taniwaki, N.N., and Mortara, R.A. (2006) Survival of Trypanosoma cruzi metacyclic trypomastigotes within Coxiella burnetii vacuoles: differentiation and replication within an acidic milieu. Microbes Infect 8: 172-182.
9. Arioka, S., Sakagami, M., Uematsu, R., Yamaguchi, H., Togame, H., Takemoto, H., etal. (2010) Potent inhibitor scaffold against Trypanosoma cruzi trans-sialidase. Bioorg Med Chem 18: 1633-1640.
10. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B.P., Carrington, M., etal. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acid Res 38: D457-D462.
11. Atwood, J.A., III, Weatherly, D.B., Minning, T.A., Bundy, B., Cavola, C., Opperdoes, F.R., etal. (2005) The Trypanosoma cruzi proteome. Science 309: 473-476.
12. Briones, M.R.S., Egima, C.M., and Schenkman, S. (1995) Trypanosoma cruzi trans-sialidase gene lacking C-terminal repeats and expressed in epimastigote forms. Mol Biochem Parasitol 70: 9-17.
13. Burleigh, B.A. (2005) Host cell signaling and Trypanosoma cruzi invasion: do all roads lead to lysosomes? Sci STKE 2005: e36.
14. Burleigh, B.A., and Andrews, N.W. (1995) The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Ann Rev Microbiol 49: 175-200.
15. Buscaglia, C.A., Alfonso, J., Campetella, O., and Frasch, A.C. (1999) Tandem amino acid repeats rrom Trypanosoma cruzi shed antigens increase the half-life of proteins in blood. Blood 93: 2025-2032.
16. Buscaglia, C.A., Campo, V.A., Frasch, A.C., and Di Noia, J.M. (2006) Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol 4: 229-236.
17. Buschiazzo, A., Amaya, M.F., Cremona, M.L., Frasch, A.C., and Alzari, P.M. (2002) The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol Cell 10: 757-768.
18. Buschiazzo, A., Muia, R., Larrieux, N., Pitcovsky, T., Mucci, J., and Campetella, O. (2012) Trypanosoma cruzi trans-sialidase in complex with a neutralizing antibody: structure/function studies towards the rational design of inhibitors. PLoS Pathog 8: e1002474.
19. Carvalho, S.T., Sola-Penna, M., Oliveira, I.A., Pita, S., Goncalves, A.S., Neves, B.C., etal. (2010) A new class of mechanism-based inhibitors for Trypanosoma cruzi trans-sialidase and their influence on parasite virulence. Glycobiology 20: 1034-1045.
20. Chioccola, V.L.P., Acosta-Serrano, A., Almeida, I.C., Ferguson, M.A.J., Souto-Padron, T., Rodrigues, M.M., etal. (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.
21. Chuenkova, M.V., and Pereira, M.A. (2003) PDNF, a human parasite-derived mimic of neurotrophic factors, prevents caspase activation, free radical formation, and death of dopaminergic cells exposed to the Parkinsonism-inducing neurotoxin MPP+. Brain Res Mol Brain Res 119: 50-61.
22. Chuenkova, M.V., and PereiraPerrin, M. (2005) A synthetic peptide modeled on PDNF, Chagas' disease parasite neurotrophic factor, promotes survival and differentiation of neuronal cells through TrkA receptor. Biochemistry 44: 15685-15694.
23. Chuenkova, M.V., and Pereiraperrin, M. (2006) Enhancement of tyrosine hydroxylase expression and activity by Trypanosoma cruzi parasite-derived neurotrophic factor. Brain Res 1099: 167-175.
24. Chuenkova, M.V., and PereiraPerrin, M. (2009) Trypanosoma cruzi targets Akt in host cells as an intracellular antiapoptotic strategy. Sci Signal 2: ra74.
25. Chuenkova, M.V., and Pereiraperrin, M. (2010) Trypanosoma cruzi-derived neurotrophic factor: role in neural repair and neuroprotection. J Neuroparasitology 1: 55-60.
26. Chuenkova, M.V., and Pereiraperrin, M. (2011) Neurodegeneration and neuroregeneration in chagas disease. Adv Parasitol 76: 195-233.
