Mechanisms of host cell invasion by trypanosoma cruzi

Advances in Parasitology

Volumn 76, Issue , 2011, Pages 33-61

  Caradonna, Kacey L ^a   Burleigh, Barbara A ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Chagas disease; Invasion; Signaling; Trypanosoma cruzi; Trypomastigotes

Indexed keywords

ACTIN; CALCIUM; CALCIUM ION; CYCLIC AMP; CYTOCHALASIN D; CYTOKERATIN 18; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN; GLYCOPROTEIN 82; GLYCOPROTEIN 85; GLYCOPROTEIN 90; INOSITOL 1,4,5 TRISPHOSPHATE; LOW DENSITY LIPOPROTEIN RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MUCIN; MUCIN ASSOCIATED PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN; PROTEIN KINASE B; REPLICATION FACTOR A; RHO KINASE; UNCLASSIFIED DRUG; VIMENTIN;

AMASTIGOTE; ANTIGEN EXPRESSION; AUTOPHAGY; BOOK; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ADHESION; CELL INTERACTION; CELL INVASION; CELL MEMBRANE; CELL PROLIFERATION; CELL VACUOLE; CHAGAS DISEASE; CYTOSKELETON; CYTOSOL; ENDOCYTOSIS; ENDOSOME; EPIMASTIGOTE; EXOCYTOSIS; EXTRACELLULAR MATRIX; FIBROBLAST; GENETIC VARIABILITY; HEART MUSCLE CELL; HOST CELL; HOST PARASITE INTERACTION; HUMAN; INFLAMMATORY INFILTRATE; INTERNALIZATION; LIFE CYCLE; LYSOSOME; MICROTUBULE; MOLECULAR INTERACTION; NEUROPROTECTION; NONHUMAN; PARASITE LOCALIZATION; PARASITE TRANSMISSION; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TROPISM; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; UMBILICAL VEIN ENDOTHELIAL CELL;

MAMMALIA; TRYPANOSOMA CRUZI;

EID: 80052154495     PISSN: 0065308X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385895-5.00002-5     Document Type: Chapter

References (121)

1. Acosta-Serrano A., Almeida I.C., Freitas-Junior L.H., Yoshida N., Schenkman S. The mucin-like glycoprotein super-family of Trypansoma cruzi: structure and biological roles. Mol. Biochem. Parasitol. 2001, 114:143-150.
2. Albertti L.A., Macedo A.M., Chiari E., Andrews N.W., Andrade L.O. Role of host lysosomal associated membrane protein (LAMP) in Trypanosoma cruzi invasion and intracellular development. Microbes Infect. 2010, 12:784-789.
3. Alves M.J., Colli W. Trypanosoma cruzi: adhesion to the host cell and intracellular survival. IUBMB Life 2007, 59:274-279.
4. Alves M.J., Colli W. Role of the gp85/trans-sialidase superfamily of glycoproteins in the interaction of Trypanosoma cruzi with host structures. Subcell. Biochem. 2008, 47:58-69.
5. Andrade L.O., Andrews N.W. Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. J. Exp. Med. 2004, 200:1135-1143.
6. Andrade L.O., Andrews N.W. The Trypanosoma cruzi-host-cell interplay: location, invasion, retention. Nat. Rev. Microbiol. 2005, 3:819-823.
7. Andrews N.W. Lysosomes and the plasma membrane: trypanosomes reveal a secret relationship. J. Cell Biol. 2002, 158:389-394.
8. Andrews N.W., Whitlow M.B. Secretion by Trypanosoma cruzi of a hemolysin active at low pH. Mol. Biochem. Parasitol. 1989, 33:249-256.
9. Andrews N.W., Abrams C.K., Slatin S.L., Griffiths G. A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 1990, 61:1277-1287.
10. Atwood J.A., Weatherly D.B., Minning T.A., Bundy B., Cavola C., Opperdoes F.R., et al. The Trypanosoma cruzi proteome. Science 2005, 309:473-476.
