Invasion of MDCK epithelial cells with altered expression of Rho GTPases by Trypanosoma cruzi amastigotes and metacyclic trypomastigotes of strains from the two major phylogenetic lineages

Microbes and Infection

Volumn 6, Issue 5, 2004, Pages 460-467

  Fernandes, Adriana B ^a   Mortara, Renato A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Amastigotes; Cell invasion; Phylogenetic lineages; Rho GTPases; Trypanosoma cruzi; Trypomastigotes

Indexed keywords

RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

AMASTIGOTE; ANIMAL CELL; ARTICLE; CELL INVASION; CELL LINE; EPITHELIUM CELL; GENETIC TRANSFECTION; KIDNEY CELL; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL LINE; CYTOSKELETAL PROTEINS; DOGS; EPITHELIAL CELLS; HOST-PARASITE RELATIONS; LIFE CYCLE STAGES; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; TRYPANOSOMA CRUZI;

MAMMALIA; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 1942485341     PISSN: 12864579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micinf.2004.01.009     Document Type: Article

References (57)

1. Souto R.P., Fernandes O., Macedo A.M., Campbell D.A., Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 83:1996;141-152.
2. Briones M.R., Souto R.P., Stolf B.S., Zingales B. The evolution of two Trypanosoma cruzi subgroups inferred from rRNA genes can be correlated with the interchange of American mammalian faunas in the Cenozoic and has implications to pathogenicity and host specificity. Mol. Biochem. Parasitol. 104:1999;219-232.
3. Devera R., Fernandes O., Coura J.R. Should Trypanosoma cruzi be called "cruzi" complex? A review of the parasite diversity and the potential of selecting population after in vitro culturing and mice infection. Mem. Inst. Oswaldo Cruz (Rio de Janeiro). 98:2003;1-12.
4. Neira I., Ferreira A.T., Yoshida N. Activation of distinct signal transduction pathways in Trypanosoma cruzi isolates with differential capacity to invade host cells. Int. J. Parasitol. 32:2002;405-414.
5. Brener Z. Biology of Trypanosoma cruzi. Annu. Rev. Microbiol. 27:1973;347-382.
6. Hudson L., Snary D., Morgan S.J. Trypanosoma cruzi: continuous cultivation with murine cell lines. Parasitology. 88:1984;2-P283-2-P294.
7. Nogueira N., Cohn Z. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J. Exp. Med. 143:1976;1402-1420.
8. Behbehani K. Developmental cycles of Trypanosoma (Schyzotrypanum) cruzi (Chagas, 1909) in mouse peritoneal macrophages in vitro. Parasitology. 66:1973;343-353.
9. Ulisses de Carvalho T.M., De Souza W. Infectivity of amastigotes of Trypanosoma cruzi. Rev. Inst. Med. Trop. São Paulo. 28:1986;205-212.
10. Andrews N.W., Hong K.-S., Robbins E.S., Nussenzweig V. Stage-specific surface antigens expressed during the morphogenesis of vertebrate forms of Trypanosoma cruzi. Exp. Parasitol. 64:1987;474-484.
11. Pan S.C.T. Trypanosoma cruzi: In vitro interactions between cultured amastigotes and human skin-muscle cells. Exp. Parasitol. 45:1978;274-286.
12. Ley V., Andrews N.W., Robbins E.S., Nussenzweig V. Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. J. Exp. Med. 168:1988;649-659.
13. Mortara R.A. Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Exp. Parasitol. 73:1991;1-14.
14. Barros H.C., Silva S., Verbisck N.V., Araguth M.F., Tedesco R.C., Procópio D.O., Mortara R.A. Release of membrane-bound trails by Trypanosoma cruzi amastigotes onto modified surfaces and mammalian cells. J. Eukaryot. Microbiol. 43:1996;275-285.
