- Introduction
- Materials and Methods
- Recombinant TcCRT (rTcCRT).
- Polyclonal antibodies.
- Monoclonal antibody.
- Cell culture.
- Parasites.
- TEM.
- Immunocytochemistry.
- Immunocytochemical procedures for CRT detection.
- Quantification of label density generated by polyclonal antibodies.
- Quantification of TcCRT molecules in kinetoplast sections.
- ELISA.
- Detection of positive cells for MHC class I antigens by flow cytometry.
- Flow cytometry data analysis.
- Statistical analysis.
- Results
- Discussion
- Conclusions
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Clayton J, 2010. Chagas disease 101. Nature 465: S4–S5.
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2.
Clayton J, 2010. Chagas disease: pushing through the pipeline. Nature 465: S12–S15.
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Coura JR, Vinas PA, 2010. Chagas disease: a new worldwide challenge. Nature 465: S6–S7.
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4.
Tyler KM, Engman DM, 2001. The life cycle of Trypanosoma cruzi revisited. Int J Parasitol 31: 472–481.
-
5.
Ramirez G, Valck C, Molina MC, Ribeiro CH, Lopez N, Sanchez G, Ferreira VP, Billetta R, Aguilar L, Maldonado I, Cattan P, Schwaeble W, Ferreira A, 2011. Trypanosoma cruzi calreticulin: a novel virulence factor that binds complement C1 on the parasite surface and promotes infectivity. Immunobiology 216: 265–273.
-
6.
Ferreira V, Molina MC, Valck C, Rojas A, Aguilar L, Ramirez G, Schwaeble W, Ferreira A, 2004. Role of calreticulin from parasites in its interaction with vertebrate hosts. Mol Immunol 40: 1279–1291.
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7.
Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M, 1999. Calreticulin: one protein, one gene, many functions. Biochem J 344: 281–292.
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Sonnichsen B, Fullekrug J, Nguyen Van P, Diekmann W, Robinson DG, Mieskes G, 1994. Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J Cell Sci 107: 2705–2717.
-
9.
Souto-Padron T, Labriola CA, de Souza W, 2004. Immunocytochemical localization of calreticulin in Trypanosoma cruzi. Histochem Cell Biol 122: 563–569.
-
10.
Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, Opas M, MacLennan DH, Michalak M, 1999. Calreticulin is essential for cardiac development. J Cell Biol 144: 857–868.
-
11.
Ferreira V, Valck C, Sanchez G, Gingras A, Tzima S, Molina MC, Sim R, Schwaeble W, Ferreira A, 2004. The classical activation pathway of the human complement system is specifically inhibited by calreticulin from Trypanosoma cruzi. J Immunol 172: 3042–3050.
-
12.
Valck C, Ramirez G, Lopez N, Ribeiro CH, Maldonado I, Sanchez G, Ferreira VP, Schwaeble W, Ferreira A, 2010. Molecular mechanisms involved in the inactivation of the first component of human complement by Trypanosoma cruzi calreticulin. Mol Immunol 47: 1516–1521.
-
13.
Ramirez G, Valck C, Ferreira VP, Lopez N, Ferreira A, 2012. Extracellular Trypanosoma cruzi calreticulin in the host-parasite interplay. Trends Parasitol 27: 115–122.
-
14.
Sosoniuk E, Vallejos G, Kenawy H, Gaboriaud C, Thielens N, Fujita T, Schwaeble W, Ferreira A, Valck C, 2014. Trypanosoma cruzi calreticulin inhibits the complement lectin pathway activation by direct interaction with L-ficolin. Mol Immunol 60: 80–85.
-
15.
Lopez NC, Valck C, Ramirez G, Rodriguez M, Ribeiro C, Orellana J, Maldonado I, Albini A, Anacona D, Lemus D, Aguilar L, Schwaeble W, Ferreira A, 2010. Antiangiogenic and antitumor effects of Trypanosoma cruzi calreticulin. PLoS Negl Trop Dis 4: e730.
-
16.
Molina MC, Ferreira V, Valck C, Aguilar L, Orellana J, Rojas A, Ramirez G, Billetta R, Schwaeble W, Lemus D, Ferreira A, 2005. An in vivo role for Trypanosoma cruzi calreticulin in antiangiogenesis. Mol Biochem Parasitol 140: 133–140.
-
17.
Ferreira V, Molina MC, Schwaeble W, Lemus D, Ferreira A, 2005. Does Trypanosoma cruzi calreticulin modulate the complement system and angiogenesis? Trends Parasitol 21: 169–174.
-
18.
