Leishmania-induced tyrosine phosphorylation in the host macrophage and its implication to infection

European Journal of Cell Biology

Volumn 71, Issue 2, 1996, Pages 206-215

  Martiny, Andrea ^a   Vannier Santos, Marcos A ^a   Borges, Valéria M ^a   Meyer Fernandes, José R ^a,b   Assreuy, Jamil ^a   Cunha E Silva, Narcisa L ^a   De Souza, Wanderley ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Cell signaling; Leishmania; Nitric oxide; Protein phosphatase; Protein tyrosine kinase (PTK); Tyrosine phosphorylation

Indexed keywords

GENISTEIN; HERBIMYCIN A; NITRIC OXIDE; PHOSPHOSERINE; PHOSPHOTHREONINE; PHOSPHOTYROSINE; STAUROSPORINE; TYRPHOSTIN; VANADATE SODIUM;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; HOST CELL; HOST PARASITE INTERACTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOGOLD STAINING; INTERNALIZATION; LEISHMANIA; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN PHOSPHORYLATION;

ANIMALIA; MURINAE;

EID: 0029860530     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (77)

1. TDR/WHO, 7th programme report (1984).
2. Alexander, J., D. G. Russell: The interaction of Leishmania species with macrophages. Adv. Parasitol. 31, 175-254 (1992).
3. Akiyama, T., H. Ogawara: Use and specificity of genistein as inhibitor of protein-tyrosine kinases. Methods. Enzymol. 201, 362-370 (1991).
4. Bakalara, N., A. Seyfang, T. Baltz, C. Davis: Trypanosoma brucei and Trypanosoma cruzi: life cycle-regulated protein tyrosine phosphatase activity. Exp. Parasitol. 81, 302-312 (1995).
5. Bakhiet, M., E. Mix, K. Kristensson, H. Wigzell, T. Olsson: T cell activation by a Trypanosoma brucei-derived lymphocyte triggering factor is dependent on tyrosine protein kinase but not on protein kinase C and A. Eur. J. Immunol. 23, 1535-1539 (1993).
6. Benaim, G., P. J. Romero: A calcium pump in plasma membrane vesicles from Leishmania braziliensis. Biochim. Biophys. Acta 1027, 79-84 (1990).
7. Bianco, C., F. M. Griffin Jr., S. C. Silverstein: Studies of macrophage complement receptor: alteration of receptor function upon macrophage activation. J. Exp. Med. 141, 1278-1290 (1975).
8. Bliska, J. B., J. E. Galán, S. Falkow: Signal transduction in the mammalian cell during bacterial attachment and entry. Cell 73, 903-920 (1993).
9. Bradford, M. M.: A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).
10. Cantley, L. C., P. Aisen: The fate of cytoplasmic vanadium: implications on (Na,K)-ATPase inhibition. J. Biol. Chem. 254, 1781-1784 (1979).
11. Chang, K. P.: Human cuntaneous Leishmania in a mouse macrophage cell line: propagation and isolation of intracellular parasites. Science 209, 1240-1242 (1980).
12. Clark, E. A., J. S. Brugge: Integrins and signal transduction pathways: the road taken. Science 268, 233-239 (1995).
13. Cunha, V. M., J. R. Meyer-Fernandes, F. Noel: A (Ca2+-Mg2+) ATPase from Schistosoma mansoni is coupled to an active transport of calcium. Mol. Biochem. Parasitol. 52, 167-173 (1992).
14. Dekker, L. V., P. J. Parker: Protein kinase C - a question of specificity? Trends Biochem. Sci. 19, 73-77 (1994).
15. Dell, K. R., J. N. Engel: Stage-specific regulation of protein phosphorylation in Leishmania major. Mol. Biochem. Parasitol. 64, 283-292 (1994).
16. DePierre, J. W., M. L. Karnovsky: Ecto-enzymes of the guinea pig polymorphonuclear leukocyte. 1. evidence for an ecto-adenosine monophosphatase, adenosine triphosphatase, and p-nitrophenyl phosphatase. J. Biol. Chem. 249, 7111-7120 (1974).
17. Descoteaux, A., S. J. Turco: The lipophosphoglycan of Leishmania and macrophage protein kinase C. Parasitol. Today 9, 468-471 (1993).
18. Fisher, E. H., H. Charbonneauh, N. K. Tonks: Protein tyrosine phosphatase: a diverse family of intracellular and transmembrane enzymes. Science 253, 401-406 (1991).