11. Barbabosa-Pliego A., Diaz-Albiter H.M., Ochoa-Garcia L., Aparicio-Burgos E., Lopez-Heydeck S.M., Velasquez-Ordonez V., et al. Trypanosoma cruzi circulating in the southern region of the tate of Mexico (Zumpahuacan) are pathogenic: a dog model. Am. J. Trop. Med. Hyg. 2009, 81:390-395.
12. Barr S.C., Dennis V.A., Klei T.R., Norcross N.L. Antibody and lymphoblastogenic responses of dogs experimentally infected with Trypanosoma cruzi isolates from North American mammals. Vet. Immunol. Immunopathol. 1991, 29:267-283.
13. Barrias E.M., Reignault L.C., de Souza W., Carvalho T.M. Dynasore, a dynamin inhibitor, inhibits Trypanosoma cruzi entry into peritoneal macrophages. PLoS One 2010, 5:1-11.
14. Bartholomeu D.C., Cerqueira G.C., Leao A.C., daRocha W.D., Pais F.S., Macedo C., et al. Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res. 2009, 37:3407-3417.
15. Benabdellah K., Gonzalez-Rey E., Gonzalez A. Alternative trans-splicing of the Trypanosoma cruzi LYT1 gene transcript results in compartmental and functional switch for the encoded protein. Mol. Microbiol. 2007, 65:1559-1567.
16. Benvenuti L.A., Roggerio A., Freitas H.F., Mansur A.J., Fiorelli A., Higuchi M.L. Chronic American trypanosomiasis: parasite persistence in endomyocardial biopsies is associated with high-grade myocarditis. Ann. Trop. Med. Parasitol. 2008, 102:481-487.
17. Bittencourt A.L., Vieira G.O., Tavares H.C., Mota E., Maguire J. Esophageal involvement in congenital Chagas' disease. Report of a case with megaesophagus. Am. J. Trop. Med. Hyg. 1984, 33:30-33.
18. Buckner F.S., Wilson A.J., Van Voorhis W.C. Detection of live Trypanosoma cruzi in tissues of infected mice by using histochemical stain for beta-galactosidase. Infect. Immun. 1999, 67:403-409.
19. Bulgin R., Raymond B., Garnett J.A., Frankel G., Crepin V.F., Berger C.N., et al. Bacterial guanine nucleotide exchange factors SopE-like and WxxxE effectors. Infect. Immun. 2010, 78:1417-1425.
20. Burleigh B.A. Host cell signaling and Trypanosoma cruzi invasion: do all roads lead to lysosomes?. Sci. STKE 2005, 293:pe36.
21. Burleigh B.A., Andrews N.W. A 120-kDa alkaline peptidase from Trypanosoma cruzi is involved in the generation of a novel Ca(2+)-signaling factor for mammalian cells. J. Biol. Chem. 1995, 270:5172-5180.
22. Burleigh B.A., Caler E.V., Webster P., Andrews N.W. A cytosolic serine endopeptidase from Trypanosoma cruzi is required for the generation of Ca2+ signaling in mammalian cells. J. Cell. Biol. 1997, 136:609-620.
23. Caler E.V., Vaena de Avalos S., Haynes P.A., Andrews N.W., Burleigh B.A. Oligopeptidase B-dependent signaling mediates host cell invasion by Trypanosoma cruzi. EMBO J. 1998, 17:4975-4986.
24. Caler E.V., Morty R.E., Burleigh B.A., Andrews N.W. Dual role of signaling pathways leading to Ca(2+) and cyclic AMP elevation in host cell invasion by Trypanosoma cruzi. Infect. Immun. 2000, 68:6602-6610.
25. Caler E.V., Chakrabarti S., Fowler K.T., Rao S., Andrews N.W. The exocytosis-regulatory protein synaptotagmin VII mediates cell invasion by Trypanosoma cruzi. J. Exp. Med. 2001, 193:1097-1104.
26. Calvet C.M., Meuser M., Almeida D., Meirelles M.N., Pereira M.C. Trypanosoma cruzi-cardiomyocyte interaction: role of fibronectin in the recognition process and extracellular matrix expression in vitro and in vivo. Exp. Parasitol. 2004, 107:20-30.