Sanchez Valdez FJ, Perez Brandan C, Zago MP, Labriola C, Ferreira A, Basombrio MA, 2013. Trypanosoma cruzi carrying a monoallelic deletion of the calreticulin (TcCRT) gene are susceptible to complement mediated killing and defective in their metacyclogenesis. Mol Immunol 53: 198–205.
-
19.
Sanchez-Valdez FJ, Perez Brandan C, Ramirez G, Uncos AD, Zago MP, Cimino RO, Cardozo RM, Marco JD, Ferreira A, Basombrio MA, 2014. A monoallelic deletion of the TcCRT gene increases the attenuation of a cultured Trypanosoma cruzi strain, protecting against an in vivo virulent challenge. PLoS Negl Trop Dis 8: e2696.
-
20.
Aguillon JC, Ferreira L, Perez C, Colombo A, Molina MC, Wallace A, Solari A, Carvallo P, Galindo M, Galanti N, Orn A, Billetta R, Ferreira A, 2000. Tc45, a dimorphic Trypanosoma cruzi immunogen with variable chromosomal localization, is calreticulin. Am J Trop Med Hyg 63: 306–312.
-
21.
Aguilar L, Ramirez G, Valck C, Molina MC, Rojas A, Schwaeble W, Ferreira V, Ferreira A, 2005. F(ab′)2 antibody fragments against Trypanosoma cruzi calreticulin inhibit its interaction with the first component of human complement. Biol Res 38: 187–195.
-
22.
Aguillon JC, Harris R, Molina MC, Colombo A, Cortes C, Hermosilla T, Carreno P, Orn A, Ferreira A, 1997. Recognition of an immunogenetically selected Trypanosoma cruzi antigen by seropositive chagasic human sera. Acta Trop 63: 159–166.
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Kohler G, Milstein C, 1975. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495–497.
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Mancino L, Rizvi SM, Lapinski PE, Raghavan M, 2002. Calreticulin recognizes misfolded HLA-A2 heavy chains. Proc Natl Acad Sci USA 99: 5931–5936.
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Saito Y, Ihara Y, Leach MR, Cohen-Doyle MF, Williams DB, 1999. Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J 18: 6718–6729.
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Trypanosoma cruzi Calreticulin Topographical Variations in Parasites Infecting Murine Macrophages
Andrea González
Andrea González
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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Carolina Valck
Carolina Valck
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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Gittith Sánchez
Gittith Sánchez
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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Steffen Härtel
Steffen Härtel
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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Jorge Mansilla
Jorge Mansilla
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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Galia Ramírez
Galia Ramírez
Programa Disciplinario de Inmunología, Programa de Genética Humana, Programa de Biología Celular y Molecular, Instituto de Ciencias Biomédicas; Laboratorio de Análisis de Imágenes Científicas (SCIAN), Instituto de Neurociencias Biomédicas, Facultad de Medicina; Departamento de Medicina Preventiva Animal, Departamento de Ciencias Biológicas Animales, Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Chile
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María Soledad Fernández
María Soledad Fernández
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José Luis Arias
José Luis Arias
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Norbel Galanti
Norbel Galanti
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Arturo Ferreira
Arturo Ferreira
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Trypanosoma cruzi calreticulin (TcCRT), a 47-kDa chaperone, translocates from the endoplasmic reticulum to the area of flagellum emergence. There, it binds to complement components C1 and mannan-binding lectin (MBL), thus acting as a main virulence factor, and inhibits the classical and lectin pathways. The localization and functions of TcCRT, once the parasite is inside the host cell, are unknown. In parasites infecting murine macrophages, polyclonal anti-TcCRT antibodies detected TcCRT mainly in the parasite nucleus and kinetoplast. However, with a monoclonal antibody (E2G7), the resolution and specificity of the label markedly improved, and TcCRT was detected mainly in the parasite kinetoplast. Gold particles, bound to the respective antibodies, were used as probes in electron microscopy. This organelle may represent a stopover and accumulation site for TcCRT, previous its translocation to the area of flagellum emergence. Finally, early during T. cruzi infection and by unknown mechanisms, an important decrease in the number of MHC-I positive host cells was observed.
Author Notes
Financial support: This work was supported by FONDECYT grant 1130099 (AF) and Associative Research ACT-112 (AF, NG), FONDECYT grant 1130113 (NG), and also CONICYT fellowships: For Doctoral Studies in Chile (21080219) and Doctoral Thesis Support (AT 24100233) (AG).
