Roles of Trypanosoma cruzi calreticulin in parasite-host interactions and in tumor growth

Molecular Immunology

Volumn 52, Issue 3-4, 2012, Pages 133-140

  Ramírez, Galia ^a   Valck, Carolina ^b   Aguilar, Lorena ^b   Kemmerling, Ulrike ^b   López Muñoz, Rodrigo ^b   Cabrera, Gonzalo ^b   Morello, Antonio ^b   Ferreira, Jorge ^b   Maya, Juan Diego ^b   Galanti, Norbel ^b   Ferreira, Arturo ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

Angiogenesis; Complement C1; Trypanosoma cruzi calreticulin (TcCRT); Tumors

Indexed keywords

CALCIUM; CALRETICULIN; COMPLEMENT COMPONENT C1; FICOLIN; METHOTREXATE;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; HOST PARASITE INTERACTION; HUMAN; LUNG CANCER; MOLECULAR CLONING; NONHUMAN; OVARY CANCER; PARASITOSIS; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN CONFORMATION; PROTEIN ISOLATION; REVIEW; SPECIES INVASION; TRYPANOSOMA CRUZI; TUMOR GROWTH; UTERINE CERVIX CANCER;

ANGIOGENESIS INHIBITORS; ANIMALS; CALRETICULIN; CELL PROLIFERATION; CHAGAS DISEASE; HOST-PARASITE INTERACTIONS; HUMANS; NEOPLASMS; TRYPANOSOMA CRUZI;

TRYPANOSOMA CRUZI; VERTEBRATA;

EID: 84861721660     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.05.006     Document Type: Review

References (134)

1. Aguilar L., Ramirez G., Valck C., Molina M.C., Rojas A., Schwaeble W., Ferreira V., Ferreira A. F(ab')2 antibody fragments against Trypanosoma cruzi calreticulin inhibit its interaction with the first component of human complement. Biological Research 2005, 38:187-195.
2. Aguilera R., Saffie C., Tittarelli A., Gonzalez F.E., Ramirez M., Reyes D., Pereda C., Hevia D., Garcia T., Salazar L., Ferreira A., Hermoso M., Mendoza-Naranjo A., Ferrada C., Garrido P., Lopez M.N., Salazar-Onfray F. Heat-shock induction of tumor-derived danger signals mediates rapid monocyte differentiation into clinically effective dendritic cells. Clinical Cancer Research 2011, 17:2474-2483.
3. Aguillon J.C., Bustos C., Vallejos P., Hermosilla T., Morello A., Repetto Y., Hellman U., Orn A., Ferreira A. Purification and preliminary sequencing of Tc-45, an immunodominant Trypanosoma cruzi antigen: absence of homology with cruzipain, cruzain, and a 46-kilodalton protein. American Journal of Tropical Medicine and Hygiene 1995, 53:211-215.
4. Aguillon J.C., Ferreira L., Perez C., Colombo A., Molina M.C., Wallace A., Solari A., Carvallo P., Galindo M., Galanti N., Orn A., Billetta R., Ferreira A. Tc45, a dimorphic Trypanosoma cruzi immunogen with variable chromosomal localization, is calreticulin. American Journal of Tropical Medicine and Hygiene 2000, 63:306-312.
5. Aguillon J.C., Harris R., Molina M.C., Colombo A., Cortes C., Hermosilla T., Carreno P., Orn A., Ferreira A. Recognition of an immunogenetically selected Trypanosoma cruzi antigen by seropositive chagasic human sera. Acta Tropica 1997, 63:159-166.
6. 2 complex and genetic background influence on the humoral immune response against epimastigotes. International Journal for Parasitology 2000, 30:981-984.
7. Andrade S.G., Grimaud J.A., Stocker-Guerret S. Sequential changes of the connective matrix components of the myocardium (fibronectin and laminin) and evolution of cardiac fibrosis in mice infected with Trypanosoma cruzi. American Journal of Tropical Medicine and Hygiene 1989, 40:252-260.
8. Araya J.E., Cornejo A., Orrego P.R., Cordero E.M., Cortez M., Olivares H., Neira I., Sagua H., da Silveira J.F., Yoshida N., Gonzalez J. Calcineurin B of the human protozoan parasite Trypanosoma cruzi is involved in cell invasion. Microbes and Infection 2008, 10:892-900.
