The Trypanosoma cruzi trans-sialidase, through its COOH-terminal tandem repeat, upregulates interleukin 6 secretion in normal human intestinal microvascular endothelial cells and peripheral blood mononuclear cells

Journal of Experimental Medicine

Volumn 190, Issue 12, 1999, Pages 1825-1836

  Saavedra, Emma ^a   Herrera, Macario ^a   Gao, Wenda ^a   Uemura, Haruki ^b   Pereira, Miercio A ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NAGASAKI UNIVERSITY   (Japan)

Author keywords

Cytokines; Endothelial cells; Interleukin 6; Trans sialidase; Trypanosoma cruzi

Indexed keywords

INTERLEUKIN 6; SIALIDASE;

ARTICLE; BLADDER CARCINOMA; CATALYSIS; CELL ACTIVATION; CHAGAS DISEASE; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; EPIMASTIGOTE; FEVER; FIBROSIS; HUMAN; HUMAN CELL; MONONUCLEAR CELL; NEUROPROTECTION; PRIORITY JOURNAL; TANDEM REPEAT; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANIMALS; ENDOTHELIUM, VASCULAR; GLYCOPROTEINS; HUMANS; INTERLEUKIN-6; INTESTINES; LEUKOCYTES, MONONUCLEAR; MICE; MICROCIRCULATION; MOLECULAR SEQUENCE DATA; NEURAMINIDASE; TANDEM REPEAT SEQUENCES; UP-REGULATION;

EID: 0033397901     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.12.1825     Document Type: Article

References (65)

