Genomic analyses, gene expression and antigenic profile of the trans-sialidase superfamily of trypanosoma cruzi reveal an undetected level of complexity

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Freitas, Leandro M ^a   dos Santos, Sara Lopes ^a   Rodrigues Luiz, Gabriela F ^a   Mendes, Tiago A O ^a   Rodrigues, Thiago S ^b   Gazzinelli, Ricardo T ^a   Teixeira, Santuza M R ^a   Fujiwara, Ricardo T ^a   Bartholomeu, Daniella C ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b CENTRO FEDERAL DE EDUCAÇÃO TECNOLÓGICA DE MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; SIALIDASE; GLYCOPROTEIN; PARASITE ANTIGEN; TRANS SIALIDASE; TRANS-SIALIDASE;

3' UNTRANSLATED REGION; ANTIGENICITY; ARTICLE; BACTERIAL CHROMOSOME; CELL ADHESION; CELL INVASION; CHAGAS DISEASE; CHROMOSOMAL LOCALIZATION; CONTROLLED STUDY; CROSS REACTION; GENE; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENOME ANALYSIS; HOST CELL; HOST PATHOGEN INTERACTION; NONHUMAN; PREDICTION; PROTEIN EXPRESSION; PROTEIN MOTIF; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIALIDASE GENE; TRYPANOSOMA CRUZI; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHROMOSOME MAP; ENZYMOLOGY; GENETICS; IMMUNOLOGY; MOLECULAR DYNAMICS; MOLECULAR GENETICS;

MUS; PROTOZOA; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; GENES, PROTOZOAN; GLYCOPROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NEURAMINIDASE; REAL-TIME POLYMERASE CHAIN REACTION; TRYPANOSOMA CRUZI;

EID: 80054790079     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025914     Document Type: Article

References (63)