27. Caradonna K., Pereiraperrin M. Preferential brain homing following intranasal administration of Trypanosoma cruzi. Infect. Immun 2009, 77:2112-2119.
28. Cardoso C.M., Groth-Pedersen L., Hoyer-Hansen M., Kirkegaard T., Corcelle E., Andersen J.S., et al. Depletion of kinesin 5B affects lysosomal distribution and stability and induces peri-nuclear accumulation of autophagosomes in cancer cells. PLoS One 2009, 4:e4424.
29. Chakrabarti S., Kobayashi K.S., Flavell R.A., Marks C.B., Miyake K., Liston D.R., et al. Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J. Cell Biol. 2003, 162:543-549.
30. Chuenkova M.V., PereiraPerrin M. Chagas' disease parasite promotes neuron survival and differentiation through TrkA nerve growth factor receptor. J. Neurochem. 2004, 91:385-394.
31. Chuenkova M.V., PereiraPerrin M. Trypanosoma cruzi targets Akt in host cells as an intracellular antiapoptotic strategy. Sci. Signal. 2009, 2:ra74.
32. Claser C., Curcio M., de Mello S.M., Silveira E.V., Monteiro H.P., Rodrigues M.M. Silencing cytokeratin 18 gene inhibits intracellular replication of Trypanosoma cruzi in HeLa cells but not binding and invasion of trypanosomes. BMC Cell Biol. 2008, 9:68.
33. Cordero E.M., Nakayasu E.S., Gentil L.G., Yoshida N., Almeida I.C., da Silveira J.F. Proteomic analysis of detergent-solubilized membrane proteins from insect-developmental forms of Trypanosoma cruzi. J. Proteome Res. 2009, 8:3642-3652.
34. Costales J., Rowland E.C. A role for protease activity and host-cell permeability during the process of Trypanosoma cruzi egress from infected cells. J. Parasitol. 2007, 93:1350-1359.
35. Cross G.A., Takle G.B. The surface trans-sialidase family of Trypanosoma cruzi. Annu. Rev. Microbiol. 1993, 47:385-411.
36. de Carvalho T.M., de Souza W. Early events related with the behaviour of Trypanosoma cruzi within an endocytic vacuole in mouse peritoneal macrophages. Cell Struct. Funct. 1989, 14:383-392.
37. de Meirelles Mde N., de Araujo Jorge T.C., de Souza W., Moreira A.L., Barbosa H.S. Trypanosoma cruzi: phagolysosomal fusion after invasion into non professional phagocytic cells. Cell Struct. Funct. 1987, 12:387-393.
38. de Melo-Jorge M., PereiraPerrin M. The Chagas' disease parasite Trypanosoma cruzi exploits nerve growth factor receptor TrkA to infect mammalian hosts. 2007, 1:251-261.
39. De Souza W. Basic cell biology of Trypanosoma cruzi. Curr. Pharm. Des. 2002, 8:269-285.
40. Dorta M.L., Ferreira A.T., Oshiro M.E., Yoshida N. Ca2+ signal induced by Trypanosoma cruzi metacyclic trypomastigote surface molecules implicated in mammalian cell invasion. Mol. Biochem. Parasitol. 1995, 73:285-289.
41. Dzikowski R., Deitsch K.W. Genetics of antigenic variation in Plasmodium falciparum. Curr. Genet. 2009, 55:103-110.
42. El-Sayed N.M., Myler P.J., Bartholomeu D.C., Nilsson D., Aggarwal G., Tran A.N., et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005, 309:409-415.
43. Fernandes M.C., Cortez M., Geraldo Yoneyama K.A., Straus A.H., Yoshida N., Mortara R.A. Novel strategy in Trypanosoma cruzi cell invasion: implication of cholesterol and host cell microdomains. Int. J. Parasitol. 2007, 37:1431-1441.
