Multigene families in Trypanosoma cruzi and their role in infectivity

Infection and Immunity

Volumn 80, Issue 7, 2012, Pages 2258-2264

  De Pablos, Luis Miguel ^a   Osuna, Antonio ^a  

^a UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C4B; DISPERSED GENE FAMILY 1 PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; LAMININ; LIGAND; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; MUCIN; SERINE PROTEINASE; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL TYPE; CHAGAS DISEASE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC VARIABILITY; HEART; HIGH THROUGHPUT SCREENING; HISTOPATHOLOGY; HOST CELL; HOST PARASITE INTERACTION; HUMAN; IMMUNITY; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOMICS; PROTOZOON; TELOMERE; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

GLYCOPROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; MUCINS; MULTIGENE FAMILY; NEURAMINIDASE; TRYPANOSOMA CRUZI; VIRULENCE FACTORS;

EID: 84864804882     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.06225-11     Document Type: Article

References (75)

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 glycosylphosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi. Biochem. J. 304:793- 802.
3. Almeida IC, Gazzinelli RT. 2001. Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. J. Leukoc. Biol. 70:467- 477.
4. Andersson B. 2011. The Trypanosoma cruzi genome; conserved core genes and extremely variable surface molecule families. Res. Microbiol. 162: 619-625.
5. Arioka S, et al. 2010. Potent inhibitor scaffold against Trypanosoma cruzi trans-sialidase. Bioorg. Med. Chem. 18:1633-1640.
6. Arner E, et al. 2007. Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants.BMCGenomics 8:391. doi:10.1186/1471-2164-8-391.
7. Atwood JA, III, et al. 2006. Glycoproteomics of Trypanosoma cruzi trypomastigotes using subcellular fractionation, lectin affinity, and stable isotope labeling. J. Proteome Res. 5:3376 -3384.
8. Atwood JA, III, et al. 2005. The Trypanosoma cruzi proteome. Science 309:473- 476.
9. Azuaje FJ, Ramirez JL, Da Silveira JF. 2007. In silico, biologicallyinspired modelling of genomic variation generation in surface proteins of Trypanosoma cruzi. Kinetoplastid Biol. Dis. 6:6. doi:10.1186/1475-9292-6-6.
10. Bartholomeu DC, et al. 2009. Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res. 37:3407-3417.
11. Beucher M, Norris KA. 2008. Sequence diversity of the Trypanosoma cruzi complement regulatory protein family. Infect. Immun. 76:750 -758.
12. Buscaglia CA, Campo VA, Frasch AC, Di Noia JM. 2006. Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat. Rev. Microbiol. 4:229 -236.
13. Buscaglia CA, Di Noia JM. 2003. Trypanosoma cruzi clonal diversity and the epidemiology of Chagas' disease. Microbes Infect. 5:419-427.
14. Buschiazzo A, Amaya MF, Cremona ML, Frasch AC, Alzari PM. 2002. The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol. Cell 10:757-768.
15. Campo VA, Buscaglia CA, Di Noia JM, Frasch AC. 2006. Immunocharacterization of the mucin-type proteins from the intracellular stage of Trypanosoma cruzi. Microbes Infect. 8:401- 409.
16. Cazzulo JJ, Frasch AC. 1992. SAPA/trans-sialidase and cruzipain: two antigens from Trypanosoma cruzi contain immunodominant but enzymatically inactive domains. FASEB J. 6:3259 -3264.
17. Chuenkova MV, Furnari FB, Cavenee WK, Pereira MA. 2001. Trypanosoma cruzi trans-sialidase: a potent and specific survival factor for human Schwann cells by means of phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl. Acad. Sci. U. S. A. 98:9936 -9941.
18. Chuenkova MV, Pereira MA. 2000. A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Mol. Biol. Cell 11:1487-1498.
19. Chuenkova MV, PereiraPerrin M. 2004. Chagas' disease parasite promotes neuron survival and differentiation through TrkA nerve growth factor receptor. J. Neurochem. 91:385-394.
20. Chuenkova MV, 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.
