Signaling pathways in Trypanosoma cruzi that modulate host cell interaction

Open Parasitology Journal

Volumn 4, Issue SPEC. ISS.1, 2010, Pages 77-83

  Alves, Maria Júlia Manso ^a   Colli, Walter ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Invasion; Kinases; Phosphatases; Signaling pathways; Trypanosoma

Indexed keywords

CELL RECEPTOR; GLYCOPROTEIN; GLYCOPROTEIN 85; MUCIN; PHOSPHATASE; PROTEIN KINASE; SIALIDASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL INTERACTION; CELL INVASION; CHAGAS DISEASE; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; GENOME; HOST CELL; HOST PARASITE INTERACTION; HUMAN; MULTIGENE FAMILY; NONHUMAN; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; PSEUDOGENE; SIGNAL TRANSDUCTION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE;

TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 84864009578     PISSN: None     EISSN: 18744214     Source Type: Journal    
DOI: 10.2174/1874421401004010077     Document Type: Article

References (90)

1. Chagas C. Nova tripanozomiaze humana. Mem Inst Oswaldo Cruz 1909; 1:11-72.
2. Zingales B, Andrade SG, Briones MRS, et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends Tc I to Tc VI. Mem Inst Oswaldo Cruz 2009; 104:1051-54.
3. Moncayo A, Silveira AC. Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Mem Inst Oswaldo Cruz 2009; 104: 17-30.
4. Williams-Blangero S, VandeBerg JL, Blangero J, Correa-Oliveira R. Genetic epidemiology of Trypanosoma cruzi infection and Chagas' disease. Front Biosci 2003; 8: 337-45.
5. Marinho CRF, Bucci DZ, Dagli MLZ, et al. Pathology affects different organs in two mouse strains chronically infected by a Trypanosoma cruzi clone: a model for genetic studies of Chagaśdisease. Infect Immun 2004; 72: 2350-57.
6. Piacenza L, Alvarez MN, Peluffo G, Radi R. Fighting the oxidative assault: the Trypanosoma cruzi journey to infection. Cur Opin Microbiol 2009; 12: 415-21.
7. Piacenza L, Zago MP, Peluffo G, Alvarez MN, Basombrio MA, Radi R. Enzymes of the antioxidant network as novel determiners of Trypanosoma cruzi virulence. Int J Parasitol 2009; 39: 1455-64.
8. Andrade LO, Andrews NW. The Trypanosoma cruzi host cell interplay: location, invasion and retention. Nat Rev Microbiol 2005; 3: 819-23.
9. Burleigh BA. Host cell signaling in Trypanosoma cruzi invasion: do all roads lead to lysosomes? Sci STEK 2005; 293: p. 36.
10. Schenkman S, Robbins ES, 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: 645-54.
11. Hall BF, Webster P, Ka MA, Joiner KA, Andrews NW. Desialylation of lysosomal membrane glycoprotein by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm. J Exp Med 1992; 176: 313-25.
12. Almeida-de-Faria M, Freymuller E, Colli W, Alves MJM. Trypanosoma cruzi: Characterization of an intracellular epimastigote- like form. Exp Parasitol 1999; 92: 263-74.
13. Tonelli RR, Silber AM, Almeida-de-Faria M, Hirata IY, Colli W, Alves MJM. L-Proline is essential for the intracellular differentiation of Trypanosoma cruzi. Cell Microbiol 2004; 6: 733-41.
14. Silber AM, Tonelli RR, Lopes CG, et al. Glucose uptake in the mammalian stages of Trypanosoma cruzi. Mol Biochem Parasitol 2009; 168: 102-08.
15. Silber AM, Colli W, Ulrich H, Alves MJM, Pereira CA. Amino acid metabolic routes in Trypanosoma cruzi: possible therapeutic targets against Chagaśdisease. Curr Drugs Targets Infect Disord 2005; 5: 53-64.
16. Coimbra VC, Yamamoto D, Khusal KG, et al. Enucleated L929 cells support invasion, differentiation, and multiplication of Trypanosoma cruzi parasites. Infect Immun 2007; 75: 3700-06.
17. Costales JA, Daily JP, Burleigh BA. Cytokine-dependent and - independent gene expression changes and cell cycle block revealed in Trypanosoma cruzi-infected host cells by comparative mRNA profiling. BMC Genomics 2009; 10: 252-69.
18. Mortara RA, Andreoli WK, Fernandes MC, et al. Host cell actin remodeling response to Trypanosoma cruzi: trypomastigote versus amastigote entry. Subcell Biochem 2008; 47: 101-09.
19. Moreno SNJ, Silva J, Vercesi AE. Cytosolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. J Exp Med 1994; 180: 1535-40.