44. Giordano R., Chammas R., Veiga S.S., Colli W., Maria Julia M.A. An acidic component of the heterogeneous Tc-85 protein family from the surface of Trypanosoma cruzi is a laminin binding glycoprotein. Mol. Biochem. Parasitol. 1994, 65:85-94.
45. Giordano R., Fouts D.L., Tewari D., Colli W., Manning J.E., Alves M.J. Cloning of a surface membrane glycoprotein specific for the infective form of Trypanosoma cruzi having adhesive properties to laminin. J. Biol. Chem. 1999, 274:3461-3468.
46. Hall B.F., Webster P., Ma A.K., Joiner K.A., 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. 1992, 176:313-325.
47. Harada A., Takei Y., Kanai Y., Tanaka Y., Nonaka S., Hirokawa N. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol. 1998, 141:51-59.
48. Heuser J. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 1989, 108:855-864.
49. Horn D. The molecular control of antigenic variation in Trypanosoma brucei. Curr. Mol. Med. 2004, 4:563-576.
50. Insel P.A., Head B.P., Patel H.H., Roth D.M., Bundey R.A., Swaney J.S. Compartmentation of G-protein-coupled receptors and their signalling components in lipid rafts and caveolae. Biochem. Soc. Trans. 2005, 33:1131-1134.
51. Jones E.M., Colley D.G., Tostes S., Lopes E.R., Vnencak-Jones C.L., McCurley T.L. Amplification of a Trypanosoma cruzi DNA sequence from inflammatory lesions in human chagasic cardiomyopathy. Am. J. Trop. Med. Hyg. 1993, 48:348-357.
52. Kahn S., Van Voorhis W.C., Eisen H. The major 85-kD surface antigen of the mammalian form of Trypanosoma cruzi is encoded by a large heterogeneous family of simultaneously expressed genes. J. Exp. Med. 1990, 172:589-597.
53. Kawashita S.Y., da Silva C.V., Mortara R.A., Burleigh B.A., Briones M.R. 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. 2009, 165:19-31.
54. Kima P.E., Burleigh B., Andrews N.W. Surface-targeted lysosomal membrane glycoprotein-1 (Lamp-1) enhances lysosome exocytosis and cell invasion by Trypanosoma cruzi. Cell. Microbiol. 2000, 2:477-486.
55. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 1989, 5:483-525.
56. Leite M.F., Moyer M.S., Andrews N.W. Expression of the mammalian calcium signaling response to Trypanosoma cruzi in Xenopus laevis oocytes. Mol. Biochem. Parasitol. 1998, 92:1-13.
57. Ley V., Robbins E., Nussenzweig V., Andrews N. The exit of Trypanosoma cruzi from the phagosome is inhibited by raising the pH of acidic compartments. J. Exp. Med. 1990, 171:401-413.
58. Maganto-Garcia E., Punzon C., Terhorst C., Fresno M. Rab5 activation by Toll-like receptor 2 is required for Trypanosoma cruzi internalization and replication in Macrophages. Traffic 2008, 9:1299-1315.
59. Magdesian M.H., Giordano R., Ulrich H., Juliano M.A., Juliano L., Schumacher R.I., et al. Infection by Trypanosoma cruzi. Identification of a parasite ligand and its host cell receptor. J. Biol. Chem. 2001, 276:19382-19389.
60. Magdesian M.H., Tonelli R.R., Fessel M.R., Silveira M.S., Schumacher R.I., Linden R., et al. A conserved domain of the gp85/trans-sialidase family activates host cell extracellular signal-regulated kinase and facilitates Trypanosoma cruzi infection. Exp. Cell Res. 2007, 313:210-218.
61. Malaga S., Yoshida N. Targeted reduction in expression of Trypanosoma cruzi surface glycoprotein gp90 increases parasite infectivity. Infect. Immun. 2001, 69:353-359.
62. Manning-Cela R., Cortes A., Gonzalez-Rey E., Van Voorhis W.C., Swindle J., Gonzalez A. LYT1 protein is required for efficient in vitro infection by Trypanosoma cruzi. Infect. Immun. 2001, 69:3916-3923.
