Molecular diversity of the Trypanosoma cruzi TcSMUG family of mucin genes and proteins

Biochemical Journal

Volumn 438, Issue 2, 2011, Pages 303-313

  Urban, Ivana ^a   Boiani Santurio, Lucía ^a   Chidichimo, Agustina ^a   Yu, Hai ^b   Chen, Xi ^b   Mucci, Juan ^a   Agüero, Fernán ^a   Buscaglia, Carlos A ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mucin; Multigene family; Quantitative PCR; TcSMUG; Trypanosoma cruzi

Indexed keywords

MUCIN; PROTEIN SMUG L; PROTOZOAL PROTEIN; SIALIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENETIC TRANSFECTION; MICROBIAL DIVERSITY; NONHUMAN; ORGANISMS BY LIFE CYCLE STAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; DNA COPY NUMBER VARIATIONS; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; GENETIC VARIATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUCINS; MULTIGENE FAMILY; N-ACETYLNEURAMINIC ACID; PROTOZOAN PROTEINS; RNA, MESSENGER; TRANSFECTION; TRYPANOSOMA CRUZI;

HEXAPODA; PROTOZOA; TRYPANOSOMA CRUZI;

EID: 80051677176     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110683     Document Type: Article

References (47)

1. Reithinger, R., Tarleton, R. L., Urbina, J. A., Kitron, U. and Gurtler, R. E. (2009) Eliminating Chagas disease: challenges and a roadmap. BMJ 338, b1283
2. Brisse, S., Barnabe, C. and Tibayrenc, M. (2000) Identification of six Trypanosoma cruzi phylogenetic lineages by random amplified polymorphic DNA and multilocus enzyme electrophoresis. Int. J. Parasitol. 30, 35-44 (Pubitemid 30089720)
3. Zingales, B., Andrade, S., Briones, M. R., Campbell, D., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A. M., Machado, C. R. et al. (2009) A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem. Inst. Oswaldo Cruz 104, 1051-1054
4. Gaunt, M. W., Yeo, M., Frame, I., Stothard, J., Carrasco, H., Taylor, M., Mena, S., Veazey, P., Miles, G. A., Acosta, N. et al. (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421, 936-939 (Pubitemid 36288023)
5. Westenberger, S. J., Barnabe, C., Campbell, D. and Sturm, N. R. (2005) Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171, 527-543
6. de Freitas, J. M., Augusto-Pinto, L., Pimenta, J., Bastos-Rodrigues, L., Goncalves, V. F., Teixeira, S. M., Chiari, E., Junqueira, A., Fernandes, O., Macedo, A. M. et al. (2006) Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathog. 2, e24
7. Buscaglia, C. A. and Di Noia, J. M. (2003) Trypanosoma cruzi clonal diversity and the epidemiology of Chagas' disease. Microbes Infect. 5, 419-427 (Pubitemid 36549184)
8. Schenkman, S., Ferguson, M. A., Heise, N., 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, 293-303 (Pubitemid 223039687)
9. 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
10. Yoshida, N. (2006) Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An. Acad. Bras. Cienc. 78, 87-111
11. Almeida, I. C. and Gazzinelli, R. T. (2001) Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. J. Leukoc. Biol. 70, 467-477 (Pubitemid 32954758)
12. Talvani, A., Coutinho, S., Barcelos, S. and Teixeira, M. M. (2009) Cyclic AMP decreases the production of NO and CCL2 by macrophages stimulated with Trypanosoma cruzi GPI-mucins. Parasitol. Res. 104, 1141-1148
13. 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
14. Cuevas, I. C., Cazzulo, J. J. and Sanchez, D. (2003) gp63 homologues in Trypanosoma cruzi: surface antigens with metalloprotease activity and a possible role in host cell infection. Infect. Immun. 71, 5739-5749 (Pubitemid 37205627)