9. Arnholdt A.C., Piuvezam M.R., Russo D.M., Lima A.P., Pedrosa R.C., Reed S.G., Scharfstein J. Analysis and partial epitope mapping of human T cell responses to Trypanosoma cruzi cysteinyl proteinase. Journal of Immunology 1993, 151:3171-3179.
10. Auerbach R., Lewis R., Shinners B., Kubai L., Akhtar N. Angiogenesis assays: a critical overview. Clinical Chemistry 2003, 49:32-40.
11. Bambino-Medeiros R., Oliveira F.O., Calvet C.M., Vicente D., Toma L., Krieger M.A., Meirelles M.N., Pereira M.C. Involvement of host cell heparan sulfate proteoglycan in Trypanosoma cruzi amastigote attachment and invasion. Parasitology 2011, 138:593-601.
12. Burleigh B.A., Woolsey A.M. Cell signalling and Trypanosoma cruzi invasion. Cellular Microbiology 2002, 4:701-711.
13. Burns K., Duggan B., Atkinson E.A., Famulski K.S., Nemer M., Bleackley R.C., Michalak M. Modulation of gene expression by calreticulin binding to the glucocorticoid receptor. Nature 1994, 367:476-480.
14. Burton D.R., Woof J.M. Human antibody effector function. Advances in Immunology 1992, 51:1-84.
15. Cabral H.R. The tumoricidal effect of Trypanosoma cruzi: its intracellular cycle and the immune response of the host. Medical Hypotheses 2000, 54:1-6.
16. Cabrera G., Barria C., Fernandez C., Sepulveda S., Valenzuela L., Kemmerling U., Galanti N. DNA repair BER pathway inhibition increases cell death caused by oxidative DNA damage in Trypanosoma cruzi. Journal of Cellular Biochemistry 2011, 112:2189-2199.
17. Cai K.X., Tse L.Y., Leung C., Tam P.K., Xu R., Sham M.H. Suppression of lung tumor growth and metastasis in mice by adeno-associated virus-mediated expression of vasostatin. Clinical Cancer Research 2008, 14:939-949.
18. 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. Experimental Parasitology 2004, 107:20-30.
19. Calvet C.M., Oliveira F.O., Araujo-Jorge T.C., Pereira M.C. Regulation of extracellular matrix expression and distribution in Trypanosoma cruzi-infected cardiomyocytes. International Journal of Medical Microbiology 2009, 299:301-312.
20. Caradonna K.L., Burleigh B.A. Mechanisms of host cell invasion by Trypanosoma cruzi. Advances in Parasitology 2011, 76:33-61.
21. Cardenas T.C., Johnson C.A., Pratap S., Nde P.N., Furtak V., Kleshchenko Y.Y., Lima M.F., Villalta F. Regulation of the extracellular matrix interactome by Trypanosoma cruzi. Journal of Open Parasitology 2010, 4:72-76.
22. 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 Biology 2008, 9:68.
23. Conte I., Labriola C., Cazzulo J.J., Docampo R., Parodi A.J. The interplay between folding-facilitating mechanisms in Trypanosoma cruzi endoplasmic reticulum. Molecular Biology of the Cell 2003, 14:3529-3540.
24. Coura J.R., Dias J.C. Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Memórias do Instituto Oswaldo Cruz 2009, 104(Suppl. 1):31-40.
25. Coura J.R., Vinas P.A. Chagas disease: a new worldwide challenge. Nature 2010, 465:S6-S7.
26. de Souza W., de Carvalho T.M., Barrias E.S. Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 2010.
27. Dedhar S., Rennie P.S., Shago M., Hagesteijn C.Y., Yang H., Filmus J., Hawley R.G., Bruchovsky N., Cheng H., Matusik R.J., et al. Inhibition of nuclear hormone receptor activity by calreticulin. Nature 1994, 367:480-483.
28. Del Nery E., Juliano M.A., Lima A.P., Scharfstein J., Juliano L. Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi. Journal of Biological Chemistry 1997, 272:25713-25718.
29. Duaso J., Rojo G., Cabrera G., Galanti N., Bosco C., Maya J.D., Morello A., Kemmerling U. Trypanosoma cruzi induces tissue disorganization and destruction of chorionic villi in an ex vivo infection model of human placenta. Placenta 2010, 31:705-711.