63. Manning-Cela R., Gonzalez A., Swindle J. Alternative splicing of LYT1 transcripts in Trypanosoma cruzi. Infect. Immun. 2002, 70:4726-4728.
64. Marchiori P.E., Alexandre P.L., Britto N., Patzina R.A., Fiorelli A.A., Lucato L.T., et al. Late reactivation of Chagas' disease presenting in a recipient as an expansive mass lesion in the brain after heart transplantation of chagasic myocardiopathy. J. Heart Lung Transplant. 2007, 26:1091-1096.
65. Martinez I., Chakrabarti S., Hellevik T., Morehead J., Fowler K., Andrews N.W. Synaptotagmin VII regulates Ca2+-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 2000, 148:1141-1150.
66. Martins R.M., Covarrubias C., Rojas R.G., Silber A.M., Yoshida N. Use of L-proline and ATP production by Trypanosoma cruzi metacyclic forms as requirements for host cell invasion. Infect. Immun. 2009, 77:3023-3032.
67. Melo-Jorge M., Pereira P.M. The Chagas' disease parasite Trypanosoma cruzi exploits nerve growth factor receptor TrkA to infect mammalian hosts. Cell Host Microbe 2007, 14:251-261.
68. Miles M.A., Llewellyn M.S., Lewis M.D., Yeo M., Baleela R., Fitzpatrick S., et al. The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology 2009, 136:1509-1528.
69. Ming M., Chuenkova M., Ortega-Barria E., Pereira M.E.A. Mediation of Trypanosoma cruzi invasion by sialic acid on the host cell and trans-sialidase on the trypanosome. Mol. Biochem. Parasitol. 1993, 59:243-252.
70. Ming M., Ewen M.E., Pereira M.E. Trypanosome invasion of mammalian cells requires activation of the TGF beta signaling pathway. Cell 1995, 82:287-296.
71. Minning T.A., Weatherly D.B., Atwood J., Orlando R., Tarleton R.L. The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 2009, 10:370.
72. Montalvo-Hicks L.D., Trevenen C.L., Briggs J.N. American trypanosomiasis (Chagas' disease) in a Canadian immigrant infant. Pediatrics 1980, 66:266-268.
73. Monteon-Padilla V., Hernandez-Becerril N., Ballinas-Verdugo M.A., Aranda-Fraustro A., Reyes P.A. Persistence of Trypanosoma cruzi in chronic chagasic cardiopathy patients. Arch. Med. Res. 2001, 32:39-43.
74. Moreno S.N., Silva J., Vercesi A.E., Docampo R. Cytosolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. J. Exp. Med. 1994, 180:1535-1540.
75. Morrison W.I. Progress towards understanding the immunobiology of Theileria parasites. Parasitology 2009, 136:1415-1426.
76. Mortara R.A., da Silva S., Patricio F.R., Higuchi M.L., Lopes E.R., Gabbai A.A., et al. Imaging Trypanosoma cruzi within tissues from chagasic patients using confocal microscopy with monoclonal antibodies. Parasitol. Res. 1999, 85:800-808.
77. Nagajyothi F., Weiss L.M., Silver D.L., Desruisseaux M.S., Scherer P.E., Herz J., et al. Trypanosoma cruzi utilizes the host low density lipoprotein receptor in invasion. Plos Negl. Trop. Dis. 2011, 5:e953.
78. Nakata T., Hirokawa N. Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J. Cell Biol. 1995, 131:1039-1053.
79. Nogueira N., Cohn Z. Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. J. Exp. Med. 1976, 143:1402-1420.
80. Ouaissi M.A., Afchain D., Capron A., Grimaud J.A. Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature 1984, 308:380-382.
81. Pereira M.E., Zhang K., Gong Y., Herrera E.M., Ming M. Invasive phenotype of Trypanosoma cruzi restricted to a population expressing trans-sialidase. Infect. Immun. 1996, 64:3884-3892.