1. Tanowitz, H.B., J.P. Gumprecht, D. Spurr, T.M. Calderon, M.C. Ventura, C. Raventos-Suarez, S. Kellie, S.M. Factor, V.B. Hatcher, M. Wittner, and J.W. Berman. 1992. Cytokine gene expression of endothelial cells infected with Trypanosoma cruzi. J. Infect. Dis. 166:598-603.
2. Van Voorhis, W.C. 1992. Coculture of human peripheral blood mononuclear cells wich Trypanosoma cruzi leads to proliferation of lymphocytes and cytokine production. J. Immunol. 148:239-248.
3. Truyens, C., A. Angelo-Barrios, F. Torrico, J. van Damme, H. Heremans, and Y. Carlier. 1994. Interleukin-6 (IL-6) production in mice infected with Trypanosoma cruzi: effect of its paradoxical increase by anti-IL-6 monoclonal antibody treatment on infection and acute-phase and humoral immune responses. Infect. Immun. 62:692-696.
4. Chandrasckar, B., P.C. Melby, D.A. Troyer, and G.L. Freeman. 1996. Induction of proinflammatory cytokine expression in experimental acute chagasic cardiomyopathy. Biochem. Biophys. Res. Commun. 223:365-371.
5. Sunnemark, D., A.-K. Ulfgren, A. Orn, and R.A. Harris. 1996. Cytokine production in hearts of Trypanosoma cruzi-infected CBA mice: do cytokine patterns in chronic stage reflect the establishment of myocardial pathology? Scand. J. Immunol. 44:421-429.
6. Sunnemark, D., J. Frostegard, A. Orn, and R.A. Harris. 1998. Cellular and cytokine characterization of vascular inflammation in CBA/J mice infected with Trypanosomna cruzi. Scand. J. Immunol. 48:480-484.
7. Zhang, L., and R. Tarleton. 1996. Persistent production of inflammatory and anti-inflammatory cytokines and associated MHC and adhesion molecule expression at the site of infection and disease in experimental Trypanosoma cruzi infections. Exp. Parasitol. 84:203-213.
8. Glienke, W., R. Esser, H. von Briessen, K. Schuster, S. Muller, R. Unger, R. Andreesen, H.J. Stutte, and H. Rubsamen-Waigman. 1994. Cytokine expression of HIV-infected monocytes/ macrophages at the single-cell level. Res. Virol. 145:193-197.
9. Breen, E.C., A.R. Rezai, K. Nakajima, G.N. Beall, R.T. Mitsuyasu, T. Hirano, T. Kishimoto, and O. Martinez-Maza. 1990. Infection with HIV is associated with elevated IL-6 levels and production. J. Immunol. 144:480-484.
10. Rieckmann, P., G. Poli, J.H. Kehlr, and A.S. Fauci. 1991. Activated B lymphocytes from human immunodeficiency virus-infected individuals induce virus expression in infected T cells and a promonocytic cell line, U1. J. Exp. Med. 173:1-5.
11. Ambrosino, C., M.R. Ruocco, X. Chen, M. Mallardo, F. Baudi, S. Trematerra, I. Quinto, S. Venuta, and G. Scala. 1997. HIV-1 Tat induces the expression of the interleukin-6 (IL-6) gene by binding to the IL-6 leader RNA and by interacting with CAAT enhancer-binding protein beta (NF-IL6) transcription factors. J. Biol. Chem. 272:14883-14892.
12. Gong, J.-H., H. Sprenger, F. Hinder, A. Bender, A. Schmidt, S. Horch, M. Nain, and D. Gemsa. 1991. Influenza A virus infection of macrophages. Enhanced tumor necrosis factor-α (TNF-α) gene expression and lipopolysaccharide-triggered TNF-α release J. Immunol. 147:3507-3513.
13. Hayden, F.G., R.S. Fritz, M.C. Lobo, W.G. Alvord, W. Strober, and S.E. Straus. 1998. Local and systemic cytokine responses during experimental human influenza A virus infection. J. Clin. Invest. 101:643-649.
14. Zhu, Z., W. Tang, A. Ray, Y. Wu, O. Einarsson, M.L. Landry, J. Gwaltney, Jr., and J.A. Elias. 1996. Rhinovirus stimulation of interleukin-6 in vivo and in vitro. J. Clin. Invest. 97: 421-430.
15. Sher, A., and R.L. Coffman. 1992. Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu. Rev. Immunol. 10:385-409.
16. DosReis, G.A. 1997. Cell-mediated immunity in experimental Trypanosoma cruzi infection. Parasitol. Today. 13:335-342.
17. Pereira, M.E.A. 1983. A developmentally regulated neuraminidase activity in Trypanosoma cruzi. Science. 219:1444-1447.
18. Schenkman, S.L., P. de Carvalho, and V. Nussenzweig. 1992. Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzyme. J. Exp. Med. 175:567-575.
19. Parodi, A.J., G.D. Pollevick, M. Mautner, A. Buschiazzo, D.O. Sanchez, and A.C.C. Frasch. 1992. Identification of the gene(s) coding for the trans-sialidase of Trypanosoma cruzi. EMBO (Eur. Mol. Biol. Organ.) J. 11:1705-1710.
