Novel strategy in Trypanosoma cruzi cell invasion: Implication of cholesterol and host cell microdomains

International Journal for Parasitology

Volumn 37, Issue 13, 2007, Pages 1431-1441

  Fernandes, Maria Cecília ^a   Cortez, Mauro ^a   Geraldo Yoneyama, Kelly Aparecida ^a   Straus, Anita Hilda ^a   Yoshida, Nobuko ^a   Mortara, Renato Arruda ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Amastigote; Cell invasion; Cholesterol; Membrane rafts; Trypanosoma cruzi; Trypomastigote

Indexed keywords

BIOLOGICAL MARKER; CHOLERA TOXIN B SUBUNIT; CHOLESTEROL; FILIPIN; FLUORESCEIN ISOTHIOCYANATE; GANGLIOSIDE GM1; MEMBRANE LIPID; METHYL BETA CYCLODEXTRIN; SPHINGOLIPID; STEROL;

CHAGAS DISEASE; CHOLERA; ETIOLOGY; HOST; INVASIBILITY; PARASITE; PROTOZOAN;

AMASTIGOTE; ANIMAL CELL; ARTICLE; CELL INVASION; CELL MEMBRANE; CELL SURFACE; CHEMICAL LABELING; FEMALE; HELA CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; LIPID RAFT; NONHUMAN; PROTEIN BINDING; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; VERO CELL;

ANIMALS; BETA-CYCLODEXTRINS; CERCOPITHECUS AETHIOPS; CHOLERA TOXIN; CHOLESTEROL; G(M1) GANGLIOSIDE; HELA CELLS; HOST-PARASITE INTERACTIONS; HUMANS; TRYPANOSOMA CRUZI; VERO CELLS;

MAMMALIA; TRYPANOSOMA CRUZI;

EID: 34548681879     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2007.04.025     Document Type: Article

References (61)