27. DaRocha, W.D., Otsu, K., Teixeira, S.M., and Donelson, J.E. (2004) Tests of cytoplasmic RNA interference (RNAi) and construction of a tetracycline-inducible T7 promoter system in Trypanosoma cruzi Mol Biochem Parasitol 133: 175-186.
28. Dias, W.B., Fajardo, F.D., Graca-Souza, A.V., Freire-de-Lima, L., Vieira, F., Girard, M.F., etal. (2008) Endothelial cell signalling induced by trans-sialidase from Trypanosoma cruzi Cell Microbiol 10: 88-99.
29. Egima, C.M., Briones, M.R.S., Freitas-Junior, L.H.G., Schenkman, R.P.F., Uemura, H., and Schenkman, S. (1996) Organization of trans-sialidase genes in Trypanosoma cruzi Mol Biochem Parasitol 77: 115-125.
30. El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., etal. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
31. Erdmann, H., Steeg, C., Koch-Nolte, F., Fleischer, B., and Jacobs, T. (2009) Sialylated ligands on pathogenic Trypanosoma cruzi interact with Siglec-E (sialic acid-binding Ig-like lectin-E). Cell Microbiol 11: 1600-1611.
32. Frasch, A.C. (2000) Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi Parasitol Today 16: 282-286.
33. Freire-de-Lima, L., Alisson-Silva, F., Carvalho, S.T., Takiya, C.M., Rodrigues, M.M., DosReis, G.A., etal. (2010) Trypanosoma cruzi subverts host cell sialylation and may compromise antigen-specific CD8+ T cell responses. J Biol Chem 285: 13388-13396.
34. Freitas, L.M., dos Santos, S.L., Rodrigues-Luiz, G.F., Mendes, T.A., Rodrigues, T.S., Gazzinelli, R.T., etal. (2011) Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of Trypanosoma cruzi reveal an undetected level of complexity. PLoS ONE 6: e25914.
35. Frevert, U., Schenkman, S., and Nussenzweig, V. (1992) Stage-specific expression and intracellular shedding of the cell surface trans-sialidase of Trypanosoma cruzi Infect Immun 60: 2349-2360.
36. Gao, W., and Pereira, M.A. (2001) Trypanosoma cruzi trans-sialidase potentiates T cell activation through antigen-presenting cells: role of IL-6 and Bruton's tyrosine kinase. Eur J Immunol 31: 1503-1512.
37. Gao, W., and Pereira, M.A. (2002) Interleukin-6 is required for parasite specific response and host resistance to Trypanosoma cruzi Int J Parasitol 32: 167-170.
38. Gao, W., Wortis, H.H., and Pereira, M.A. (2002) The Trypanosoma cruzi trans-sialidase is a T cell-independent B cell mitogen and an inducer of non-specific Ig secretion. Int Immunol 14: 299-308.
39. Garcia, E.S., and Azambuja, P. (1991) Development and interactions of Trypanosoma cruzi within the insect vector. Parasitol Today 7: 240-244.
40. Henrissat, B., and Bairoch, A. (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316: 695-696.
41. Kornfeld, S., and Mellman, I. (1989) The biogenesis of lysosomes. Annu Rev Cell Biol 5: 483-525.
42. Lieke, T., Grobe, D., Blanchard, V., Grunow, D., Tauber, R., Zimmermann-Kordmann, M., etal. (2011) Invasion of Trypanosoma cruzi into host cells is impaired by N-propionylmannosamine and other N-acylmannosamines. Glycoconj J 28: 31-37.
43. Lu, B., Alroy, J., Luquetti, A.O., and PereiraPerrin, M. (2008) Human autoantibodies specific for neurotrophin receptors TrkA, TrkB, and TrkC protect against lethal Trypanosoma cruzi infection in mice. Am J Pathol 173: 1406-1414.
44. Martin, D., and Tarleton, R. (2004) Generation, specificity, and function of CD8+ T cells in Trypanosoma cruzi infection. Immun Rev 201: 304-317.
45. de Melo-Jorge, M., and PereiraPerrin, M. (2007) The Chagas' disease parasite Trypanosoma cruzi exploits nerve growth factor receptor TrkA to infect mammalian hosts. Cell Host Microbe 1: 251-261.