30. Duaso J., Rojo G., Jana F., Galanti N., Cabrera G., Bosco C., Lopez-Munoz R., Maya J.D., Ferreira J., Kemmerling U. Trypanosoma cruzi induces apoptosis in ex vivo infected human chorionic villi. Placenta 2011, 32:356-361.
31. Duaso J., Yanez E., Castillo C., Galanti N., Cabrera G., Corral G., Maya J.D., Zulantay I., Apt W., Kemmerling U. Reorganization of extracellular matrix in placentas from women with asymptomatic chagas disease: mechanism of parasite invasion or local placental defense?. Journal of Tropical Medicine 2012, 758357.
32. El Gengehi N., El Ridi R., Tawab N.A., El Demellawy M., Mangold B.L. A Schistosoma mansoni 62-kDa band is identified as an irradiated vaccine T-cell antigen and characterized as calreticulin. Journal of Parasitology 2000, 86:993-1000.
33. Epting C.L., Coates B.M., Engman D.M. Molecular mechanisms of host cell invasion by Trypanosoma cruzi. Experimental Parasitology 2010, 126:283-291.
34. Ferreira V., Molina M.C., Schwaeble W., Lemus D., Ferreira A. Does Trypanosoma cruzi calreticulin modulate the complement system and angiogenesis?. Trends in Parasitology 2005, 21:169-174.
35. Ferreira V., Molina M.C., Valck C., Rojas A., Aguilar L., Ramirez G., Schwaeble W., Ferreira A. Role of calreticulin from parasites in its interaction with vertebrate hosts. Molecular Immunology 2004, 40:1279-1291.
36. Ferreira V., Valck C., Sanchez G., Gingras A., Tzima S., Molina M.C., Sim R., Schwaeble W., Ferreira A. The classical activation pathway of the human complement system is specifically inhibited by calreticulin from Trypanosoma cruzi. Journal of Immunology 2004, 172:3042-3050.
37. Folkman J. Fundamental concepts of the angiogenic process. Current Molecular Medicine 2003, 3:643-651.
38. Ganz P.A. Survivorship: adult cancer survivors. Primary Care: Clinics in Office Practice 2009, 36:721-741.
39. Garg N., Tarleton R.L. Genetic immunization elicits antigen-specific protective immune responses and decreases disease severity in Trypanosoma cruzi infection. Infection and Immunity 2002, 70:5547-5555.
40. Garzoni L.R., Adesse D., Soares M.J., Rossi M.I., Borojevic R., de Meirelles Mde.N. Fibrosis and hypertrophy induced by Trypanosoma cruzi in a three-dimensional cardiomyocyte-culture system. Journal of Infectious Diseases 2008, 197:906-915.
41. Gold L., Eggleton P., Sweetwyne M., Van Duyn L., Greives M., Naylor S., Michalak M., Murphy-Ullrich J. Calreticulin: non-endoplasmic reticulum functions in physiology and disease. FASEB Journal 2010, 24:665-6683.
42. Gold L.I., Rahman M., Blechman K.M., Greives M.R., Churgin S., Michaels J., Callaghan M.J., Cardwell N.L., Pollins A.C., Michalak M., Siebert J.W., Levine J.P., Gurtner G.C., Nanney L.B., Galiano R.D., Cadacio C.L. Overview of the role for calreticulin in the enhancement of wound healing through multiple biological effects. Journal of Investigative Dermatology Symposium Proceedings 2006, 11:57-65.
43. Griffioen A.W., Molema G. Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacological Reviews 2000, 52:237-268.
44. Gupta K., Zhang J. Angiogenesis: a curse or cure?. Postgraduate Medical Journal 2005, 81:236-242.
45. Hauschka T.S., Goodwin M.B. Trypanosoma cruzi endotoxin (KR) in the treatment of malignant mouse tumors. Science 1948, 107:600-602.
46. Holaska J.M., Black B.E., Love D.C., Hanover J.A., Leszyk J., Paschal B.M. Calreticulin is a receptor for nuclear export. Journal of Cell Biology 2001, 152:127-140.
47. Iakova P., Wang G.L., Timchenko L., Michalak M., Pereira-Smith O.M., Smith J.R., Timchenko N.A. Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO Journal 2004, 23:406-417.