15. Bartholomeu, D. C., Cerqueira, G., Leao, A., daRocha, W., Pais, F., Macedo, C., Djikeng, A., Teixeira, S. M. and El-Sayed, N. M. (2009) Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucl. Acids Res. 37, 3407-3417
16. Previato, J. O., Wait, R., Jones, C., DosReis, G. A., Todeschini, A., Heise, N. and Previato, L. M. (2004) Glycoinositolphospholipid from Trypanosoma cruzi: structure, biosynthesis and immunobiology. Adv. Parasitol. 56, 1-41
17. de Lederkremer, R. M. and Agusti, R. (2009) Glycobiology of Trypanosoma cruzi. Adv. Carbohydr. Chem. Biochem. 62, 311-366
18. Di Noia, J. M., D'Orso, I., Sanchez, D. and Frasch, A. C. (2000) AU-rich elements in the 3′-untranslated region of a new mucin-type gene family of Trypanosoma cruzi confers mRNA instability and modulates translation efficiency. J. Biol. Chem. 275, 10218-10227 (Pubitemid 30202078)
19. Campo, V., Di Noia, J. M., Buscaglia, C. A., Aguero, F., Sanchez, D. and Frasch, A. C. (2004) Differential accumulation of mutations localized in particular domains of the mucin genes expressed in the vertebrate host stage of Trypanosoma cruzi. Mol. Biochem. Parasitol. 133, 81-91 (Pubitemid 37510311)
20. Buscaglia, C. A., Campo, V. A., Di Noia, J. M., Torrecilhas, A., De Marchi, C. R., Ferguson, M. A., Frasch, A. C. and Almeida, I. C. (2004) The surface coat of the mammal-dwelling infective trypomastigote stage of Trypanosoma cruzi is formed by highly diverse immunogenic mucins. J. Biol. Chem. 279, 15860-15869 (Pubitemid 38509273)
21. Campo, V. A., Buscaglia, C. A., Di Noia, J. M. and Frasch, A. C. (2006) Immunocharacterization of the mucin-type proteins from the intracellular stage of Trypanosoma cruzi. Microbes Infect. 8, 401-409 (Pubitemid 43214602)
22. Nakayasu, E. S., Yashunsky, D., Nohara, L., Torrecilhas, A., Nikolaev, A. and Almeida, I. C. (2009) GPIomics: global analysis of glycosylphosphatidylinositol-anchored molecules of Trypanosoma cruzi. Mol. Syst. Biol. 5, 261
23. Paba, J., Santana, J., Teixeira, A., Fontes, W., Sousa, M. and Ricart, C. A. (2004) Proteomic analysis of the human pathogen Trypanosoma cruzi. Proteomics 4, 1052-1059 (Pubitemid 38445963)
24. Atwood, 3rd, J. A., Weatherly, D., Minning, T. A., Bundy, B., Cavola, C., Opperdoes, F. R., Orlando, R. and Tarleton, R. L. (2005) The Trypanosoma cruzi proteome. Science 309, 473-476
25. Ferella, M., Nilsson, D., Darban, H., Rodrigues, C., Bontempi, E. J., Docampo, R. and Andersson, B. (2008) Proteomics in Trypanosoma cruzi - localization of novel proteins to various organelles. Proteomics 8, 2735-2749 (Pubitemid 351988577)
26. Notredame, C., Higgins, D. and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217
27. Felsenstein, J. (1993) PHYLIP version 3.
28. Han, M. and Zmasek, C. (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10, 356
29. Bustin, S., Benes, V., Garson, J., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M., Shipley, G. et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622
30. Buscaglia, C. A., Penesetti, D., Tao, M. and Nussenzweig, V. (2006) Characterization of an aldolase-binding site in the Wiskott-Aldrich syndrome protein. J. Biol. Chem. 281, 1324-1331
31. Parussini, F., Garcia, M., Mucci, J., Aguero, F., Sanchez, D., Hellman, U., Aslund, L. and Cazzulo, J. J. (2003) Characterization of a lysosomal serine carboxypeptidase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 131, 11-23 (Pubitemid 37101175)