82. Pereira-Chioccola V.L., Acosta-Serrano A., Correia de Almeida I., Ferguson M.A., Souto-Padron 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. 2000, 113(Pt. 7):1299-1307.
83. Prioli R.P., Rosenberg I., Pereira M.E. High- and low-density lipoproteins enhance infection of Trypanosoma cruzi in vitro. Mol. Biochem. Parasitol. 1990, 38(2):191-198.
84. Ramirez M.I., Ruiz Rde C., Araya J.E., Da Silveira J.F., Yoshida N. Involvement of the stage-specific 82-kilodalton adhesion molecule of Trypanosoma cruzi metacyclic trypomastigotes in host cell invasion. Infect. Immun. 1993, 61:3636-3641.
85. Reddy A., Caler E.V., Andrews N.W. Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes. Cell 2001, 106:157-169.
86. Rodriguez A., Rioult M.G., Ora A., Andrews N.W. A trypanosome-soluble factor induces IP3 formation, intracellular Ca2+ mobilization and microfilament rearrangement in host cells. J. Cell Biol. 1995, 129:1263-1273.
87. Rodriguez A., Samoff E., Rioult M.G., Chung A., Andrews N.W. Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J. Cell Biol. 1996, 134:349-362.
88. Rodriguez A., Martinez I., Chung A., Berlot C.H., Andrews N.W. cAMP regulates Ca2+-dependent exocytosis of lysosomes and lysosome-mediated cell invasion by Trypanosomes. J. Biol. Chem. 1999, 274:16754-16759.
89. Romano P.S., Arboit M.A., Vazquez C.L., Colombo M.I. The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell. Autophagy 2009, 5(1):6-18.
90. Ropolo A.S., Touz M.C. A lesson in survival, by Giardia lamblia. ScientificWorldJournal 2010, 10:2019-2031.
91. Rubin-de-Celis S.S.C., Uemura H., Yoshida N., Schenkman S. Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cell. Microbiol. 2006, 8:1888-1898.
92. Ruiz R.C., Favoreto S., Dorta M.L., Oshiro M.E., Ferreira A.T., Manque P.M., et al. Infectivity of Trypanosoma cruzi strains is associated with differential expression of surface glycoproteins with differential Ca2+ signalling activity. Biochem. J. 1998, 330(Pt. 1):505-511.
93. Santos M.A., Garg N., Tarleton R. The identification and molecular characterization of Trypanosoma cruzi amastigote surface protein-1, a member of the trans-sialidase gene super-family. Mol. Biochem. Parasitol. 1997, 86:1-11.
94. Sartori A.M., Lopes M.H., Caramelli B., Duarte M.I., Pinto P.L., Neto V., et al. Simultaneous occurrence of acute myocarditis and reactivated Chagas' disease in a patient with AIDS. Clin. Infect. Dis. 1995, 21:1297-1299.
95. Scharfstein J., Lima A.P. Roles of naturally occurring protease inhibitors in the modulation of host cell signaling and cellular invasion by Trypanosoma cruzi. Subcell. Biochem. 2008, 47:140-154.
96. Scharfstein J., Schmitz V., Morandi V., Capella M.M.A., Lima A.P.C.A., Morrot A., et al. Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B2 receptors. J. Exp. Med. 2000, 192:1289-1300.
97. Schenkman S., Robbins E.S., Nussenzweig V. Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infect. Immun. 1991, 59:645-654.
98. Schenkman S., Pontes de Carvalho L., Nussenzweig V. Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. J. Exp. Med. 1992, 175:567-575.
99. Simonsen A., Tooze S.A. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 2009, 186:773-782.
100. Staquicini D.I., Martins R.M., Macedo S., Sasso G.R., Atayde V.D., Juliano M.A., et al. Role of GP82 in the selective binding to gastric mucin during oral infection with Trypanosoma cruzi. PLoS Negl. Trop. Dis. 2010, 4:e613.
101. Taketo M., Yokoyama S., Kimura Y., Higashida H. Ca2+ release and Ca2+ influx in Chinese hamster ovary cells expressing the cloned mouse B2 bradykinin receptor: tyrosine kinase inhibitor-sensitive and -insensitive processes. Biochim. Biophys. Acta 1996, 1355:89-98.