48. Ishii J., Adachi H., Aoki J., Koizumi H., Tomita S., Suzuki T., Tsujimoto M., Inoue K., Arai H. SREC-II, a new member of the scavenger receptor type F family, trans-interacts with SREC-I through its extracellular domain. Journal of Biological Chemistry 2002, 277:39696-39702.
49. Jazowiecka-Rakus J., Jarosz M., Kozlowska D., Sochanik A., Szala S. Combination of vasostatin and cyclophosphamide in the therapy of murine melanoma tumors. Acta Biochimica Polonica 2007, 54:125-133.
50. Junqueira C., Santos L.I., Galvao-Filho B., Teixeira S.M., Rodrigues F.G., DaRocha W.D., Chiari E., Jungbluth A.A., Ritter G., Gnjatic S., Old L.J., Gazzinelli R.T. Trypanosoma cruzi as an effective cancer antigen delivery vector. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:19695-19700.
51. Kallinikova V.D., Matekin P.V., Ogloblina T.A., Leikina M.I., Kononenko A.F., Sokolova N.M., Pogodina L.S. Anticancer properties of flagellate protozoan Trypanosoma cruzi Chagas, 1909. Izvestiia Akademii Nauk. Seriia Biologicheskaia 2001, 299-311.
52. Kasper G., Brown A., Eberl M., Vallar L., Kieffer N., Berry C., Girdwood K., Eggleton P., Quinnell R., Pritchard D.I. A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunology 2001, 23:141-152.
53. Kemmerling U., Bosco C., Galanti N. Infection and invasion mechanisms of Trypanosoma cruzi in the congenital transmission of Chagas' disease: a proposal. Biological Research 2010, 43:307-316.
54. Kim J.O., Jung S.S., Kim S.Y., Kim T.Y., Shin D.W., Lee J.H., Lee Y.H. Inhibition of Lewis lung carcinoma growth by Toxoplasma gondii through induction of Th1 immune responses and inhibition of angiogenesis. Journal of Korean Medical Science 2007, 22(Suppl.):S38-S46.
55. Kiupel M. Special focus: diagnosis and prognosis of neoplastic diseases in companion animals. Veterinary Pathology 2011, 48:6.
56. Krementsov N. The Cure: A Story of Cancer and Politics from the Annals of the Cold War 2002, University of Chicago Press, 277.
57. Krementsov N. Trypanosoma cruzi, cancer and the cold war. História, Ciências, Saúde-Manguinhos 2009, 16(Suppl. 1):75-94.
58. Labriola C., Cazzulo J.J., Parodi A.J. Trypanosoma cruzi calreticulin is a lectin that binds monoglucosylated oligosaccharides but not protein moieties of glycoproteins. Molecular Biology of the Cell 1999, 10:1381-1394.
59. Labriola C., Conte I., López Medus M., Parodi A., Caramelo J. Endoplasmic reticulum calcium regulates the retrotranslocation of Trypanosoma cruzi calreticulin to the cytosol. PLoS One 2010, 5:e13141.
60. Lima A.P., Almeida P.C., Tersariol I.L., Schmitz V., Schmaier A.H., Juliano L., Hirata I.Y., Muller-Esterl W., Chagas J.R., Scharfstein J. Heparan sulfate modulates kinin release by Trypanosoma cruzi through the activity of cruzipain. Journal of Biological Chemistry 2002, 277:5875-5881.
61. Lima A.P., Tessier D.C., Thomas D.Y., Scharfstein J., Storer A.C., Vernet T. Identification of new cysteine protease gene isoforms in Trypanosoma cruzi. Molecular and Biochemical Parasitology 1994, 67:333-338.
62. Lopez-Munoz R., Faundez M., Klein S., Escanilla S., Torres G., Lee-Liu D., Ferreira J., Kemmerling U., Orellana M., Morello A., Ferreira A., Maya J.D. Trypanosoma cruzi: in vitro effect of aspirin with nifurtimox and benznidazole. Experimental Parasitology 2010, 124:167-171.
63. Lopez N.C., Valck C., Ramirez G., Rodriguez M., Ribeiro C., Orellana J., Maldonado I., Albini A., Anacona D., Lemus D., Aguilar L., Schwaeble W., Ferreira A. Antiangiogenic and antitumor effects of Trypanosoma cruzi calreticulin. PLoS Neglected Tropical Diseases 2010, 4:e730.
64. Machado J., Fernandez P.C., Baumann I., Dobbelaere D.A. Characterisation of NF-kappa B complexes in Theileria parva-transformedT cells. Microbes and Infection 2000, 2:1311-1320.