20. Burleigh BA, Woolsey AM. Cell signaling and Trypanosoma cruzi invasion. Cell Microbiol 2002; 4: 701-11.
21. Alves MJM, Colli W. Trypanosoma cruzi: adhesion to the host cell and intracellular survival. IUMB Life 2007; 59: 274-79.
22. Alves MJM, Mortara R. A century of research: what we learned about the interaction of Trypanosoma cruzi with host cells? Mem Inst Oswaldo Cruz 2009; 104: 76-88.
23. Villalta F, Scharfstein J, Ashton AW, et al. Perspectives on the Trypanosoma cruzi-host cell receptor interactions. Parasitol Res 2009; 104: 1251-60.
24. Gonçalves MF, Umezawa ES, Katzin AM, et al. Trypanosoma cruzi: shedding of surface antigens as membrane vesicles. Exp Parasitol 1991; 72: 43-53.
25. Torrecilhas ACT, Tonelli RR, Pavanelli WR, et al. Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate intense inflammatory response. Microbes Infect 2009; 11: 29-39.
26. Frasch AC. Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today 2000; 16: 282-86.
27. De Lederkeremer RM, Agusti R. Glycobiology of Trypanosoma cruzi. Adv Carbohydr Chem Biochem 2009; 62: 311-66.
28. El-Sayed NM, Myler PJ, Bartholomeu DC, et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005; 309: 409-15.
29. Buscaglia CA, Campo VA, Frasch ACC, Di Noia JM. Trypanosoma surface mucins: host dependent coat diversity. Nat Rev Microbiol 2006; 4: 229-36.
30. Schenkman S, Eichinger D, Pereira MEA, Nussensweig V. Structural and functional properties of trypanosome trans-sialidase. Ann Rev Microbiol 1994; 48: 499-532.
31. Yoshida N. Trypanosoma cruzi infection by oral route. How the interplay between parasite and host components modulates infectivity. Parasitol Int 2008; 57: 105-09.
32. Jacobs T, Erdmann H, Fleischer B. Molecular interaction of Siglecs (sialic acid-binding Ig-like lectins) with sialylated ligands on Trypanosoma cruzi. Eur J Cell Biol 2010; 89: 113-16.
33. Mucci J, Risso MG, Leguizamón MS, Frasch ACC, Campetella O. The trans-sialidase from Trypanosoma cruzi triggers apoptosis by target cell sialylation. Cell Microbiol 2006; 8: 1086-95.
34. Palenchar JB, Bellofatto V. Gene transcription in trypanosomes. Mol Biochem Parasitol 2006; 146: 135-41.
35. Noé G, de Gaudenzi JG, Frasch AC. Functionally related transcripts have common RNA motifs for specific RNA-binding proteins in trypanosomes. BMC Mol Biol 2008; 9: 107.
36. Abuin G, Freitas-Junior LH, Colli W, Alves MJM, Schenkman S. Expression of trans-sialidase and 85kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post- transcriptional level by labile protein factors. J Biol Chem 1999; 274: 13041-47.
37. Gentil LG, Cordero EM, do Carmo MS, dos Santos MRM, da Silveira JF. Posttranscriptional mechanisms involved in the control of expression of the stage-specific GP82 surface glycoprotein in Trypanosoma cruzi. Acta Trop 2009; 109: 152-58.
38. Giordano R, Fouts D, Tewari D, Colli W, Manning J, Alves MJM. Cloning of a surface membrane glycoprotein specific for the infective form of Trypanosoma cruzi having adhesive properties to laminin. J Biol Chem 1999; 274: 3461-68.
39. Marroquin-Quelopana M, Oyama S, Pertinhez TA, et al. Modeling the Trypanosoma cruzi Tc85-11 protein mapping the laminin- binding site. Biochem Biophys Res Commun 2004; 325: 612-18.
40. Magdesian MH, Giordano R, Ulrich H, et al. Infection by Trypanosoma cruzi: identification of a parasite ligand and its host- cell receptor. J Biol Chem 2001; 276: 19382-89.
41. Magdesian MH, Tonelli RR, Fessel MR, 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: 210-18.
42. Dias WB, Fajardo FD, Graça-Souza AV, et al. Endothelial cell signaling induced by trans-sialidase from Trypanosoma cruzi. Cell Microbiol 2008; 10: 88-99.
43. Chuenkova MV, Pereira M. A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Mol Biol Cell 2000; 11:1487-98.
44. Chuenkova MV, Furnari FB, Cavenee WK, Pereira M. 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 USA 2001; 98: 9936-41.
45. Chuenkova MV, PereiraPerrin M. A synthetic peptide modeled on PDNF, Chagaśdisease parasite neutrophic factor, promotes survival and differentiation of neuronal cells through TrkA receptor. Biochemistry 2005; 44: 15685-94.