21. Chuenkova MV, PereiraPerrin M. 2009. Trypanosoma cruzi targets Akt in host cells as an intracellular antiapoptotic strategy. Sci. Signal. 2(97):ra74. doi:10.1126/scisignal.2000374.
22. Cura CI, et al. 2010. Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. Int. J. Parasitol. 40:1599 -1607.
23. de Melo-Jorge M, 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.
24. De Pablos LM, et al. 2011. Differential expression and characterization of a member of the mucin-associated surface proteins (MASP) family secreted by Trypanosoma cruzi. Infect. Immun. 79:3993- 4001.
25. De Pablos LM, Osuna A. 2012. Conserved regions as markers of different patterns of expression and distribution of the mucin-associated surfaceproteins (MASP) of Trypanosoma cruzi. Infect. Immun. 80:169 -174.
26. Di Noia JM, Buscaglia CA, De Marchi CR, Almeida IC, Frasch AC. 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.
27. Di Noia JM, D'Orso I, Sanchez DO, Frasch AC. 2000. AU-rich elements in the 3=-untranslated region of a new mucin-type gene family of Trypanosoma cruzi confersmRNAinstability and modulates translation efficiency. J. Biol. Chem. 275:10218 -10227.
28. El-Sayed NM, et al. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
29. El-Sayed NM, et al. 2005. Comparative genomics of trypanosomatid parasitic protozoa. Science 309:404-409.
30. Falla A, et al. 2009. Haplotype identification within Trypanosoma cruzi I in Colombian isolates from several reservoirs, vectors and humans. Acta Trop. 110:15-21.
31. Ferreira D, Cortez M, Atayde VD, Yoshida N. 2006. Actin cytoskeletondependent and -independent host cell invasion by Trypanosoma cruzi is mediated by distinct parasite surface molecules. Infect. Immun. 74:5522- 5528.
32. Franchin G, Pereira-Chioccola VL, Schenkman S, Rodrigues MM. 1997. Passive transfer of a monoclonal antibody specific for a sialic aciddependent epitope on the surface of Trypanosoma cruzi trypomastigotes reduces infection in mice. Infect. Immun. 65:2548 -2554.
33. Franzén O, et al. 2011. Shotgun sequencing analysis of Trypanosoma cruzi I Sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Negl. Trop. Dis. 5:e984. doi:10.1371/journal.pntd.0000984.
34. Freitas LM, et al. 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. doi:10.1371/ journal.pone.0025914.
35. Gibson W, Stevens J. 1999. Genetic exchange in the trypanosomatidae. Adv. Parasitol. 43:1- 46.
36. Giordano R, et al. 1999. Cloning of a surface membrane glycoprotein specific for the infective form of Trypanosoma cruzi having adhesive properties to laminin. J. Biol. Chem. 274:3461-3468.
37. Huang EJ, Reichardt LF. 2003. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72:609-642.
38. Jäger AV, Muia RP, Campetella O. 2008. Stage-specific expression of Trypanosoma cruzi trans-sialidase involves highly conserved 3= untranslated regions. FEMS Microbiol. Lett. 283:182-188.
39. Kawashita SY, Da Silva CV, Mortara RA, Burleigh BA, Briones MR. 2009. Homology, paralogy and function of DGF-1, a highly dispersed Trypanosoma cruzi specific gene family and its implications for information entropy of its encoded proteins. Mol. Biochem. Parasitol. 165:19 -31.
40. Kim D, 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.
41. Kissinger JC. 2006. A tale of three genomes: the kinetoplastids have arrived. Trends Parasitol. 22:240 -243.
42. Lander N, et al. 2010. Localization and developmental regulation of a dispersed gene family 1 protein in Trypanosoma cruzi. Infect. Immun. 78:231-240.
43. 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.
44. Macedo AM, Machado CR, Oliveira RP, Pena SD. 2004. Trypanosoma cruzi: genetic structure of populations and relevance of genetic variability to the pathogenesis of chagas disease. Mem. Inst. Oswaldo Cruz 99:1-12.
45. Magdesian MH, et al. 2001. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J. Biol. Chem. 276: 19382-19389.
46. Ming M, Chuenkova M, Ortega-Barria E, Pereira ME. 1993. Mediation of Trypanosoma cruzi invasion by sialic acid on the host cell and transsialidase on the trypanosome. Mol. Biochem. Parasitol. 59:243-252.