65. Malhotra R. Collectin receptor (C1q receptor): structure and function. Behring Institute Mitteilungen 1993, 254-261.
66. Manarin R., Pascutti M.F., Ruffino J.P., De Las Heras B., Bosca L., Bottasso O., Revelli S., Serra E. Benznidazole blocks NF-kappaB activation but not AP-1 through inhibition of IKK. Molecular Immunology 2010, 47:2485-2491.
67. 2+ signaling activity in stably transfected Trypanosoma cruzi epimastigotes expressing the metacyclic stage-specific surface molecule gp82. Infection and Immunity 2003, 71:1561-1565.
68. Marcelain K., Colombo A., Molina M.C., Ferreira L., Lorca M., Aguillon J.C., Ferreira A. Development of an immunoenzymatic assay for the detection of human antibodies against Trypanosoma cruzi calreticulin, an immunodominant antigen. Acta Tropica 2000, 75:291-300.
69. Marino A.P., Silva A.A., Pinho R.T., Lannes-Vieira J. Trypanosoma cruzi infection: a continuous invader-host cell cross talk with participation of extracellular matrix and adhesion and chemoattractant molecules. Brazilian Journal of Medical and Biological Research 2003, 36:1121-1133.
70. Meirelles M.N., Juliano L., Carmona E., Silva S.G., Costa E.M., Murta A.C., Scharfstein J. Inhibitors of the major cysteinyl proteinase (GP57/51) impair host cell invasion and arrest the intracellular development of Trypanosoma cruzi in vitro. Molecular and Biochemical Parasitology 1992, 52:175-184.
71. Mendes-da-Cruz D.A., Silva J.S., Cotta-de-Almeida V., Savino W. Altered thymocyte migration during experimental acute Trypanosoma cruzi infection: combined role of fibronectin and the chemokines CXCL12 and CCL4. European Journal of Immunology 2006, 36:1486-1493.
72. Michalak M., Corbett E.F., Mesaeli N., Nakamura K., Opas M. Calreticulin: one protein, one gene, many functions. Biochemical Journal 1999, 344(Pt 2):281-292.
73. Michalak M., Groenendyk J., Szabo E., Gold L.I., Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochemical Journal 2009, 417:651-666.
74. Molina M.C., Ferreira V., Valck C., Aguilar L., Orellana J., Rojas A., Ramirez G., Billetta R., Schwaeble W., Lemus D., Ferreira A. An in vivo role for Trypanosoma cruzi calreticulin in antiangiogenesis. Molecular and Biochemical Parasitology 2005, 140:133-140.
75. Murta A.C., Persechini P.M., Padron Tde S., de Souza W., Guimaraes J.A., Scharfstein J. Structural and functional identification of GP57/51 antigen of Trypanosoma cruzi as a cysteine proteinase. Molecular and Biochemical Parasitology 1990, 43:27-38.
76. Nagajyothi F., Desruisseaux M., Bouzahzah B., Weiss L.M., Andrade Ddos S., Factor S.M., Scherer P.E., Albanese C., Lisanti M.P., Tanowitz H.B. Cyclin and caveolin expression in an acute model of murine Chagasic myocarditis. Cell Cycle 2006, 5:107-112.
77. Nanney L.B., Woodrell C.D., Greives M.R., Cardwell N.L., Pollins A.C., Bancroft T.A., Chesser A., Michalak M., Rahman M., Siebert J.W., Gold L.I. Calreticulin enhances porcine wound repair by diverse biological effects. American Journal of Pathology 2008, 173:610-630.
78. Nde P.N., Simmons K.J., Kleshchenko Y.Y., Pratap S., Lima M.F., Villalta F. Silencing of the laminin gamma-1 gene blocks Trypanosoma cruzi infection. Infection and Immunity 2006, 74:1643-1648.
79. Nickenig G., Michaelsen F., Muller C., Berger A., Vogel T., Sachinidis A., Vetter H., Bohm M. Destabilization of AT(1) receptor mRNA by calreticulin. Circulation Research 2002, 90:53-58.
80. Norris K.A. Ligand-binding renders the 160 kDa Trypanosoma cruzi complement regulatory protein susceptible to proteolytic cleavage. Microbial Pathogenesis 1996, 21:235-248.