Authors' addresses: Andrea González, Caroline Valck, and Arturo Ferreira, University of Chile, Program of Immunology, Institute of Biomedical Sciences, Faculty of Medicine, Santiago, Chile, E-mails: angozu@ciq.uchile.cl, cvalck@gmail.com, and aferreir@med.uchile.cl. Gittith Sánchez, University of Chile, Program of Human Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Santiago, Chile, E-mail: gsanchez@med.uchile.cl. Steffen Härtel and Jorge Mansilla, University of Chile, Biomedical Neuroscience Institute, Institute of Biomedical Sciences, Faculty of Medicine, Santiago, Chile, E-mails: shartel@med.uchile.cl and jorgemansillas@gmail.com. Galia Ramírez, University of Chile, Department of Preventing Animal Medicine, Faculty of Veterinarian Medicine, Santiago, Chile, E-mail: galiaramirez@gmail.com. María Soledad Fernández and José L. Arias, University of Chile, Department of Animal Biological Sciences, Faculty of Veterinarian Medicine, Santiago, Chile, E-mails: sofernan@uchile.cl and jarias@uchile.cl. Norbel Galanti, University of Chile, Program of Cellular and Molecular Biology, Institute of Biomedical Sciences, Faculty of Medicine, Santiago, Chile, E-mail: ngalanti@med.uchile.cl.
- Introduction
- Materials and Methods
- Recombinant TcCRT (rTcCRT).
- Polyclonal antibodies.
- Monoclonal antibody.
- Cell culture.
- Parasites.
- TEM.
- Immunocytochemistry.
- Immunocytochemical procedures for CRT detection.
- Quantification of label density generated by polyclonal antibodies.
- Quantification of TcCRT molecules in kinetoplast sections.
- ELISA.
- Detection of positive cells for MHC class I antigens by flow cytometry.
- Flow cytometry data analysis.
- Statistical analysis.
- Results
- Discussion
- Conclusions
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Clayton J, 2010. Chagas disease 101. Nature 465: S4–S5.
-
2.
Clayton J, 2010. Chagas disease: pushing through the pipeline. Nature 465: S12–S15.
-
3.
Coura JR, Vinas PA, 2010. Chagas disease: a new worldwide challenge. Nature 465: S6–S7.
-
4.
Tyler KM, Engman DM, 2001. The life cycle of Trypanosoma cruzi revisited. Int J Parasitol 31: 472–481.
-
5.
Ramirez G, Valck C, Molina MC, Ribeiro CH, Lopez N, Sanchez G, Ferreira VP, Billetta R, Aguilar L, Maldonado I, Cattan P, Schwaeble W, Ferreira A, 2011. Trypanosoma cruzi calreticulin: a novel virulence factor that binds complement C1 on the parasite surface and promotes infectivity. Immunobiology 216: 265–273.
-
6.
Ferreira V, Molina MC, Valck C, Rojas A, Aguilar L, Ramirez G, Schwaeble W, Ferreira A, 2004. Role of calreticulin from parasites in its interaction with vertebrate hosts. Mol Immunol 40: 1279–1291.
-
7.
Michalak M, Corbett EF, Mesaeli N, Nakamura K, Opas M, 1999. Calreticulin: one protein, one gene, many functions. Biochem J 344: 281–292.
-
8.
Sonnichsen B, Fullekrug J, Nguyen Van P, Diekmann W, Robinson DG, Mieskes G, 1994. Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J Cell Sci 107: 2705–2717.
-
9.
Souto-Padron T, Labriola CA, de Souza W, 2004. Immunocytochemical localization of calreticulin in Trypanosoma cruzi. Histochem Cell Biol 122: 563–569.
-
10.
Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, Opas M, MacLennan DH, Michalak M, 1999. Calreticulin is essential for cardiac development. J Cell Biol 144: 857–868.
-
11.
Ferreira V, Valck C, Sanchez G, Gingras A, Tzima S, Molina MC, Sim R, Schwaeble W, Ferreira A, 2004. The classical activation pathway of the human complement system is specifically inhibited by calreticulin from Trypanosoma cruzi. J Immunol 172: 3042–3050.
-
12.
Valck C, Ramirez G, Lopez N, Ribeiro CH, Maldonado I, Sanchez G, Ferreira VP, Schwaeble W, Ferreira A, 2010. Molecular mechanisms involved in the inactivation of the first component of human complement by Trypanosoma cruzi calreticulin. Mol Immunol 47: 1516–1521.
-
13.
Ramirez G, Valck C, Ferreira VP, Lopez N, Ferreira A, 2012. Extracellular Trypanosoma cruzi calreticulin in the host-parasite interplay. Trends Parasitol 27: 115–122.
-
14.
Sosoniuk E, Vallejos G, Kenawy H, Gaboriaud C, Thielens N, Fujita T, Schwaeble W, Ferreira A, Valck C, 2014. Trypanosoma cruzi calreticulin inhibits the complement lectin pathway activation by direct interaction with L-ficolin. Mol Immunol 60: 80–85.