46. Mucci, J., Risso, M.G., Leguizamon, M.S., Frasch, A.C., and Campetella, O. (2006) The trans-sialidase from Trypanosoma cruzi triggers apoptosis by target cell sialylation. Cell Microbiol 8: 1086-1095.
47. Muia, R.P., Yu, H., Prescher, J.A., Hellman, U., Chen, X., Bertozzi, C.R., and Campetella, O. (2010) Identification of glycoproteins targeted by Trypanosoma cruzi trans-sialidase, a virulence factor that disturbs lymphocyte glycosylation. Glycobiology 20: 833-842.
48. Parodi, A.J., Pollevick, G.D., Mautner, M., Buschiazzo, A., Sanchez, D.O., and Frasch, A.C.C. (1992) Identification of the gene(s) coding for the trans-sialidase of Trypanosoma cruzi EMBO J 11: 1705-1710.
49. Pereira, M.E. (1983) A developmentally regulated neuraminidase activity in Trypanosoma cruzi Science 219: 1444-1446.
50. Pereira, M.E.A., Loures, M.A., Villalta, F., and Andrade, A.F.B. (1980) Lectin receptors as markers for Trypanosoma cruzi developmental stages and a study of the interaction of wheat germ agglutinin with sialic acid residues on epimastigote cells. J Exp Med 152: 1375-1382.
51. Pereira-Chioccola, V.L., Schenkman, S., and Kloetzel, J. (1994) Sera from chronic Chagasic patients and animals infected with Trypanosoma cruzi inhibit trans-sialidase by recognizing its catalytic domain. Infect Immun 62: 2973-2978.
52. Pitcovsky, T.A., Buscaglia, C.A., Mucci, J., and Campetella, O. (2002) A functional network of intramolecular cross-reacting epitopes delays the elicitation of neutralizing antibodies to Trypanosoma cruzi trans-sialidase. J Infect Dis 186: 397-404.
53. Pollevick, G.D., Affranchino, J.L., Frasch, A.C.C., and Sanchez, D.O. (1991) The complete sequence of a shed acute-phase antigen of Trypanosoma cruzi Mol Biochem Parasitol 47: 247-250.
54. Previato, J.O., Andrade, A.F., Pessolani, M.C., and Mendonça-Previato, L. (1985) Incorporation of sialic acid into Trypanosoma cruzi macromolecules. A proposal for a new metabolic route. Mol Biochem Parasitol 16: 85-96.
55. Ribeirão, M., Pereira-Chioccola, V.L., Renia, L., Augusto Fragata Filho, A., Schenkman, S., and Rodrigues, M.M. (2000) Chagasic patients develop a type 1 immune response to Trypanosoma cruzi trans-sialidase. Parasite Immunol 22: 49-53.
56. Risso, M.G., Pitcovsky, T.A., Caccuri, R.L., Campetella, O., and Leguizamon, M.S. (2007) Immune system pathogenesis is prevented by the neutralization of the systemic trans-sialidase from Trypanosoma cruzi during severe infections. Parasitology 134: 503-510.
57. Rodrigues, M.M., Ribeirão, M., Pereira-Chioccola, V.L., Renia, L., and Costa, F. (1999) Predominance of CD4 Th1 and CD8 TC1 cells revealed by characterization of the cellular immune response generated by immunization with a DNA vaccine containing a Trypanosoma cruzi gene. Infect Immun 67: 3855-3863.
58. Rosenberg, C.S., Martin, D.L., and Tarleton, R.L. (2010) CD8+ T cells specific for immunodominant trans-sialidase epitopes contribute to control of Trypanosoma cruzi infection but are not required for resistance. J Immunol 185: 560-568.
59. Rubin-de-Celis, S.S., Uemura, H., Yoshida, N., and Schenkman, S. (2006) Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell Microbiol 8: 1888-1898.
60. Saavedra, E., Herrera, M., Gao, W., Uemura, H., and Pereira, M.A. (1999) The Trypanosoma cruzi trans-sialidase, through its COOH-terminal tandem repeat, upregulates interleukin 6 secretion in normal human intestinal microvascular endothelial cells and peripheral blood mononuclear cells. J Exp Med 190: 1825-1836.