19. Galán, J. E., J. Pace, M. J. Hayman: Involvement of the epidermal growth factor receptor in the mammalian cells by Salmonella typhimurium. Nature 357, 588-589 (1992).
20. Geng, Y., B. Zhang, M. Lotz: Protein tyrosine kinase is required for lipopolysaccharide induction of cytokines in human blood monocytes. J. Immunol. 151, 66292-6700 (1993).
21. Glaser, K. B., A. Sung, J. Bauer, B. M. Weichman: Regulation of eicosanoid biosynthesis in the macrophage: involvement of protein tyrosine phosphorylation and modulation by selective protein tyrosine kinase inhibitors. Biochem. Pharmacol. 45, 711-721 (1993).
22. Glew, R. H., A. K. Saha, S. Das, A. T. Remaley: Biochemistry of Leishmania species. Microbiol. Rev. 52, 412-432 (1988).
23. Gordon, J. A.: Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol. 201, 477-482 (1991).
24. Green, C. L., D. A. Wagner, J. Glogowski, P. L. Skipper, J. S. Wishnok, S. R. Tannenbaum: Analysis of nitrate, nitrite and [15N]nitrate in biological fluids. Anal. Biochem. 126, 131-138 (1982).
25. Green, S. J., C. A. Nacy, M. S. Meltzeer: Cytokine-induced synthesis of nitrogen oxides in macrophages: a protective host response to Leishmania and other intracellular pathogens. J. Leuk. Biol. 50, 93-103 (1991).
26. Greenberg, S.: Signal transduction of phagocytosis. Trends Cell Biol. 5, 93-99 (1995).
27. Greenberg, S., P. Chang, S. C. Silverstein: Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177, 529-534 (1993).
28. Greenberg, S., S. C. Silverstein: Phagocytosis. In: W. W. Paul (ed.): Fundamental Immunology, pp. 941-964. Raven Press, 3rd ed. New York 1991.
29. Greenlund, A. C., M. A. Farrar, B. L. Viviano, R. D. Schreiber: Ligand-induced IFNγ receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91). EMBO J. 13, 1591-1600 (1994).
30. Hanks, S. K., M. B. Calalb, M. C. Harper, S. K. Patel: Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl. Acad. Sci. USA 89, 8487-8491 (1989).
31. Hunter, T.: Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225-236 (1995).
32. Indik, Z. K., J. C. Park, X. Q. Pan, A. D. Schreiber: Induction of phagocytosis by a protein tyrosine kinase. Blood 85, 1175-1180 (1995).
33. Isberg, R. R., G. Tran Van Nhieu: Binding and internalization of microorganisms by integrin receptors. Trends Microbiol. 2, 10-14 (1994).
34. Kardami, E., T. W. Pearson, R. P. Beecroft, R. R. Fandrich: Identification of basic fibroblast growth factor-like proteins in african trypanosoma and Leishmania. Mol. Biochem. Parasitol. 51, 171-182 (1992).
35. Klarlund, J.: Transformation of cells by an inhibitor of phosphatases acting on phosphotyrosine proteins. Cell 41, 707-717 (1985).
36. Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
37. Levitzki, A., A. Gazit, N. Osherov, I. Posner, C. Gilon: Inhibition of protein-tyrosine kinases by tyrphostins. Methods Enzymol. 201, 347-363 (1991).
38. Li, Z.-Y., C. L. Manthey, P. Y. Perera, A. Sher, S. N. Vogel: Toxoplasma gondii soluble antigen induces a subset of lipopolysaccharide-inducible genes and tyrosine phosphoproteins in peritoneal macrophages. Infect. Immun. 62, 3434-3440 (1994).
39. Liew, F. Y.: The role of nitric oxide in parasitic diseases. Ann. Trop. Mod. Parasitol. 87, 637-642 (1993).
40. Lovelace, J. K., D. M. Dwyer, M. Gottlieb: Purification and characterization of the extracellular acid phosphatase of Leishmania donovani. Mol. Biochem. Paratisol. 20, 243-251 (1986).
41. Mitsuyama, T., K. Takeshige, S. Minakami: Tyrosine phosphorylation is involved in the respiratory burst of electropermeabilized human neutrophils at a step before diacylglycerol formation by phospholipase C. FEBS Lett. 322, 280-284 (1993).