46. Melo-Jorge M, PereiraPerrin M. The Chagaśdisease parasite Trypanosoma cruzi exploits nerve growth factor receptor TrkA to infect mammalian hosts. Cell Host Microbe 2007; 1: 251-61.
47. Coura JR. Transmission of chagasic infection by oral route in the natural history of Chagas'disease. Rev Soc Bras Med Trop 2006; 39: 113-17.
48. Mendonça-Previato L, Todeschini AR, Heise N, Previato JO. Protozoan parasite-specific carbohydrate structures. Curr Opin Struct Biol 2005; 15: 499-05.
49. Ropert C, Ferreira LR, Campos MA, et al. Macrophage signaling by glycosylphosphatidylinositol-anchored mucin-like glycoproteins derived from Trypanosoma cruzi trypomastigotes. Microbes Infect 2002; 4: 41015-25.
50. Campos MA, Gazzinelli RT. Trypanosoma cruzi and its components as exogenous mediators of inflammation recognized through Toll-like receptors. Mediators Inflamm 2004; 13: 139-43.
51. Nogueira NFS, Gonzalez MS, Gomes JE, et al. Trypanosoma cruzi: involvement of glycoinositolsphospholipids in the attachment to the luminal midgut surface of Rhodnius prolixus. Exp Parasitol 2007; 116: 120-28.
52. + signaling activity. Biochem J 1998; 330: 505-11.
53. Turner CW, Lima MF, Villalta F. Trypanosoma cruzi uses a 45- kDa mucin for adhesion to mammalian cells. Biochem Biophys Res Commun 2002; 290: 29-34.
54. Yoshida N, Dorta ML, Ferreira AT, et al. Removal of sialic acid from mucin-like surface molecules of Trypanosoma cruzi metacyclic trypomastigotes enhances parasite-host cell interaction. Mol Biochem Parasitol 1997; 84: 57-67.
55. Vray B, Camby I, Vercruysse V, et al. Up-regulation of galectin-3 and its ligands by Trypanosoma cruzi infection with modulation of adhesion and migration of murine dendritic cells. Glycobiology 2004; 14: 647-57.
56. Ulrich H, Magdesian MH, Alves MJM, 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: 20756-62.
57. Ouaissi MA, Afchain D, Capron. Fibronectin receptors on Trypanosoma cruzi trypomastigotes and their biological function. Nature 1984; 308: 380-2.
58. Simmons KJ, Nude PN, Kleschchenko YY, Lima MF, Villalta F. Stable RNA interference of host thrombospondin-1 blocks Trypanosoma infection. FEBS Lett 2006; 580: 2365-70.
59. Moody T, Ochieng J, Villalta F. Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix- mediated by human galectin-3. FEBS Lett 2000; 470: 305-08.
60. Nde PN, Simmons KJ, Kleshchenko YY, Pratap S, Lima MF, Villalta F. Silencing of the laminin gamma-1 gene blocks Trypanosoma cruzi infection. Infect Immun 2006; 74: 1643-8.
61. Herrera EM, Ming M, Ortega-Barria E, Pereira ME. Mediation of Trypanosoma cruzi invasion by heparan sulfate receptors on host cells and penetrin counterreceptors on the trypanosomes. Mol Biochem Parasitol 1994; 65: 73-83.
62. Calvet CM, Toma L, de Souza FR, Meirelles MNL, Pereira MCS. Heparan sulfate proteoglycans mediate the invasion of cardiomyocytes by Trypanosoma cruzi. J Eukaryot Microbiol 2003; 50: 97-103.
63. Oliveira Jr FOR, Alves CR, Calvet CM, et al. Trypanosoma cruzi heparin-binding proteins and the nature of the host cell heparin sulfate-binding domain. Microb Pathog 2008; 44: 329-38.
64. Andrade SG, Grimaud JA, Stocker-Guerret S. Sequential change of the connective matrix components of the myocardium (fibronectin and laminin) and evolution of cardiac fibrosis in mice infected with Trypanosoma cruzi. Am J Trop Med Hyg 1989; 40: 252-60.
65. Pinho RT, Vannier-Santos MA, Alves CR, Marino APMP, Castello Branco LRR, Lannes-Vieira J. Effect of Trypanosoma cruzi re- leased antigens binding to non-infected cells on anti-parasite antibody recognition and expression of extracellular matrix components. Acta Trop 2002; 83: 103-15.
66. Garzoni LR, Adesse D, Soares MJ, Rossi MID, Borojevic R, Meirelles MNL. Fibrosis and hypertrophy induced by Trypanosoma cruzi in a three-dimensional cardiomyocyte- culture system. J Infec Dis 2008; 197: 906-15.