-
15.
Lopez NC, Valck C, Ramirez G, Rodriguez M, Ribeiro C, Orellana J, Maldonado I, Albini A, Anacona D, Lemus D, Aguilar L, Schwaeble W, Ferreira A, 2010. Antiangiogenic and antitumor effects of Trypanosoma cruzi calreticulin. PLoS Negl Trop Dis 4: e730.
-
16.
Molina MC, Ferreira V, Valck C, Aguilar L, Orellana J, Rojas A, Ramirez G, Billetta R, Schwaeble W, Lemus D, Ferreira A, 2005. An in vivo role for Trypanosoma cruzi calreticulin in antiangiogenesis. Mol Biochem Parasitol 140: 133–140.
-
17.
Ferreira V, Molina MC, Schwaeble W, Lemus D, Ferreira A, 2005. Does Trypanosoma cruzi calreticulin modulate the complement system and angiogenesis? Trends Parasitol 21: 169–174.
-
18.
Sanchez Valdez FJ, Perez Brandan C, Zago MP, Labriola C, Ferreira A, Basombrio MA, 2013. Trypanosoma cruzi carrying a monoallelic deletion of the calreticulin (TcCRT) gene are susceptible to complement mediated killing and defective in their metacyclogenesis. Mol Immunol 53: 198–205.
-
19.
Sanchez-Valdez FJ, Perez Brandan C, Ramirez G, Uncos AD, Zago MP, Cimino RO, Cardozo RM, Marco JD, Ferreira A, Basombrio MA, 2014. A monoallelic deletion of the TcCRT gene increases the attenuation of a cultured Trypanosoma cruzi strain, protecting against an in vivo virulent challenge. PLoS Negl Trop Dis 8: e2696.
-
20.
Aguillon JC, Ferreira L, Perez C, Colombo A, Molina MC, Wallace A, Solari A, Carvallo P, Galindo M, Galanti N, Orn A, Billetta R, Ferreira A, 2000. Tc45, a dimorphic Trypanosoma cruzi immunogen with variable chromosomal localization, is calreticulin. Am J Trop Med Hyg 63: 306–312.
-
21.
Aguilar L, Ramirez G, Valck C, Molina MC, Rojas A, Schwaeble W, Ferreira V, Ferreira A, 2005. F(ab′)2 antibody fragments against Trypanosoma cruzi calreticulin inhibit its interaction with the first component of human complement. Biol Res 38: 187–195.
-
22.
Aguillon JC, Harris R, Molina MC, Colombo A, Cortes C, Hermosilla T, Carreno P, Orn A, Ferreira A, 1997. Recognition of an immunogenetically selected Trypanosoma cruzi antigen by seropositive chagasic human sera. Acta Trop 63: 159–166.
-
23.
Kohler G, Milstein C, 1975. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256: 495–497.
-
24.
Yasumura YK, Kawakita M, 1963. The research for the SV40 by means of tissue culture technique. Nippon Rinsho 21: 1201–1219.
-
25.
Paulsson K, Wang P, 2003. Chaperones and folding of MHC class I molecules in the endoplasmic reticulum. Biochim Biophys Acta 1641: 1–12.
-
26.
Mancino L, Rizvi SM, Lapinski PE, Raghavan M, 2002. Calreticulin recognizes misfolded HLA-A2 heavy chains. Proc Natl Acad Sci USA 99: 5931–5936.
-
27.
Saito Y, Ihara Y, Leach MR, Cohen-Doyle MF, Williams DB, 1999. Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J 18: 6718–6729.
-
28.
Wada I, Imai S, Kai M, Sakane F, Kanoh H, 1995. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J Biol Chem 270: 20298–20304.
-
29.
Bayer-Santos E, Aguilar-Bonavides C, Rodrigues SP, Cordero EM, Marques AF, Varela-Ramirez A, Choi H, Yoshida N, da Silveira JF, Almeida IC, 2012. Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res 12: 883–897.
-
30.
Van Overtvelt L, Andrieu M, Verhasselt V, Connan F, Choppin J, Vercruysse V, Goldman M, Hosmalin A, Vray B, 2002. Trypanosoma cruzi down-regulates lipopolysaccharide-induced MHC class I on human dendritic cells and impairs antigen presentation to specific CD8(+) T lymphocytes. Int Immunol 14: 1135–1144.
-
31.
Buckner FS, Wipke BT, Van Voorhis WC, 1997. Trypanosoma cruzi infection does not impair major histocompatibility complex class I presentation of antigen to cytotoxic T lymphocytes. Eur J Immunol 27: 2541–2548.
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