1. Abrami L., and Der Goot F.G. Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol. 147 (1999) 175-184
2. Andrews N.W., Hong K.-S., Robbins E.S., and Nussenzweig V. Stage-specific surface antigens expressed during the morphogenesis of vertebrate forms of Trypanosoma cruzi. Exp. Parasitol. 64 (1987) 474-484
3. Andrews N.W., Robbins E.S., Ley V., Hong K.S., and Nussenzweig V. Developmentally regulated, phospholipase C-mediated release of the major surface glycoprotein of amastigotes of Trypanosoma cruzi. J. Exp. Med. 167 (1988) 300-314
4. Barros H.C., Verbisck N.V., Silva S., Araguth M.F., and 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
5. Brener Z. Biology of Trypanosoma cruzi. Annu. Rev. Microbiol. 27 (1973) 347-382
6. Brener Z., and Chiari E. Variações morfológicas observadas em diferentes amostras de Trypanosoma cruzi. Rev. Inst. Med. Trop. São Paulo 5 (1963) 220-224
7. Briones M.R., Souto R.P., Stolf B.S., and 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
8. Brisse S., Dujardin J.C., and Tibayrenc M. Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Mol. Biochem. Parasitol. 111 (2000) 95-105
9. 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
10. Cardoso de Almeida M.L., and Heise N. Proteins anchored via glycosylphosphatidylinositol and solubilizing phospholipases in Trypanosoma cruzi. Biol. Res. 26 (1993) 285-312
11. Coppens I., and Joiner K.A. Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol. Biol. Cell 14 (2003) 3804-3820
12. De Souza W. Basic cell biology of Trypanosoma cruzi. Curr. Pharm. Des. 8 (2002) 269-285
13. Fernandes A.B., and Mortara R.A. 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. Infect. 6 (2004) 460-467
14. Fernandes A.B., Neira I., Ferreira A.T., and Mortara R.A. Cell invasion by Trypanosoma cruzi amastigotes of distinct infectivities: studies on signaling pathways. Parasitol. Res. 100 (2006) 59-68
15. Ferreira D., Cortez M., Atayde V.D., and Yoshida N. Actin cytoskeleton-dependent and -independent host cell invasion by Trypanosoma cruzi is mediated by distinct parasite surface molecules. Infect. Immun. 74 (2006) 5522-5528
16. Fewster M.E., Burns B.J., and Mead J.F. Quantitative densitometric thin-layer chromatography of lipids using copper acetate reagent. J. Chromatogr. 43 (1969) 120-126
17. Gulbins E., Dreschers S., Wilker B., and Grassme H. Ceramide, membrane rafts and infections. J. Mol. Med. 82 (2004) 357-363
18. Ilangumaran S., and Hoessli D.C. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335 Pt 2 (1998) 433-440
19. Incardona J.P., and Eaton S. Cholesterol in signal transduction. Curr. Opin. Cell Biol. 12 (2000) 193-203
20. Kruth H.S., and Vaughan M. Quantification of low density lipoprotein binding and cholesterol accumulation by single human fibroblasts using fluorescence microscopy. J. Lipid Res. 21 (1980) 123-130
21. Lafont F., and van der Goot F.G. Bacterial invasion via lipid rafts. Cell Microbiol. 7 (2005) 613-620
22. Lauer S., VanWye J., Harrison T., McManus H., Samuel B.U., Hiller N.L., Mohandas N., and Haldar K. Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19 (2000) 3556-3564
23. Lencer W.I., and Tsai B. The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 28 (2003) 639-645
24. Ley V., Andrews N.W., Robbins E.S., and Nussenzweig V. Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. J. Exp. Med. 168 (1988) 649-659
25. Li N., Mak A., Richards D.P., Naber C., Keller B.O., Li L., and Shaw A.R. Monocyte lipid rafts contain proteins implicated in vesicular trafficking and phagosome formation. Proteomics 3 (2003) 536-548
26. Li X., Leu S., Cheong A., Zhang H., Baibakov B., Shih C., Birnbaum M.J., and Donowitz M. Akt2, phosphatidylinositol 3-kinase, and PTEN are in lipid rafts of intestinal cells: role in absorption and differentiation. Gastroenterology 126 (2004) 122-135
27. Manes S., del Real G., and Martinez A. Pathogens: raft hijackers. Nat. Rev. Immunol. 3 (2003) 557-568
28. Ming M., Ewen M.E., and Pereira M.E.A. Trypanosome invasion of mammalian cells requires activation of the TGFβ signaling pathway. Cell 82 (1995) 287-296
29. Mortara R.A. Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Exp. Parasitol. 73 (1991) 1-14
30. Mortara R.A., Andreoli W.K., Taniwaki N.N., Fernandes A.B., Silva C.V., Fernandes M.C., L'Abbate C., and Silva S. Mammalian cell invasion and intracellular trafficking by Trypanosoma cruzi infective forms. An. Acad. Bras. Cienc. 77 (2005) 77-94
31. Mortara R.A., Procópio D.O., Barros H.C., Verbisck N.V., Andreoli W.K., Silva R.B., and Silva S. Features of host cell invasion by different infective forms of Trypanosoma cruzi. Mem. Inst. Oswaldo Cruz 94 Suppl. 1 (1999) 135-137
32. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
33. Neira I., Ferreira A.T., and 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
34. Ohvo-Rekila H., Akerlund B., and Slotte J.P. Cyclodextrin-catalyzed extraction of fluorescent sterols from monolayer membranes and small unilamellar vesicles. Chem. Phys. Lipids 105 (2000) 167-178
35. Ortega-Barria E., and Pereira M.E.A. A novel Trypanosoma cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67 (1991) 411-421
36. Pang H., Le P.U., and Nabi I.R. Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J. Cell Sci. 117 (2004) 1421-1430
37. Pelkmans L. Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim. Biophys. Acta 1746 (2005) 295-304
38. Pike L.J. Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J. Lipid Res. 47 (2006) 1597-1598
39. Procópio D.O., Barros H.C., and 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
40. Pucadyil T.J., Tewary P., Madhubala R., and Chattopadhyay A. Cholesterol is required for Leishmania donovani infection: implications in leishmaniasis. Mol. Biochem. Parasitol. 133 (2004) 145-152
41. Ramirez M.I., Ruiz R.C., Araya J.E., Franco da Silveira J., and Yoshida N. Involvement of the stage-specific 82-kilodalton adhesion molecule of Trypanosoma cruzi metacyclic trypomastigotes in host cell invasion. Infect. Immun. 61 (1993) 3636-3641
42. Rodriguez N.E., Gaur U., and Wilson M.E. Role of caveolae in Leishmania chagasi phagocytosis and intracellular survival in macrophages. Cell Microbiol. 8 (2006) 1106-1120
43. 2+ signalling activity. Biochem. J. 330 (1998) 505-511
44. Ruiz R.C., Rigoni V.L., Gonzalez J.C., and Yoshida N. The 35/50 kDa surface antigen of Trypanosoma cruzi metacyclic trypomastigotes, an adhesion molecule involved in host cell invasion. Parasite Immunol. 15 (1993) 121-125
45. Schenkman S., Ferguson M.A., Heise N., de Almeida M.L., Mortara R.A., and Yoshida N. 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 (1993) 293-303
46. Seveau S., Bierne H., Giroux S., Prevost M.C., and Cossart P. Role of lipid rafts in E-cadherin-and HGF-R/Met - mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 166 (2004) 743-753
47. Silva C.V., Luquetti A.O., Rassi A., and Mortara R.A. Involvement of Ssp-4-related carbohydrate epitopes in mammalian cell invasion by Trypanosoma cruzi amastigotes. Microbes. Infect. 8 (2006) 2120-2129
48. Simons K., and Ehehalt R. Cholesterol, lipid rafts, and disease. J. Clin. Invest. 110 (2002) 597-603
49. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
50. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 (2000) 31-39
51. Souto R.P., Fernandes O., Macedo A.M., Campbell D.A., and Zingales B. DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 83 (1996) 141-152
52. Straus A.H., Levery S.B., Jasiulionis M.G., Salyan M.E.K., Steele S.J., Travassos L.R., Hakomori S., and Takahashi H.K. Stage-specific glycosphingolipids from amastigote forms of Leishmania (L.) amazonensis. Immunogenicity and role in parasite binding and invasion of macrophages. J. Biol. Chem. 268 (1993) 13723-13730
53. Tardieux I., Webster P., Ravesloot J., Boron W., Lunn J.A., Heuser J.E., and Andrews N.W. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 71 (1992) 1117-1130
54. Tewary P., Veena K., Pucadyil T.J., Chattopadhyay A., and Madhubala R. The sterol-binding antibiotic nystatin inhibits entry of non-opsonized Leishmania donovani into macrophages. Biochem. Biophys. Res. Commun. 339 (2006) 661-666
55. Wilkowsky S.E., Barbieri M.A., Stahl P., and Isola E.L.D. Trypanosoma cruzi: phosphatidylinositol 3-kinase and protein kinase B activation is associated with parasite invasion. Exp. Cell Res. 264 (2001) 211-218
56. Woolsey A.M., Sunwoo L., Petersen C.A., Brachmann S.M., Cantley L.C., and Burleigh B.A. Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J. Cell Sci. 116 (2003) 3611-3622
57. Yancey P.G., Rodrigueza W.V., Kilsdonk E.P., Stoudt G.W., Johnson W.J., Phillips M.C., and Rothblat G.H. Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271 (1996) 16026-16034
58. Yoneyama K.A., Tanaka A.K., Silveira T.G., Takahashi H.K., and Straus A.H. Characterization of Leishmania (Viannia) braziliensis membrane microdomains, and their role in macrophage infectivity. J. Lipid Res. 47 (2006) 2171-2178
59. Yoshida N. Surface antigens of metacyclic trypomastigotes of Trypanosoma cruzi. Infect. Immun. 40 (1983) 836-839
60. Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An. Acad. Bras. Cienc. 78 (2006) 87-111
61. Yoshida N., Mortara R.A., Araguth M.F., Gonzalez J.C., and Russo M. Metacyclic neutralizing effect of monoclonal antibody 10D8 directed to the 35- and 50-kilodalton surface glycoconjugates of Trypanosoma cruzi. Infect. Immun. 57 (1989) 1663-1667