81. Norris K.A., Bradt B., Cooper N.R., So M. Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the human complement regulatory protein, decay-accelerating factor. Journal of Immunology 1991, 147:2240-2247.
82. Norris K.A., Galvao L.M., Schrimpf J.E., Cancado J.R., Krettli A.U. Humoral immune response to the Trypanosoma cruzi complement regulatory protein as an indicator of parasitologic clearance in human Chagas' disease. Infection and Immunity 1994, 62:4072-4074.
83. Obeid M., Panaretakis T., Joza N., Tufi R., Tesniere A., van Endert P., Zitvogel L., Kroemer G. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death and Differentiation 2007, 14:1848-1850.
84. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N., Metivier D., Larochette N., van Endert P., Ciccosanti F., Piacentini M., Zitvogel L., Kroemer G. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nature Medicine 2007, 13:54-61.
85. Obeid M., Tesniere A., Panaretakis T., Tufi R., Joza N., van Endert P., Ghiringhelli F., Apetoh L., Chaput N., Flament C., Ullrich E., de Botton S., Zitvogel L., Kroemer G. Ecto-calreticulin in immunogenic chemotherapy. Immunological Reviews 2007, 220:22-34.
86. Oliveira E.C., Leite M.S., Miranda J.A., Andrade A.L., Garcia S.B., Luquetti A.O., Moreira H. Chronic Trypanosoma cruzi infection associated with low incidence of 1,2-dimethylhydrazine-induced colon cancer in rats. Carcinogenesis 2001, 22:737-740.
87. Ortega-Barria E., Pereira M.E. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 1991, 67:411-421.
88. Ouaissi A. Molecular aspects of Trypanosoma cruzi interaction with host cell and parasite differentiation mechanisms. Annales de la Societe Belge de Medecine Tropicale 1992, 72(Suppl. 1):23-25.
89. 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.
90. Pereira K.S., Schmidt F.L., Guaraldo A.M., Franco R.M., Dias V.L., Passos L.A. Chagas' disease as a foodborne illness. Journal of Food Protection 2009, 72:441-446.
91. Pike S.E., Yao L., Jones K.D., Cherney B., Appella E., Sakaguchi K., Nakhasi H., Teruya-Feldstein J., Wirth P., Gupta G., Tosato G. Vasostatin, a calreticulin fragment, inhibits angiogenesis and suppresses tumor growth. Journal of Experimental Medicine 1998, 188:2349-2356.
92. Pike S.E., Yao L., Setsuda J., Jones K.D., Cherney B., Appella E., Sakaguchi K., Nakhasi H., Atreya C.D., Teruya-Feldstein J., Wirth P., Gupta G., Tosato G. Calreticulin and calreticulin fragments are endothelial cell inhibitors that suppress tumor growth. Blood 1999, 94:2461-2468.
93. Ramirez G., Valck C., Ferreira V.P., Lopez N., Ferreira A. Extracellular Trypanosoma cruzi calreticulin in the host-parasite interplay. Trends in Parasitology 2011, 27:115-122.
94. Ramirez G., Valck C., Molina M.C., Ribeiro C.H., Lopez N., Sanchez G., Ferreira V.P., Billetta R., Aguilar L., Maldonado I., Cattan P., Schwaeble W., Ferreira A. Trypanosoma cruzi calreticulin: a novel virulence factor that binds complement C1 on the parasite surface and promotes infectivity. Immunobiology 2011, 216:265-273.
95. Ramos R., Juri M., Ramos A., Hoecker G., Lavandero S., Pena P., Morello A., Repetto Y., Aguillon J.C., Ferreira A. An immunogenetically defined and immunodominant Trypanosoma cruzi antigen. American Journal of Tropical Medicine and Hygiene 1991, 44:314-322.
96. Ribatti D. The crucial role of vascular permeability factor/vascular endothelial growth factor in angiogenesis: a historical review. British Journal of Haematology 2005, 128:303-309.
97. Ribeiro C.H., Lopez N.C., Ramirez G.A., Valck C.E., Molina M.C., Aguilar L., Rodriguez M., Maldonado I., Martinez R., Gonzalez C., Troncoso R., Lavandero S., Gingras A.R., Schwaeble W., Ferreira A. Trypanosoma cruzi calreticulin: a possible role in Chagas' disease autoimmunity. Molecular Immunology 2009, 46:1092-1099.