67. Calvet CM, Oliveira Jr FOR, Araujo-Jorge TC, Pereira MCS. Regulation of extracellular matrix expression and distribution in Trypanosoma cruzi- infected cardiomyocytes. Int J Med Microbiol 2009; 299: 301-12.
68. Araújo-Jorge TC, Waghabi MC, Soieiro M, Keramidas M, Bailly S, Feige JJ. Pivotal role of TGF- in infectious heart disease: the case of Trypanosoma cruzi infection and consequent Chagasic myocardiopathy. Cytokine Growth Factor Rev 2008; 19: 405-13.
69. Waghabi MC, Keramidas M, Bailly S, et al. Uptake of host cell transforming growth factor-beta by Trypanosoma cruzi amastigotes in cardiomyocytes: potential role in parasite cycle completion. Am J Pathol 2005; 167: 993-1003.
70. Waghabi MC, Keramidas M, Calvet CM, et al. SB-431542, a transforming growth factor beta inhibitor, impairs Trypanosoma cruzi infection in cardiomyocytes and parasite cycle completion. Antimicrob Agents Chemother 2007; 51: 2905-10.
71. Waghabi MC, de Souza EM, de Oliveira GM, et al. Pharmacological inhibition of transforming growth factor signaling decreases infection and prevents heart damage in acute Chagaśdisease. Antimicrob Agents Chemother 2009; 53: 4694-701.
72. Parsons M, Worthey EA, Ward PN, Mottram JC. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 2005; 6: 127.
73. Brenchley R, Tariq H, McElhinney H, et al. The TriTryp phosphatoma: analysis of the protein phosphatase catalytic domains. BMC Genomics 2007; 8: 434.
74. Wiese M. Leishmania MAP Kinases- Familiar proteins in an unusual context. Int J Parasitol 2007; 37: 1053-62.
75. Bahia D, Oliveira LM, Lima FM, et al. The TryPIkinome of five human pathogenic trypanosomatids: Trypanosoma brucei, Trypanosoma cruzi, Leishmania major, Leishmania braziliensis and Leishmania infantum- New tools for designing specific inhibitors. Biochem Biophys Res Commun 2009; 390: 963-70.
76. Kutuzov MA, Andreeva A. Protein Ser/Thr phosphatases of parasitic protozoa. Mol Biochem Parasitol 2008; 161: 81-90.
77. Andreeva AV, Kutuzov MA. Protozoan protein tyrosine phosphatases. Int J Parasitol 2008; 38: 1279-95.
78. Laxman S, Beavo JA. Cyclic nucleotide signaling mechanisms in trypanosomes: possible targets for therapeutic agents. Mol Interv 2007; 7: 203-15.
79. Field MC, ÓReilly AJ. How complex is GTPase signaling in trypanosomes? Trends Parasitol 2008; 24: 243-57.
80. Routureau B, Morales MA, Basin P, Spath GF. The flagellum- mitogen-activated protein kinase connection in Trypanosomatids: a key sensory role in parasite signaling and development? Cell Microbiol 2009; 11: 710-18.
81. Szoor B, Ruberto I, Burchmore R, Matthews KR. A novel phosphatase cascade regulates differentiation in Trypanosoma brucei via a glycosomal signaling pathway. Genes Dev 2010; 24: 1306-16.
82. Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci 2009; 122: 3589-94
83. Madeira da Silva L, Beverley SM. Expansion of the target of rapamycin (TOR) kinase family and function in Leishmania shows that TOR3 is required for acidocalcisome biogenisis and animal infectivity. Proc Natl Acad Sci USA 2010; 29: 11965-70.
84. Barquilla A, Crespo JL, Navarro M. Rapamycin inhibits trypanosome cell growth by preventing TOR complex 2 formation. Proc Natl Acad Sci USA 2008; 105: 14579-84.
85. De Jesus TCL, Tonelli RR, Nardelli SC, et al. Tor-like 1 kinase is involved in the control of polyphosphate levels and acidocalcisome maintenance in Trypanosoma brucei. J Biol Chem 2010; 285: 24131-40.
86. Araya JE, Cornejo A, Orrego PR, et al. Calcineurin B of the human protozoa parasite Trypanosoma cruzi is involved in cell invasion. Microbe Infect 2008; 10: 892-900.
87. Moreno VR, Aguero F, Tekiel V, Sanchez DO. The calcineurin A homologue from Trypanosoma cruzi lacks two important regulatory domains. Acta Trop 2007; 101: 80-9.
88. Ulrich H, Wrenger C. Disease- specific biomarker discovery by aptamers. Cytometry A 2009; 75A: 727-33.
89. Gamo F-J, Sanz LM, Vidal J, et al. Thousands of chemical starting points for antimalarial lead identification. Nature 2010; 465: 305-10.
90. Costa-Junior HM, Suetsugu MJ, Krieger JE, Schechtman D. Specific modulation of protein kinase activity via small peptides. Regul Pept 2009; 153: 11-18.