61. Sartor, P.A., Cardinal, M.V., Orozco, M.M., Gurtler, R.E., and Leguizamon, M.S. (2011) Trans-sialidase neutralizing antibody detection in Trypanosoma cruzi-infected domestic reservoirs. Clin Vaccine Immunol 18: 984-989.
62. Schauer, R., and Kamerling, J.P. (2011) The chemistry and biology of trypanosomal trans-sialidases: virulence factors in Chagas disease and sleeping sickness. Chembiochem 2246: 2246-2764.
63. Schauer, R., Reuter, G., Muhlpfordt, H., Andrade, A.F., and Pereira, M.E. (1983) The occurrence of N-acetyl- and N-glycoloylneuraminic acid in Trypanosoma cruzi Hoppe Seylers Z Physiol Chem 364: 1053-1057.
64. Schenkman, S., Man-Shiow, J., Hart, G.W., and 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.
65. Schenkman, S., Pontes de Carvalho, L., and Nussenzweig, V. (1992) Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. J Exp Med 175: 567-575.
66. Schenkman, S., Ferguson, M.A.J., Heise, N., Cardoso de Almeida, M.L., Mortara, R.A., and Yoshida, N. (1993) 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: 293-304.
67. Schenkman, S., Eichinger, D., Pereira, M.E.A., and Nussenzweig, V. (1994a) Structural and functional properties of Trypanosoma cruzi trans-sialidase. Ann Rev Microbiol 48: 499-523.
68. Schenkman, S., Chaves, L.B., Pontes de Carvalho, L., and Eichinger, D. (1994b) A proteolytic fragment of Trypanosoma cruzi trans-sialidase lacking the carboxy-terminal domain is active, monomeric and generates antibodies that inhibit enzymatic activity. J Biol Chem 269: 7970-7975.
69. Todeschini, A.R., Nunes, M.P., Pires, R.S., Lopes, M.F., Previato, J.O., Mendonca-Previato, L., and DosReis, G.A. (2002) Costimulation of host T lymphocytes by a trypanosomal trans-sialidase: involvement of CD43 signaling. J Immunol 168: 5192-5198.
70. Todeschini, A.R., Dias, W.B., Girard, M.F., Wieruszeski, J.M., Mendonca-Previato, L., and Previato, J.O. (2004) Enzymatically inactive trans-sialidase from Trypanosoma cruzi binds sialyl and beta-galactopyranosyl residues in a sequential ordered mechanism. J Biol Chem 279: 5323-5328.
71. Tomlinson, S., Pontes de Carvalho, L.C., Vandekerckhove, F., and Nussenzweig, V. (1994) Role of sialic acid in the resistance of Trypanosoma cruzi trypomastigotes to complement. J Immunol 153: 3141-3147.
72. Tribulatti, M.V., Mucci, J., Van Rooijen, N., Leguizamon, M.S., and 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.
73. Uemura, H., Schenkman, S., Nussenzweig, V., and Eichinger, D. (1992) Only some members of a gene family in Trypanosoma cruzi encode proteins which express both trans-sialidase and neuraminidase. EMBO J 11: 3837-3844.
74. Vercelli, C.A., Hidalgo, A.M., Hyon, S.H., and Argibay, P.F. (2005) Trypanosoma cruzi trans-sialidase inhibits human lymphocyte proliferation by nonapoptotic mechanisms: implications in pathogenesis and transplant immunology. Transplant Proc 37: 4594-4597.
75. Weinkauf, C., Salvador, R., and Pereiraperrin, M. (2011) Neurotrophin receptor TrkC is an entry receptor for Trypanosoma cruzi in neural, glial and epithelial cells. Infect Immun 79: 4081-4087.
76. Yoshida, N., and Cortez, M. (2008) Trypanosoma cruzi: parasite and host cell signaling during the invasion process. Subcell Biochem 47: 82-91.
77. Zingales, B., Carniol, C., Lederkremer, R.M., and Colli, W. (1987) Direct sialic acid transfer from a protein donor to glycolipids of trypomastigote forms of Trypanosoma cruzi Mol Biochem Parasitol 26: 135-144.