98. Rimoldi M.T., Tenner A.J., Bobak D.A., Joiner K.A. Complement component C1q enhances invasion of human mononuclear phagocytes and fibroblasts by Trypanosoma cruzi trypomastigotes. Journal of Clinical Investigation 1989, 84:1982-1989.
99. 2+ mobilization and microfilament rearrangement in host cells. Journal of Cell Biology 1995, 129:1263-1273.
100. Rokeach L.A., Zimmerman P.A., Unnasch T.R. Epitopes of the Onchocerca volvulus RAL1 antigen, a member of the calreticulin family of proteins, recognized by sera from patients with onchocerciasis. Infection and Immunity 1994, 62:3696-3704.
101. Roskin G.I. L' action des toxines sur le cancer experimental. Acta Medica URSS 1939, 2.
102. Santana J.M., Grellier P., Schrevel J., Teixeira A.R. A Trypanosoma cruzi-secreted 80kDa proteinase with specificity for human collagen types I and IV. Biochemical Journal 1997, 325(Pt 1):129-137.
103. Scharfstein J., Morrot A. A role for extracellular amastigotes in the immunopathology of Chagas disease. Memorias do Instituto Oswaldo Cruz 1999, 94(Suppl. 1):51-63.
104. Scharfstein J., Schechter M., Senna M., Peralta J.M., Mendonca-Previato L., Miles M.A. Trypanosoma cruzi: characterization and isolation of a 57/51,000m.w. surface glycoprotein (GP57/51) expressed by epimastigotes and bloodstream trypomastigotes. Journal of Immunology 1986, 137:1336-1341.
105. Schmunis G.A. Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Memorias do Instituto Oswaldo Cruz 2007, 102(Suppl. 1):75-85.
106. Singh N.K., Atreya C.D., Nakhasi H.L. Identification of calreticulin as a rubella virus RNA binding protein. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:12770-12774.
107. Souto-Padron T., Labriola C.A., de Souza W. Immunocytochemical localisation of calreticulin in Trypanosoma cruzi. Histochemistry and Cell Biology 2004, 122:563-569.
108. Stuart G.R., Lynch N.J., Day A.J., Schwaeble W.J., Sim R.B. The C1q and collectin binding site within C1q receptor (cell surface calreticulin). Immunopharmacology 1997, 38:73-80.
109. Stuart G.R., Lynch N.J., Lu J., Geick A., Moffatt B.E., Sim R.B., Schwaeble W.J. Localisation of the C1q binding site within C1q receptor/calreticulin. FEBS Letters 1996, 397:245-249.
110. Svensjo E., Cyrino F.Z., Juliano L., Scharfstein J. Plasma leakage induced in postcapillary venules by the major cysteine-proteinase from Trypanosoma cruzi and its modulation by H1-blocker mepyramine. Microvascular Research 1997, 54:93-97.
111. Tanowitz H.B., Weiss L.M., Montgomery S.P. Chagas disease has now gone global. PLoS Neglected Tropical Diseases 2011, 5:e1136.
112. Tesniere A., Apetoh L., Ghiringhelli F., Joza N., Panaretakis T., Kepp O., Schlemmer F., Zitvogel L., Kroemer G. Immunogenic cancer cell death: a key-lock paradigm. Current Opinion in Immunology 2008, 20:504-511.
113. Timchenko L.T., Iakova P., Welm A.L., Cai Z.J., Timchenko N.A. Calreticulin interacts with C/EBPalpha and C/EBPbeta mRNAs and represses translation of C/EBP proteins. Molecular and Cellular Biology 2002, 22:7242-7257.
114. Toledo V., Ramirez G., Valck C., Lopez N., Ribeiro C.H., Maldonado I., Aguilar L., Lemus D., Ferreira A. Comparative in vivo antiangiogenic effects of calreticulin from Trypanosoma cruzi and Homo sapiens sapiens. Biological Research 2010, 43:287-289.
115. Tonelli R.R., Giordano R.J., Barbu E.M., Torrecilhas A.C., Kobayashi G.S., Langley R.R., Arap W., Pasqualini R., Colli W., Alves M.J. Role of the gp85/trans-sialidases in Trypanosoma cruzi tissue tropism: preferential binding of a conserved peptide motif to the vasculature in vivo. PLoS Neglected Tropical Diseases 2010, 4:e864.