15. Villalta F., Kierszenbaum F. Growth of isolated amastigotes of Trypanosoma cruzi in cell-free medium. J. Protozool. 29:1982;570-576.
16. Pan A.A., McMahon-Pratt D. Amastigote and epimastigote stage-specific components of Trypanosoma cruzi characterized by using monoclonal antibodies. J. Immunol. 143:1989;1001-1008.
17. Barros H.C., Verbisck N.V., Silva S., Araguth M.F., Mortara R.A. Distribution of epitopes of Trypanosoma cruzi amastigotes during the intracellular life cycle within mammalian cells. J. Eukaryot. Microbiol. 44:1997;332-344.
18. Silva E.O., Saraiva E.M.B., De Souza W., Souto-Padrón T. Cell surface characterization of amastigotes of Trypanosoma cruzi obtained from different sources. Parasitol. Res. 84:1998;257-263.
19. Hall B.F., Joiner K.A. Developmentally-regulated virulence factors of Trypanosoma cruzi and their relationship to evasion of host defences. J. Euk. Microbiol. 40:1993;207-213.
20. Jacobson K.C., Fletcher R.C., Kuhn R.E. Binding of antibody and resistance to lysis of trypomastigotes of Trypanosoma cruzi. Parasite Immunol. 14:1992;1-12.
21. Carvalho R.M.G., Meirelles M.N.L., De Souza W., Leon W. Isolation of the intracellular stage of Trypanosoma cruzi and its interaction with mouse macrophages in vitro. Infect. Immun. 33:1981;546-554.
22. Umezawa E.S., Milder R.V., Abrahamsohn I.A. Trypanosoma cruzi amastigotes: development in vitro and infectivity in vivo of the forms isolated from spleen and liver. Acta Trop. 42:1985;25-32.
23. Iida K., Whitlow M.B., Nussenzweig V. Amastigotes of Trypanosoma cruzi escape destruction by the terminal complement components. J. Exp. Med. 169:1989;881-891.
24. Verbisck N.V., Silva S., Mortara R.A. Trypanosoma cruzi: amastigote polymorphism defined by monoclonal antibodies. Braz. J. Med. Biol. Res. 31:1998;1583-1591.
25. Schenkman S., Mortara R.A. HeLa cells extend and internalize pseudopodia during active invasion by Trypanosoma cruzi trypomastigotes. J. Cell Sci. 101:1992;895-905.
26. Kahn S., Wleklinski M., Aruffo A., Farr A., Coder D., Kahn M. Trypanosoma cruzi amastigote adhesion to macrophages is facilitated by the mannose receptor. J. Exp. Med. 182:1995;1243-1258.
27. Schenkman R.P.F., Vandekerckhove F., Schenkman S. Mammalian cell sialic acid enhances invasion by Trypanosoma cruzi. Infect. Immun. 61:1993;898-902.
28. Stecconi-Silva R.B., Andreoli W.K., Mortara R.A. Parameters affecting cellular invasion and escape from the parasitophorous vacuole by different infective forms of Trypanosoma cruzi. Mem. Inst. Oswaldo Cruz (Rio de Janeiro). 98:2003;953-958.
29. Procópio D.O., Silva S., Cunningham C.C., Mortara R.A. Trypanosoma cruzi: effect of protein kinase inhibitors and cytoskeletal protein organization and expression on host cell invasion by amastigotes and metacyclic trypomastigotes. Exp. Parasitol. 90:1998;1-13.
30. Procópio D.O., Barros H.C., Mortara R.A. Actin-rich structures formed during the invasion of cultured cells by infective forms of Trypanosoma cruzi. Eur. J. Cell Biol. 78:1999;911-924.
31. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:1992;389-399.
32. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
33. Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10:1994;31-54.
34. Nobes C.D., Hall A. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995;53-62.
35. Kozma R., Ahmed S., Best A., Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15:1995;1942-1952.
36. Jou T.S., Nelson W.J. Effects of regulated expression of mutant RhoA and Rac1 small GTPases on the development of epithelial (MDCK) cell polarity. J. Cell Biol. 142:1998;85-100.