20. Scudder, P., J.P. Doom, M. Chuenkova, I.D. Manger, and M.E.A. Pereira. 1993. Enzymatic characterization of the βD-galactoside α2,3-trans-sialidase from Trypanosoma cruzi. J. Biol. Chem. 268:9886-9891.
21. Schenkman, S., D. Eichinger, M.E.A. Pereira, and V. Nussenzweig. 1994. Structural and functional properties of trypanosoma trans-sialidase. Annu. Rev. Microbiol. 48:499-532.
22. Pereira, M.E.A., J.S. Mejia, E. Ortega-Barria, D. Matzilevich, and R.P. Prioli. 1991. The Trypanosoma cruzi neuraminidase contains sequences similar to bacterial neuraminidases, YWTI) repeats of the low-density lipoprotein receptor, and type III modules of fibronectin. J. Exp. Med. 174:179-191.
23. Rosenberg, I., R.P. Prioli, E. Ortega-Barria, and M.E.A. Pereira. 1991. Stage-specific phospholipase C mediated release of Trypanosoma cruzi neuraminidase. Mol. Biochem. Parasitol. 46:303-306.
24. De Titto, E., and F.G. Araujo. 1988. Serum neuraminidase activity and hematological alterations in acute human Chagas' disease. Clin. Immunol. Immunopathol. 46:157-161.
25. Chuenkova, M., and M.E.A. Pereira. 1995. Trypanosoma cruzi trans-sialidase: enhancement of virulence in a murine model of Chagas' disease. J. Exp. Med. 181:1693-1703.
26. Strong, S.A., T.T. Pizarro, J.S. Klein, F. Cominelli, and C. Fiocchi. 1998. Proinflammatory cytokines differentially modulate their own expression in human intestinal mucosal mesenchymal cells. Gastroenterology. 114:1244-1256.
27. Coligan, J.E., A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober. 1995. Current Protocols in Immunology. John Wiley & Sons, Inc., New York. 7.1.1-7.1.2.
28. Ortega-Barria, E., and M.E.A. Pereira. 1991. A novel T. cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell. 67:411-421.
29. Uemura, H., S. Schenkman, V. Nussenzweig, and D. Eichinger. 1992. Only some members of a gene family of Trypanosoma cruzi encode proteins that express both trans-sialidase and neuraminidase activities. EMBO (Eur. Mol. Biol. Organ.) J. 11:3837-3844.
30. Bock, G.H., C.A. Long, M.L. Kiley. J.D. White, C.C. Kurnian, T.A. Fleischer, M. Tsokos, M. Brown, D. Serbousek, and W.D. Schwietermann. 1993. Characterization of a new IL-6 dependent human B-lymphoma cell line in long term culture. Cytokine. 5:480-489.
31. Wong, H., W.D. Anderson, T. Cheng, and K.T. Riabowo. 1994. Monitoring mRNA expression by polymerase chain reaction: the "primer-dropping" method. Anal. Biochem. 223: 251-258.
32. Pereira, M.E.A., K. Zhang, Y. Gong, E.M. Herrera, and M. Ming. 1996. Invasive phenotype of Trypanosoma cruzi restricted to a population expressing trans-sialidase. Infect. Immun. 64:3884-3892.
33. Swerlick, R.A., and T.J. Lawley. 1993. Role of microvascular endothelial cells in inflammation. J. Invest. Dermatol. 100: 111S-115S.
34. Granger, D.N., and P. Kubes. 1994. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J. Leukoc. Biol. 55:662-675.
35. Augustin, H.G., D.T. Kozian, and R.C. Johnson. 1994. Differentiation of endothelial cells: analysis of the constitutive and activated endothelial cell phenotypes. Bioessays. 16: 901-906.
36. Binion, D.G., G.A. West, K. Ina, N.P. Ziats, S.N. Emancipator, and C. Fiocchi. 1997. Enhanced leukocyte binding by intestinal microvascular endothelial cells in inflammatory bowel disease. Gastroenterology. 112:1895-1907.
37. Nilsen, E.M., F.-E. Johansen, F.L. Jahnsen, K.E.A. Lundin, T. Scholz, P. Brandtzaeg, and G. Haraldsen. 1998. Cytokine profiles of cultured microvascular endothelial cells from human intestine. Gut. 42:635-642.
38. Bubenik, J., M. Baresova, V. Viklicky, J. Jakoubkova, H. Samerova, and J. Donner. 1973. Established cell line of urinary bladder carcinoma (T24) containing tumor-specific antigen. Int. J. Cancer. 11:765-773.
39. Yasukawa, K., T. Hirano, Y. Watanabe, K. Muratani, T. Matsuda, S. Nakai, and T. Kishimoto. 1987. Structure and expression of human B cell stimulatory factor-2 (BSF-2/IL-6) gene. EMBO (Eur. Mol. Biol. Organ.) J. 6:2939-2945.
40. Stein, B., and M.S.K. Sutherland. 1998. IL-6 as a drug discovery target. Drug Discovery Today. 3:202-213.
41. Cicco, N.A., A. Lindemann, J. Content, P. Vandenbussche, M. Lubbert, J. Gauss, R. Mertelsmann, and F. Herrmann. 1990. Inducible production of interleukin-6 by human polymorphonuclear neutrophils: role of granulocyte-macrophage colony stimulating factor and tumor necrosis factor-alpha. Blood. 75:2049-2052.