116. Totary-Jain H., Naveh-Many T., Riahi Y., Kaiser N., Eckel J., Sasson S. Calreticulin destabilizes glucose transporter-1 mRNA in vascular endothelial and smooth muscle cells under high-glucose conditions. Circulation Research 2005, 97:1001-1008.
117. Valck C., Ramirez G., Lopez N., Ribeiro C.H., Maldonado I., Sanchez G., Ferreira V.P., Schwaeble W., Ferreira A. Molecular mechanisms involved in the inactivation of the first component of human complement by Trypanosoma cruzi calreticulin. Molecular Immunology 2010, 47:1516-1521.
118. Van Duyn Graham L., Sweetwyne M.T., Pallero M.A., Murphy-Ullrich J.E. Intracellular calreticulin regulates multiple steps in fibrillar collagen expression, trafficking, and processing into the extracellular matrix. Journal of Biological Chemistry 2010, 285:7067-7078.
119. Vieira M.C., de Carvalho T.U., de Souza W. Effect of protein kinase inhibitors on the invasion process of macrophages by Trypanosoma cruzi. Biochemical and Biophysical Research Communications 1994, 203:967-971.
120. Villalta F., Madison M.N., Kleshchenko Y.Y., Nde P.N., Lima M.F. Molecular analysis of early host cell infection by Trypanosoma cruzi. Frontiers in Bioscience 2008, 13:3714-3734.
121. Villalta F., Zhang Y., Bibb K.E., Pratap S., Burns J.M., Lima M.F. Signal transduction in human macrophages by gp83 ligand of Trypanosoma cruzi: trypomastigote gp83 ligand up-regulates trypanosome entry through protein kinase C activation. Molecular Cell Biology Research Communications 1999, 2:64-70.
122. WHO, 2007. Reporte del grupo de trabajo científico sobre la enfermedad de Chagas: 17-20 de Abril de 2005, actualizado en julio de 2007. Word Health Organization, Geneva, Buenos Aires, Argentina.
123. Wilkowsky S.E., Barbieri M.A., Stahl P., Isola E.L. Trypanosoma cruzi: phosphatidylinositol 3-kinase and protein kinase B activation is associated with parasite invasion. Experimental Cell Research 2001, 264:211-218.
124. Wirth J.J., Kierszenbaum F. Macrophage mediation of the inhibitory effects of elevated intracellular levels of adenosine-3':5' cyclic monophosphate (cAMP) on macrophage-Trypanosoma cruzi association. International Journal for Parasitology 1984, 14:401-404.
125. 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. Cellular Microbiology 2004, 6:829-838.
126. 2 domains contributes to their differential ability to bind and activate complement. Journal of Biological Chemistry 1994, 269:3469-3474.
127. Yao L., Pike S.E., Pittaluga S., Cherney B., Gupta G., Jaffe E.S., Tosato G. Anti-tumor activities of the angiogenesis inhibitors interferon-inducible protein-10 and the calreticulin fragment vasostatin. Cancer Immunology, Immunotherapy 2002, 51:358-366.
128. Yao L., Pike S.E., Tosato G. Laminin binding to the calreticulin fragment vasostatin regulates endothelial cell function. Journal of Leukocyte Biology 2002, 71:47-53.
129. Yoshida N. Molecular basis of mammalian cell invasion by Trypanosoma cruzi. Anais da Academia Brasileira de Ciencias 2006, 78:87-111.
130. Yoshida N. Trypanosoma cruzi infection by oral route: how the interplay between parasite and host components modulates infectivity. Parasitology International 2008, 57:105-109.
131. Yoshida N., Cortez M. Trypanosoma cruzi: parasite and host cell signaling during the invasion process. Sub-Cellular Biochemistry 2008, 47:82-91.
132. Zhong L., Lu H.G., Moreno S.N., Docampo R. Tyrosine phosphate hydrolysis of host proteins by Trypanosoma cruzi is linked to cell invasion. FEMS Microbiology Letters 1998, 161:15-20.
133. Zhu L., Niu G., Fang X., Chen X. Preclinical molecular imaging of tumor angiogenesis. Quarterly Journal of Nuclear Medicine and Molecular Imaging 2010, 54:291-308.
134. Zitvogel L., Kepp O., Senovilla L., Menger L., Chaput N., Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clinical Cancer Research 2010, 16:3100-3104.