Trypanosoma cruzi cell invasion and traffic: Influence of Coxiella burnetii and pH in a comparative study between distinct infective forms

Microbial Pathogenesis

Volumn 43, Issue 1, 2007, Pages 22-36

  Fernandes, Maria Cecília ^a   L'Abbate, Carolina ^a   Kindro Andreoli, Walter ^a   Mortara, Renato Arruda ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Amastigote; Cell invasion; Coxiella burnetii; Phagosome; Trypanosoma cruzi; Trypomastigote

Indexed keywords

EARLY ENDOSOME ANTIGEN 1; FUNGUS ANTIGEN; HEMOLYSIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; SIALIDASE; UNCLASSIFIED DRUG;

AMASTIGOTE; ANIMAL CELL; ARTICLE; CELL INVASION; CELL MIGRATION; CELL PH; CELL VACUOLE; CONTROLLED STUDY; COXIELLA BURNETII; ENZYME ACTIVITY; FUNGAL CELL; FUNGAL STRAIN; FUNGAL VIRULENCE; HOST PATHOGEN INTERACTION; INTRACELLULAR TRANSPORT; MOUSE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; STRAIN DIFFERENCE; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; VERO CELL;

ANIMALS; CERCOPITHECUS AETHIOPS; COXIELLA BURNETII; ENDOSOMES; HYDROGEN-ION CONCENTRATION; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMES; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; TRYPANOSOMA CRUZI; VACUOLES; VERO CELLS; VESICULAR TRANSPORT PROTEINS;

BACTERIA (MICROORGANISMS); COXIELLA BURNETII; TRYPANOSOMA CRUZI;

EID: 34247622275     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2007.02.005     Document Type: Article

References (64)