1. World Health Organization (2002) Control of Chagas Disease. Second report of the WHO Expert Committee. WHO Technical Report Series 905.
2. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
3. Previato JO, Andrade AF, Pessolani MC, 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.
4. 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.
5. Vercelli CA, Hidalgo AM, Hyon SH, Argibay PF, (2005) Trypanosoma cruzi trans-sialidase inhibits human lymphocyte proliferation by nonapoptotic mechanisms: implications in pathogenesis and transplant immunology. Transplant Proc 37: 4594-4597.
6. Frasch AC, (2000) Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today 16: 282-286.
7. Pereira-Chioccola VL, Acosta-Serrano A, Correia de Almeida I, Ferguson MA, Souto-Padron T, et al. (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 (Pt 7): 1299-1307.
8. Schenkman S, Eichinger D, Pereira ME, Nussenzweig V, (1994) Structural and functional properties of Trypanosoma trans-sialidase. Annu Rev Microbiol 48: 499-523.
9. Souza W, Carvalho TM, Barrias ES, (2010) Review on Trypanosoma cruzi: Host Cell Interaction. Int J Cell Biol 2010: 1-18.
10. Tonelli RR, Giordano RJ, Barbu EM, Torrecilhas AC, Kobayashi GS, et al. (2010) Role of the gp85/trans-sialidases in Trypanosoma cruzi tissue tropism: preferential binding of a conserved peptide motif to the vasculature in vivo. PLoS Negl Trop Dis 4: e864.
11. Tzelepis F, de Alencar BC, Penido ML, Claser C, Machado AV, et al. (2008) Infection with Trypanosoma cruzi restricts the repertoire of parasite-specific CD8+ T cells leading to immunodominance. J Immunol 180: 1737-1748.
12. Rubin-de-Celis SS, Uemura H, Yoshida N, 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.
13. Cross GA, Takle GB, (1993) The surface trans-sialidase family of Trypanosoma cruzi. Annu Rev Microbiol 47: 385-411.
14. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
15. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
16. Felsenstein J, (1989) Phylogeny Inference Package (Version 3.2). Cladistics 5: 164-166.
17. Felsenstein J, (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Free program distributed by the authors over the internet from http://evolution.genetics.washington.edu/phylip.html: Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
18. Hartigan JA, Wong MA, (1979) Algorithm AS 136: A k-means clustering algorithm. Journal of the Royal Statistical Society Series C (Applied Statistics) 28: 100-108.
19. R Development Core Team (2011) R: A language and environment for statistical computing, reference index version 2.13.0. (R Foundation for Statistical Computing, Vienna).
20. Weatherly DB, Boehlke C, Tarleton RL, (2009) Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10: 255.
21. Yan T, Yoo D, Berardini TZ, Mueller LA, Weems DC, et al. (2005) PatMatch: a program for finding patterns in peptide and nucleotide sequences. Nucleic Acids Res 33: W262-266.
22. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
23. Fankhauser N, Mäser P, (2005) Identification of GPI anchor attachment signals by a Kohonen self-organizing map. Bioinformatics 21: 1846-1852.
24. Bartholomeu DC, Silva RA, Galvão LM, el-Sayed NM, Donelson JE, et al. (2002) Trypanosoma cruzi: RNA structure and post-transcriptional control of tubulin gene expression. Exp Parasitol 102: 123-133.
25. Larsen JE, Lund O, Nielsen M, (2006) Improved method for predicting linear B-cell epitopes. Immunome Res 2: 2.
26. Frank R, (1992) Spot-synthesis: an easy technique for the position- ally addressable, parallel chemical synthesis on a membrane support. Tetrahedron 48: 9217-9232.
27. Colli W, (1993) Trans-sialidase: a unique enzyme activity discovered in the protozoan Trypanosoma cruzi. FASEB J 7: 1257-1264.
28. Roggentin P, Rothe B, Kaper JB, Galen J, Lawrisuk L, et al. (1989) Conserved sequences in bacterial and viral sialidases. Glycoconj J 6: 349-353.
29. Beucher M, Norris KA, (2008) Sequence diversity of the Trypanosoma cruzi complement regulatory protein family. Infect Immun 76: 750-758.
30. Todeschini AR, Mendonça-Previato L, Previato JO, Varki A, van Halbeek H, (2000) Trans-sialidase from Trypanosoma cruzi catalyzes sialoside hydrolysis with retention of configuration. Glycobiology 10: 213-221.
31. Teixeira SM, Russell DG, Kirchhoff LV, Donelson JE, (1994) A differentially expressed gene family encoding "amastin," a surface protein of Trypanosoma cruzi amastigotes. J Biol Chem 269: 20509-20516.
32. Campos PC, Bartholomeu DC, DaRocha WD, Cerqueira GC, Teixeira SM, (2008) Sequences involved in mRNA processing in Trypanosoma cruzi. Int J Parasitol 38: 1383-1389.
33. Pollevick GD, Affranchino JL, Frasch AC, Sánchez DO, (1991) The complete sequence of a shed acute-phase antigen of Trypanosoma cruzi. Mol Biochem Parasitol 47: 247-250.
34. Burns JM, Shreffler WG, Rosman DE, Sleath PR, March CJ, et al. (1992) Identification and synthesis of a major conserved antigenic epitope of Trypanosoma cruzi. Proc Natl Acad Sci U S A 89: 1239-1243.