32. Barderi, P., Campetella, O., Frasch, A. C., Santome, J., Hellman, U., Pettersson, U. and Cazzulo, J. J. (1998) The NADP+ -linked glutamate dehydrogenase from Trypanosoma cruzi: sequence, genomic organization and expression. Biochem. J. 330, 951-958
33. Martinez-Calvillo, S., Lopez, I. and Hernandez, R. (1997) pRIBOTEX expression vector: a pTEX derivative for a rapid selection of Trypanosoma cruzi transfectants. Gene 199, 71-76 (Pubitemid 27448203)
34. Pollevick, G. D., Di Noia, J. M., Salto, M. L., Lima, C., Leguizamon, M. S., de Lederkremer, R. M. and Frasch, A. C. (2000) Trypanosoma cruzi surface mucins with exposed variant epitopes. J. Biol. Chem. 275, 27671-27680
35. Buscaglia, C. A., Pollevick, G. D., Veloso, C., Lorca, M., Frasch, A. C. and Sanchez, D. O. (1996) A putative pyruvate dehydrogenase alpha subunit gene from Trypanosoma cruzi. Biochim. Biophys. Acta 1309, 53-57 (Pubitemid 26382349)
36. Cordero, E. M., Nakayasu, E. S., Gentil, L., Yoshida, N., Almeida, I. C. and da Silveira, J. F. (2009) Proteomic analysis of detergent-solubilized membrane proteins from insect-developmental forms of Trypanosoma cruzi. J. Proteome Res. 8, 3642-3652
37. Almeida, I. C., Ferguson, M. A., Schenkman, S. and Travassos, L. R. (1994) Lytic anti-α-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
38. Buscaglia, C. A., Alfonso, J., Campetella, O. and Frasch, A. C. (1999) Tandem amino acid repeats from Trypanosoma cruzi shed antigens increase the half-life of proteins in blood. Blood 93, 2025-2032 (Pubitemid 29128505)
39. Yu, H., Chokhawala, H., Karpel, R., Yu, H., Wu, B., Zhang, J., Zhang, Y., Jia, Q. and Chen, X. (2005) A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries. J. Am. Chem. Soc. 127, 17618-17619 (Pubitemid 43003372)
40. Muia, R. P., Yu, H., Prescher, J., 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
41. Arner, E., Kindlund, E., Nilsson, D., Farzana, F., Ferella, M., Tammi, M. and Andersson, B. (2007) Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants. BMC Genomics 8, 391
42. Hanke, J., Sanchez, D., Henriksson, J., Aslund, L., Pettersson, U., Frasch, A. C. and Hoheisel, J. D. (1996) Mapping the Trypanosoma cruzi genome: analyses of representative cosmid libraries. BioTechniques 21, 690-693
43. Di Noia, J. M., Buscaglia, C. A., De Marchi, C. R., Almeida, I. C. and Frasch, A. C. (2002) A Trypanosoma cruzi small surface molecule provides the first immunological evidence that Chagas' disease is due to a single parasite lineage. J. Exp. Med. 195, 401-413 (Pubitemid 34461294)
44. Previato, J. O., Sola-Penna, M., Agrellos, O., Jones, C., Oeltmann, T., Travassos, L. R. and Mendonca-Previato, L. (1998) Biosynthesis of O-N-acetylglucosamine-linked glycans in Trypanosoma cruzi. J. Biol. Chem. 273, 14982-14988
45. Macrae, J. I., Acosta-Serrano, A., Morrice, N., Mehlert, A. and Ferguson, M. A. (2005) Structural characterization of NETNES, a novel glycoconjugate in Trypanosoma cruzi epimastigotes. J. Biol. Chem. 280, 12201-12211
46. Risso, M. G., Garbarino, G. B., Mocetti, E., Campetella, O., Gonzalez Cappa, S. M., Buscaglia, C. A. and Leguizamon, M. S. (2004) Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. J. Infect. Dis. 189, 2250-2259 (Pubitemid 38757198)
47. Nogueira, N., Gonzalez, M., Gomes, J., de Souza, W., Garcia, E. S., Azambuja, P., Nohara, L., Almeida, I. C., Zingales, B. and Colli, W. (2007) Trypanosoma cruzi: involvement of glycoinositolphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Exp. Parasitol. 116, 120-128 (Pubitemid 46602253)