102. Tanida I. Autophagy basics. Microbiol. Immunol. 2011, 55:1-11.
103. Tanowitz H., Wittner M., Kress Y., Bloom B. Studies of in vitro infection by Trypanosoma cruzi. Ultrastructural studies on the invasion of macrophages and L-cells. Am. J. Trop. Med. Hyg. 1975, 24:25-33.
104. 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 1992, 71:1117-1130.
105. Tardieux I., Nathanson M.H., Andrews N.W. Role in host cell invasion of Trypanosoma cruzi-induced cytosolic-free Ca2+ transients. J. Exp. Med. 1994, 179:1017-1022.
106. Todorov A.G., Andrade D., Pesquero J.B., Araujo R.C., Bader M., et al. Trypanosoma cruzi induces edematogenic responses in mice and invades cardiomyocytes and endothelial cells in vitro by activating distinct kinin receptor (B1/B2) subtypes. FASEB J. 2003, 17:73-75.
107. Tonelli R.R., Giordano R.J., Barbu E.M., Torrecilhas A.C., Kobayashi G.S., Langley R.R., et al. 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. 2010, 4:e864.
108. Tyler K.M., Luxton G.W., Applewhite D.A., Murphy S.C., Engman D.M. Responsive microtubule dynamics promote cell invasion by Trypanosoma cruzi. Cell. Microbiol. 2005, 7:1579-1591.
109. Ulrich H., Magdesian M.H., Alves M.J., Colli W. In vitro selection of RNA aptamers that bind to cell adhesion receptors of Trypanosoma cruzi and inhibit cell invasion. J. Biol. Chem. 2002, 277:20756-20762.
110. Voss T.S., Healer J., Marty A.J., Duffy M.F., Thompson J.K., Beeson J.G., et al. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 2006, 439:1004-1008.
111. Weinkauf C., Pereiraperrin M. Trypanosoma cruzi promotes neuronal and glial cell survival through the neurotrophic receptor TrkC. Infect. Immun. 2009, 77:1368-1375.
112. Weston D., Patel B., Van Voorhis W.C. Virulence in Trypanosoma cruzi infection correlates with the expression of a distinct family of sialidase superfamily genes. Mol. Biochem. Parasitol. 1999, 98:105-116.
113. Wilkowsky S.E., Barbieri M.A., Stahl P., Isola E.L.D. Trypanosoma cruzi: phosphatidylinositol 3-kinase and protein kinase B activation is associated with parasite invasion. Exp. Cell Res. 2001, 264:211-218.
114. Woolsey A.M., Burleigh B.A. Host cell actin polymerization is required for cellular retention of Trypanosoma cruzi and early association with endosomal/lysosomal compartments. Cell. Microbiol. 2004, 6:829-838.
115. Woolsey A.M., Sunwoo L., Petersen C.A., Brachmann S.M., Cantley L.C., Burleigh B.A. Novel PI 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. J. Cell Sci. 2003, 116:3611-3622.
116. Yang Z., Klionsky D.J. Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 2010, 22:124-131.
117. Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. An. Acad. Bras. Cienc. 2006, 78:87-111.
118. Yoshida N. Molecular mechanisms of Trypanosoma cruzi infection by oral route. Mem. Inst. Oswaldo Cruz 2009, 104(Suppl. 1):101-107.
119. Yoshida N., Cortez M. Trypanosoma cruzi: parasite and host cell signaling during the invasion process. Subcell. Biochem. 2008, 47:82-91.
120. Zhang L., Tarleton R.L. Parasite persistence correlates with disease severity and localization in chronic Chagas' disease. J. Infect. Dis. 1999, 180:480-486.
121. Zhang J., Andrade Z.A., Yu Z.X., Andrade S.G., Takeda K., Sadirgursky M., et al. Apoptosis in a canine model of acute Chagasic myocarditis. J. Mol. Cell. Cardiol. 1999, 31:581-596.