47. Minning TA, Weatherly DB, Flibotte S, Tarleton RL. 2011. Widespread, focal copy number variations (CNV) and whole chromosome aneuploidies in Trypanosoma cruzi strains revealed by array comparative genomic hybridization. BMC Genomics 12:139. doi:10.1186/1471-2164-12-139.
48. Moreira DR, Leite AC, dos Santos RR, Soares MB. 2009. Approaches for the development of new anti-Trypanosoma cruzi agents. Curr. Drug Targets 10:212-231.
49. Mucci J, et al. 2002. Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc. Natl. Acad. Sci. U. S. A. 99:3896 -3901.
50. 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.
51. Norris KA, Schrimpf JE. 1994. Biochemical analysis of the membrane and soluble forms of the complement regulatory protein of Trypanosoma cruzi. Infect. Immun. 62:236 -243.
52. Parodi AJ, et al. 1992. Identification of the gene(s) coding for the transsialidase of Trypanosoma cruzi. EMBO J. 11:1705-1710.
53. Pena SD, Machado CR, Macedo AM. 2009. Trypanosoma cruzi: ancestral genomes and population structure. Mem. Inst. Oswaldo Cruz 104(Suppl. 1):108 -114.
54. Pereira-Chioccola VL, 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. 113:1299- 1307.
55. Pereira ME. 1983. A developmentally regulated neuraminidase activity in Trypanosoma cruzi. Science 219:1444 -1446.
56. Pereira ME, Loures MA, Villalta F, Andrade AF. 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. 152:1375-1392.
57. Pollevick GD, et al. 2000. Trypanosoma cruzi surface mucins with exposed variant epitopes. J. Biol. Chem. 275:27671-27680.
58. 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.
59. 2+ signalling activity. Biochem. J. 330(Pt 1):505-511.
60. Schauer R, Reuter G, Mühlpfordt H, Andrade AF, Pereira ME. 1980. The occurrence of N-acetyl- and N-glycoloylneuraminic acid in Trypanosoma cruzi. Hoppe-Seylers Z. Physiol. Chem. 364:1053-1057.
61. 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.
62. Schenkman S, Mortara RA. 1992. HeLa cells extend and internalize pseudopodia during active invasion by Trypanosoma cruzi trypomastigotes. J. Cell Sci. 101(Pt 4):895-905.
63. Scudder P, Doom JP, Chuenkova M, Manger ID, Pereira ME. 1993. Enzymatic characterization of beta-D-galactoside alpha 2,3-trans-sialidase from Trypanosoma cruzi. J. Biol. Chem. 268:9886 -9891.
64. Souza RT, et al. 2007. New Trypanosoma cruzi repeated element that shows site specificity for insertion. Eukaryot. Cell 6:1228 -1238.
65. Sturm NR, Campbell DA. 2009. Alternative lifestyles: the population structure of Trypanosoma cruzi. Acta Trop. 115:35- 43.
66. Tibayrenc M, Ward P, Moya A, Ayala FJ. 1986. Natural populations of Trypanosoma cruzi, the agent of Chagas disease, have a complex multiclonal structure. Proc. Natl. Acad. Sci. U. S. A. 83:115-119.
67. Todeschini AR, et al. 2002. Trans-sialidase from Trypanosoma cruzi binds host T-lymphocytes in a lectin manner. J. Biol. Chem. 277:45962- 45968.
68. Tonelli RR, 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. doi:10.1371/ journal.pntd.0000864.
69. Tribulatti MV, Mucci J, Van Rooijen N, Leguizamón 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.
70. Ulrich PN, et al. 2011. Identification of contractile vacuole proteins in Trypanosoma cruzi. PLoS One 6:e18013. doi:10.1371/journal. pone.0018013.
71. Urban I, et al. 2011. Molecular diversity of the Trypanosoma cruzi TcSMUG family of mucin genes and proteins. Biochem. J. 438:303-313.
72. Villalta F, Smith CM, Ruiz-Ruano A, Lima MF. 2001. A ligand that Trypanosoma cruzi uses to bind to mammalian cells to initiate infection. FEBS Lett. 505:383-388.
73. Weinkauf C, Pereiraperrin M. 2009. Trypanosoma cruzi promotes neuronal and glial cell survival through the neurotrophic receptor TrkC. Infect. Immun. 77:1368 -1375.
74. Weinkauf C, Salvador R, PereiraPerrin M. 2011. Neurotrophin receptor TrkC is an entry receptor for Trypanosoma cruzi in neural, glial, and epithelial cells. Infect. Immun. 79:4081- 4087.
75. Zingales B, 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.