35. Giordano R, Chammas R, Veiga SS, Colli W, Alves MJ, (1994) Trypanosoma cruzi binds to laminin in a carbohydrate-independent way. Braz J Med Biol Res 27: 2315-2318.
36. Ouaissi A, Cornette J, Taibi A, Velge P, Capron A, (1988) Major surface immunogens of Trypanosoma cruzi trypomastigotes. Mem Inst Oswaldo Cruz 83 (Suppl 1): 502.
37. Velge P, Ouaissi MA, Cornette J, Afchain D, Capron A, (1988) Identification and isolation of Trypanosoma cruzi trypomastigote collagen-binding proteins: possible role in cell-parasite interaction. Parasitology 97 (Pt 2): 255-268.
38. Santana JM, Grellier P, Schrével J, Teixeira AR, (1997) A Trypanosoma cruzi secreted 80 kDa proteinase with specificity for human collagen types I and IV. Biochem J 325 (Pt 1): 129-137.
39. Magdesian MH, Giordano R, Ulrich H, Juliano MA, Juliano L, et al. (2001) Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J Biol Chem 276: 19382-19389.
40. Norris KA, Bradt B, Cooper NR, So M, (1991) Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the human complement regulatory protein, decay-accelerating factor. J Immunol 147: 2240-2247.
41. Van Voorhis WC, Eisen H, (1989) Fl-160. A surface antigen of Trypanosoma cruzi that mimics mammalian nervous tissue. J Exp Med 169: 641-652.
42. Engstler M, Reuter G, Schauer R, (1992) Purification and characterization of a novel sialidase found in procyclic culture forms of Trypanosoma brucei. Mol Biochem Parasitol 54: 21-30.
43. Grisard EC, Stoco PH, Wagner G, Sincero TC, Rotava G, et al. (2010) Transcriptomic analyses of the avirulent protozoan parasite Trypanosoma rangeli. Mol Biochem Parasitol 174: 18-25.
44. Buschiazzo A, Campetella O, Frasch AC, (1997) Trypanosoma rangeli sialidase: cloning, expression and similarity to T. cruzi trans-sialidase. Glycobiology 7: 1167-1173.
45. Briones MR, Egima CM, Eichinger D, Schenkman S, (1995) Trans-sialidase genes expressed in mammalian forms of Trypanosoma cruzi evolved from ancestor genes expressed in insect forms of the parasite. J Mol Evol 41: 120-131.
46. Magdesian MH, Tonelli RR, Fessel MR, Silveira MS, Schumacher RI, et al. (2007) A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp Cell Res 313: 210-218.
47. Tonelli RR, Torrecilhas AC, Jacysyn JF, Juliano MA, Colli W, et al. (2011) In vivo infection by Trypanosoma cruzi: the conserved FLY domain of the gp85/trans-sialidase family potentiates host infection. Parasitology 138: 481-492.
48. Gaskell A, Crennell S, Taylor G, (1995) The three domains of a bacterial sialidase: a beta-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure 3: 1197-1205.
49. Cremona ML, Campetella O, Sánchez DO, Frasch AC, (1999) Enzymically inactive members of the trans-sialidase family from Trypanosoma cruzi display beta-galactose binding activity. Glycobiology 9: 581-587.
50. Todeschini AR, Dias WB, Girard MF, Wieruszeski JM, Mendonça-Previato L, et al. (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.
51. Copley RR, Russell RB, Ponting CP, (2001) Sialidase-like Asp-boxes: sequence-similar structures within different protein folds. Protein Sci 10: 285-292.
52. Oppezzo P, Obal G, Baraibar MA, Pritsch O, Alzari PM, et al. (2011) Crystal structure of an enzymatically inactive trans-sialidase-like lectin from Trypanosoma cruzi: The carbohydrate binding mechanism involves residual sialidase activity. Biochim Biophys Acta 1814: 1154-1161.
53. Scherf A, Lopez-Rubio JJ, Riviere L, (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62: 445-470.
54. Kim D, Chiurillo MA, El-Sayed N, Jones K, Santos MR, et al. (2005) Telomere and subtelomere of Trypanosoma cruzi chromosomes are enriched in (pseudo)genes of retrotransposon hot spot and trans-sialidase-like gene families: the origins of T. cruzi telomeres. Gene 346: 153-161.
55. Horn D, Barry JD, (2005) The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosome Res 13: 525-533.
56. Chiurillo MA, Peralta A, Ramírez JL, (2002) Comparative study of Trypanosoma rangeli and Trypanosoma cruzi telomeres. Mol Biochem Parasitol 120: 305-308.
57. Cano MI, (2001) Telomere biology of trypanosomatids: more questions than answers. Trends Parasitol 17: 425-429.
58. Scherf A, Figueiredo LM, Freitas-Junior LH, (2001) Plasmodium telomeres: a pathogen's perspective. Curr Opin Microbiol 4: 409-414.
59. Atwood JA, Weatherly DB, Minning TA, Bundy B, Cavola C, et al. (2005) The Trypanosoma cruzi proteome. Science 309: 473-476.
60. Azuaje FJ, Ramirez JL, Da Silveira JF, (2007) In silico, biologically-inspired modelling of genomic variation generation in surface proteins of Trypanosoma cruzi. Kinetoplastid Biology and Disease 6: 6-17.
61. Azuaje F, Ramirez JL, Da Silveira JF, (2007) An exploration of the genetic robustness landscape of surface protein families in the human protozoan parasite Trypanosoma cruzi. IEEE Transactions on Nanobioscience 6: 223-228.
62. Pitcovsky TA, Buscaglia CA, Mucci J, 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.
63. Ratier L, Urrutia M, Paris G, Zarebski L, Frasch AC, et al. (2008) Relevance of the diversity among members of the Trypanosoma cruzi trans-sialidase family analyzed with camelids single-domain antibodies. PLoS One 3: e3524.