1. 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
2. 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
3. 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
4. Behbehani K. Developmental cycles of Trypanosoma (Schyzotrypanum) cruzi (Chagas, 1909) in mouse peritoneal macrophages in vitro. Parasitology 66 (1973) 343-353
5. Nogueira N., and Cohn Z. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J Exp Med 143 (1976) 1402-1420
6. Hudson L., Snary D., and Morgan S.J. Trypanosoma cruzi: continuous cultivation with murine cell lines. Parasitology 88 (1984) 283-294
7. Ulisses de Carvalho T.M., and De Souza W. Infectivity of amastigotes of Trypanosoma cruzi. Rev Inst Med Trop São Paulo 28 (1986) 205-212
8. Pan S.C.T. Trypanosoma cruzi: in vitro interactions between cultured amastigotes and human skin-muscle cells. Exp Parasitol 45 (1978) 274-286
9. 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
10. 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
11. Mortara R.A. Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Exp Parasitol 73 (1991) 1-14
12. 2+ signalling activity. Biochem J 330 (1998) 505-511
13. Malaga S., and Yoshida N. Targeted reduction in expression of Trypanosoma cruzi surface glycoprotein gp90 increases parasite infectivity. Infect Immun 69 (2001) 353-359
14. 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
15. 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
16. Mortara R.A., Procópio D.O., Barros H.C., Verbisck N.V., Andreoli W.K., Silva R.B., et al. Features of host cell invasion by different infective forms of Trypanosoma cruzi. Mem Inst Oswaldo Cruz 94 Suppl. 1 (1999) 135-137
17. Acosta-Serrano A., Almeida I.C., Freitas-Junior L.H., Yoshida N., and Schenkman S. The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. Mol Biochem Parasitol 114 (2001) 143-150
18. Burleigh B.A., and Andrews N.W. The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu Rev Microbiol 49 (1995) 175-200
19. Yoshida N., Favoreto Jr. S., Ferreira A.T., and Manque P.M. Signal transduction induced in Trypanosoma cruzi metacyclic trypomastigotes during the invasion of mammalian cells. Braz J Med Biol Res 33 (2000) 269-278
20. Tardieux I., Webster P., Ravesloot J., Boron W., Lunn J.A., Heuser J.E., et al. Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 71 (1992) 1117-1130
21. Procópio D.O., Silva S., Cunningham C.C., and 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
22. Andreoli W.K., and Mortara R.A. Acidification modulates the traffic of Trypanosoma cruzi trypomastigotes in Vero cells harboring Coxiella burnetti vacuoles. Int J Parasitol 33 (2003) 185-197
23. Stecconi-Silva R.B., Andreoli W.K., and Mortara R.A. Parameters affecting cellular invasion and escape from the parasitophorous vacuole by different infective forms of Trypanosoma cruzi. Mem Inst Oswaldo Cruz 98 (2003) 953-958
24. Andrews N.W., and Whitlow M.B. Secretion by Trypanosoma cruzi of a hemolysin active at low pH. Mol Biochem Parasitol 33 (1989) 249-256
25. Hall B.F., Webster P., Ma A.K., Joiner K.A., and Andrews N.W. Desialylation of lysosomal membrane glycoproteins by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm. J Exp Med 176 (1992) 313-325
26. Knodler L.A., Celli J., and Finlay B.B. Pathogenic trickery: deception of host cell processes. Nat Rev Mol Cell Biol 2 (2001) 578-588
27. Rabinovitch M., Freymuller E., de Paula R.A., Manque P.M., Andreoli W.K., and Mortara R.A. Cell co-infections with non-viral pathogens and the construction of doubly infected phagosomes. In: Gordon S. (Ed). Phagocytosis: microbial invasion (1999), JAI Press Inc., Stamford, Connecticut 349-371
28. Rabinovitch M., and Veras P.S. Cohabitation of Leishmania amazonensis and Coxiella burnetii. Trends Microbiol 4 (1996) 158-161
29. Baca O.G., and Paretsky D. Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiol Rev 47 (1983) 127-149
30. Hackstadt T., and Williams J.C. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci USA 78 (1981) 3240-3244
31. Maurin M., Benoliel A.M., Bongrand P., and Rault D. Phagolysosome of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect Immun 60 (1992) 5013-5016
32. Veras P.S.T., Moulia C., Dauguet C., Tunis C.T., Thibon M., and Rabinovitch M. Entry and survival of Leishmania amazonensis amastigotes within phagolysosome-like vacuoles that shelter Coxiella burnetii in Chinese hamster ovary cells. Infect Immun 63 (1995) 3502-3506
33. Sinai A.P., Paul S., Rabinovitch M., Kaplan G., and Joiner K.A. Coinfection of fibroblasts with Coxiella burnetti and Toxoplasma gondii: to each their own. Microbes Infect 2 (2000) 727-736
34. Andreoli W.K., Taniwaki N.N., and Mortara R.A. Survival of Trypanosoma cruzi metacyclic trypomastigotes within Coxiella burnetii vacuoles: differentiation and replication within an acidic milieu. Microbes Infect 8 (2006) 172-182
35. Burton P.R., Stueckemann J., Welsh R.M., and Paretsky D. Some ultrastructural effects of persistent infections by the rickettsia Coxiella burnetii in mouse L cells and green monkey kidney (Vero) cells. Infect Immun 21 (1978) 556-566
36. Dröšse S., and Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200 Pt 1 (1997) 1-8
37. Andrews N.W. The acid-active hemolysin of Trypanosoma cruzi. Exp Parasitol 71 (1990) 241-244
38. 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
39. Wilkowsky S.E., Barbieri M.A., Stahl P.D., and Isola E.L. Regulation of Trypanosoma cruzi invasion of nonphagocytic cells by the endocytically active GTPases dynamin, Rab5, and Rab7. Biochem Biophys Res Commun 291 (2002) 516-521
40. 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
41. Clague M.J., Urbe S., Aniento F., and Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J Biol Chem 269 (1994) 21-24
42. Yamamoto A., Tagawa Y., Yoshimori T., Moriyama Y., Masaki R., and Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23 (1998) 33-42
43. Presley J.F., Mayor S., McGraw T.E., Dunn K.W., and Maxfield F.R. Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J Biol Chem 272 (1997) 13929-13936
44. Caler E.V., Vaena d.A., Haynes P.A., Andrews N.W., and Burleigh B.A. Oligopeptidase B-dependent signaling mediates host cell invasion by Trypanosoma cruzi. EMBO J 17 (1998) 4975-4986
45. 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
46. 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
47. 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
48. Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An Acad Bras Ciênc 78 (2006) 87-111
49. 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
50. 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
51. 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
52. Pereira-Chioccola V.L., Acosta-Serrano A., Almeida I.C., Ferguson M.A., Souto-Padrón T., Rodrigues M.M., et al. 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 (2000) 1299-1307
53. Rodriguez A., Samoff E., Rioult M.G., Chung A., and Andrews N.W. Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol 134 (1996) 349-362
54. 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
55. Mortara R.A., Andreoli W.K., Taniwaki N.N., Fernandes A.B., Silva C.V., Fernandes M.C., et al. Mammalian cell invasion and intracellular trafficking by Trypanosoma cruzi infective forms. An Acad Bras Ciênc 77 (2005) 77-94
56. Zamboni D.S., Mortara R.A., and Rabinovitch M. Infection of Vero cells with Coxiella burnetii phase II: relative intracellular bacterial load and distribution estimated by confocal laser scanning microscopy and morphometry. J Microbiol Meth 43 (2001) 223-232
57. Yoshida N. Surface antigens of metacyclic trypomastigotes of Trypanosoma cruzi. Infect Immun 40 (1983) 836-839
58. Pizzi T.P., Rubio M.D., Prager R., and Silva R.C. Acción de la cortisona en la infección experimental por Trypanosoma cruzi. Bol Chil Parasitol 7 (1952) 22-24
59. Brener Z., and Chiari E. Variações morfológicas observadas em diferentes amostras de Trypanosoma cruzi. Rev Inst Med Trop São Paulo 5 (1963) 220-224
60. Silva L.H.P., and Nussenzweig V. Sobre uma cepa de Trypanosoma cruzi altamente virulenta para o camundongo branco. Folia Clin Biol 20 (1953) 191-203
61. Schenkman S., Robbins E.S., and Nussenzweig V. Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infect Immun 59 (1991) 645-654
62. Schenkman S., Chaves L.B., Pontes de Carvalho L.C., and Eichinger D. A proteolytic fragment of Trypanosoma cruzi trans-sialidase lacking the carboxyl-terminal domain is active, monomeric, and generates antibodies that inhibit enzymatic activity. J Biol Chem 269 (1994) 7970-7975
63. Andreoli W.K., and Mortara R.A. Traffic of Trypanosoma cruzi trypomastigotes within Vero cells colonized with Coxiella burnetii: invasion, transference and...escape?. Rev Inst Med Trop São Paulo 45 (2003) 36
64. Zhou Y., Marcus E.M., and Haugland R.P. Opas M, Use of a new fluorescent probe, seminaphthofluorescein-calcein, for determination of intracellular pH by simultaneous dual-emission imaging laser scanning confocal microscopy. J Cell Physiol 164 (1995) 9-16