42. Chaves, L.B., M.R. Briones, and S. Schenkman. 1993. Trans-sialidase from Trypanosoma cruzi epimastigotes is expressed at the stationary phase and is different from the enzyme expressed in trypomastigotes. Mol. Biochem. Parasitol. 61:97-106.
43. Briones, M.R., C.M. Egima, and S. Schenkman. 1995. Trypanosoma cruzi trans-sialidase gene lacking C-terminal repeats and expressed in epimastigote forms. Mol. Biochem. Parasitol. 70:9-17.
44. Reiner, S.L., and R.M. Locksley. 1995. The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13: 151-177.
45. Yamamura, M., X.H. Wang, J.D. Ohmen, K. Uyemura, T.H. Rea, B.R. Bloom, and R.L. Modlin. 1992. Cytokine patterns of immunologically mediated tissue damage. J. Immunol. 149:1470-1475.
46. Wilson, M., R. Seymour, and B. Henderson. 1998. Bacterial perturbation of cytokine networks. Infect. Immun. 66:2401-2409.
47. Alcami, A., and G.L. Smith. 1992. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell. 71:153-167.
48. Hsu, D.H., R. de Waal-Malfyt, D.F. Fiorentino, M.-N. Dang, P. Vieira, J. deVries, H. Spits, T.R. Mosmann, and K.W. Moore. 1990. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRFI. Science. 250:830-832.
49. Kishimoto, T. 1989. The biology of interleukin-6. Blood. 74: 1-10.
50. Uyttenhove, C., P.G. Coulie, and J. Van Snick. 1998. T cell growth and differentiation induced by interleukin-1 HP1/IL-6, the murine hybridoma/plasmacytoma growth factor. J. Exp. Med. 167:1417-1427.
51. + T cells. J. Exp. Med. 185:461-469.
52. Minoprio, P.M., H. Eisen, F. Forni, M.R. D'Imperio Lima, M. Joskowicz, and A. Coutinho. 1986. Polyclonal lymphocyte responses to murine Trypanosoma cruzi infection. I. Quantitation of both T-and B-cell responses. Scand. J. Immunol. 24:661-668.
53. Duncan, M.R., and B. Berman. 1991. Stimulation of collagen and glycosaminoglycan production in cultured human adult dermal fibroblasts by recombinant human interleukin 6. J. Invest. Dermatol. 97:686-692.
54. Kawaguchi, Y., M. Hara, and T.M. Wright. 1999. Endogenous IL-1α from systemic sclerosis fibroblasts induces IL-6 and PDGF-A. J. Clin. Invest. 103:1253-1260.
55. Kÿberle, F. 1974. Pathogenesis of Chagas' disease. Ciba Found. Symp. 20:137-147.
56. Andrade, Z.A. 1983. Mechanisms of myocardial damage in Trypanosoma cruzi infection. Ciba Found. Symp. 99:214-233.
57. Gruol, D.L., and T.E. Nelson. 1997. Physiological and pathological roles of interleukin-6 in the central nervous system. Mol. Neurobiol. 15:307-339.
58. Tafuri, W.L. 1970. Pathogenesis of lesions of the autonomic nervous system of the mouse in experimental acute Chagas' disease. Am. J. Trop. Med. Hyg. 19:405-417.
59. Ming, M., M. Chuenkova, E. Ortega-Barria, and M.E.A. Pereira. 1993. Mediation of Trypanosoma cruzi invasion by sialic acid on the host cell and trans-sialidase on the trypanosomes. Mol. Biochem. Parasitol. 59:243-252.
60. Schenkman, R.P., F. Vandekerckhove, and S. Schenkman. 1993. Mammalian cell sialic acid enhances Trypanosoma cruzi invasion. Infect. Immun. 61:898-902.
61. Cavalesco, R., and M.E.A Pereira. 1988. Antibody to Trypanosoma cruzi neuraminidase enhances infection in vitro and identifies a subpopulation of trypomastigotes. J. Immunol. 140:617-625.
62. Prioli, R.P., J.S. Mejia, and M.E.A. Pereira. 1990. Monoclonal antibodies against Trypanosoma cruzi neuraminidase reveal enzyme polymorphism, recognize a subset of trypomastigotes, and enhance infection in vitro. J. Immunol. 144:4384-4389.
63. Costa, F., G. Franchin, V.L. Pereira-Chioccola, M. Riberao, S. Schenkman, and M.M. Rodrigues. 1998. Immunization with a plasinid DNA containing the gene of trans-sialidase reduces Trypanosoma cruzi infection in mice. Vaccine. 16:768-774.
64. Leguizamon, M.S., O.E. Campetella, S.M. Gonzalez Cappa, and A.C.C. Frasch. 1994. Mice infected with Trypanosoma cruzi produce antibodies against the enzymatic domain of trans-sialidase that inhibit its activity. Infect. Immun. 62:3441-3446.
65. Franchin, G., V.L. Pereira-Chioccola, S. Schenkman, and M.M. Rodrigues. 1997. Passive transfer of a monoclonal antibody specific for a sialic acid-dependent epitope on the surface of Trypanosoma cruzi trypomastigotes reduces infection in mice. Infect. Immun. 65:2548-2554.