37. Yoshida N. Surface antigens of metacyclic trypomastigotes of Trypanosoma cruzi. Infect. Immun. 40:1983;836-839.
38. Pizzi T.P., Rubio M.D., Prager R., Silva R.C. Acción de la cortisona en la infección experimental por Trypanosoma cruzi. Bol. Chil. Parasitol. 7:1952;22-24.
39. Brener Z., Chiari E. Variações morfológicas observadas em diferentes amostras de Trypanosoma cruzi. Rev. Inst. Med. Trop. São Paulo. 5:1963;220-224.
40. Silva L.H.P., Nussenzweig V. Sobre uma cepa de Trypanosoma cruzi altamente virulenta para o camundongo branco. Folia Clin. Biol. 20:1953;191-203.
41. Abrahamsohn I.A., Katzin A.M., Milder R.V. A method for isolating Trypanosoma cruzi amastigotes from spleen and liver using two-step discontinuous gradient centrifugation. J. Parasitol. 69:1983;437-439.
42. Boné G.J., Steinert M. Isotopes incorporated in nucleic acids of Trypanosoma mega. Nature. 178:1956;308-309.
43. Camargo E.P. Growth and differentiation in Trypanosoma cruzi: origin of metacyclic trypomastigotes in liquid media. Rev. Inst. Med. Trop. São Paulo. 6:1964;93-100.
44. Almeida I.C., Milani S.R., Gorin P.A.J., Travassos L.R. Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-α-galactosyl antibodies. J. Immunol. 146:1991;2394-2400.
45. Nogueira N., Bianco C., Cohn Z. Studies on the selective lysis and purification of Trypanosoma cruzi. J. Exp. Med. 142:1975;224-229.
46. Schenkman S., Diaz C., Nussenzweig V. Attachment of Trypanosoma cruzi trypomastigotes to receptors at restricted cell surface domains. Exp. Parasitol. 72:1991;76-86.
47. Teixeira M.M.G., Yoshida N. Stage-specific surface antigens of metacyclic trypomastigotes of Trypanosoma cruzi identified by monoclonal antibodies. Mol. Biochem. Parasitol. 18:1986;271-282.
48. Mortara R.A., Procópio D.O., Barros H.C., Verbisck N.V., Andreoli W.K., Silva R.B., Silva S. Features of host cell invasion by different infective forms of Trypanosoma cruzi. Mem. Inst. Oswaldo Cruz. 94:(Suppl 1):1999;135-137.
49. Morais Rêgo S.F. Sôbre o encontro de formas tissulares do Trypanosoma cruzi (Chagas 1909) no sangue circulante do camundongo branco (Mus musculus). Folia Clin. Biol. 26:1956;17-45.
50. McCabe R.E., Remington J.S., Araujo F.G. Mechanisms of invasion and replication of the intracellular stage in Trypanosoma cruzi. Infect. Immun. 46:1984;372-376.
51. Burleigh B.A., Andrews N.W. The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu. Rev. Microbiol. 49:1995;175-200.
52. Criss A.K., Ahlgren D.M., Jou T.S., McCormick B.A., Casanova J.E. The GTPase Rac1 selectively regulates Salmonella invasion at the apical plasma membrane of polarized epithelial cells. J. Cell Sci. 114:2001;1331-1341.
53. Stender S., Friebel A., Linder S., Rohde M., Mirold S., Hardt W.D. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36:2000;1206-1221.
54. Friebel A., Ilchmann H., Aepfelbacher M., Ehrbar K., Machleidt W., Hardt W.D. SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J. Biol. Chem. 276:2001;34035-34040.
55. Mounier J., Laurent V., Hall A., Fort P., Carlier M.F., Sansonetti P.J., Egile C. Rho family GTPases control entry of Shigella flexneri into epithelial cells but not intracellular motility. J. Cell Sci. 112:2003;2069-2080.
56. Procópio D.O., Barros H.C., Mortara R.A. Actin-rich structures formed during the invasion of cultured cells by infective forms of Trypanosoma cruzi. Eur. J. Cell Biol. 78:1999;911-924.
57. 2+ signalling activity. Biochem. J. 330:1998;505-511.