42. Moore, K. J., S. Labrecque, G. Mathlashewski, G.: Alteration of Leishmania donovani infection levels by selective impairment of macrophage signal transduction. J. Immunol. 150, 4457-4465 (1993).
43. Morisaki, J. H., J. E. Heuser, L. D. Sibley: Invasion of Toxoplasma gondii occurs by active penetration of the host cell. J. Cell Sci. 108, 2457-2464 (1995).
44. Mosser, D. M., L. A. Rosenthal: Leishmania-macrophage interactions: multiple receptors, mutiple ligands and diverse cellular responses. Semin. Cell Biol. 4, 315-322 (1993).
45. Murray, H. W.: Pretreatment with phorbol myristate acetate inhibits macrophage activity against intracellular protozoa. RES: J Reticuloendoth. Soc. 31, 479-487 (1982).
46. Nandan, D., E. N. Reiner: Attenuation of gamma-interferon-induced tyrosine phosphorylation in mononuclear phagocytes infected with Leishmania donovani: selective inhibition of signaling through janus kinases and stat1. Infect. Immun. 63, 4495-4500 (1995).
47. Olivier, M., K. J. Baimbridge, N. E. Reiner: Stimulus-response coupling in monocytes infected with Leishmania. Attenuation of calcium transients is related to defective agonist-induced accumulation of inositol phosphates. J. Immunol. 148, 1188-1196 (1992).
48. O'Neal, S. G., D. B. Rhoads, E. Racker: Vanadate inhibition of sarcoplasmic reticulum Ca2+-ATPase and other ATPases. Biochem. Biophys. Res. Commun. 89, 845-850 (1979).
49. Pace, J., M. J. Hayman, J. E. Galán: Signal transduction and invasion of epithelial cells by S. typhimurium. Cell 72, 505-514 (1993).
50. Pan, M. G., T. Florio, P. J. Stork: G protein activation of a hormone-stimulated phosphatase in human tumor cells. Science 256, 1215-1217 (1992).
51. Parsons, C. J., M. D. Schaller, J. Hildebrand, T. H. Leu, A. Richardson, C. Otey: Focal adhesion kinase: structure and signaling. J. Cell Sci. 18S, 109-113 (1994).
52. Rangachari, K., A. Dluzewski, R. J. M. Wilson, W. M. Gratzer: Control of malarial invasion by phosphorylation of the host cell membrane cytoskeleton. Nature 324, 364-365 (1986).
53. Reiner, N. E.: Altered cell signaling and mononuclear phagocyte deactivation during intracellular infection. Immunol. Today 15, 347-381 (1994).
54. Reiner, N. E., C. J. Malemud: Arachidonic acid metabolism by murine peritoneal macrophages infected with Leishmania donovani: in vitro evidence for parasite induced alterations in cyclooxygenase and lipooxygenase pathways. J. Immunol. 134, 556-563 (1985).
55. Rosenshine, I., M. S. Donnenberg, J. B. Kaper, B. B. Finlay: Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J. 11, 3551-3560 (1992).
56. Rosenshine, I., V. Duronio, B. B. Finlay: Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect. Immun. 60, 2211-2217 (1992).
57. Saito, S., H. Shinomiya, M. Nakano: Protein phosphorylation in murine peritoneal macrophages induced by infection with Salmonella species. Infect. Immun. 62, 1551-1556 (1994).
58. Schofield, L., P. Gerold, R. T. Schwarz, S. Tachado: Signal transduction in host cells mediated by Glycosylphosphatidylinositols of parasitic protozoa, or why parasitic protozoa have so many GPI molecules? Braz. J. Med. Biol. Res. 27, 249-254 (1994).
59. Souto-Padrón, T., M. B. Reyes, S. Leguizamon, O. E. Campetella, A. C. C. Frasch, W. De Souza: Trypanosoma cruzi proteins which arc antigenic during human infections are located in defined regions of the parasite. Eur. J. Cell Biol. 50, 272-278 (1989).
60. Swarup, G., S. Cohen, D. L. Garbers: Inhibition of membrane phosphotyrosyl-protein phosphatase activity by vanadate. Biochem. Biophys. Res. Commun. 107, 1104-1109 (1982).
61. Tamaoki, T.: Use and specificity of staurosporine, UCN-01, and calphostin C as protein kinase inhibitors. Methods. Enzymol. 201, 340-474 (1991).
62. Townbin, H., T. Staehelin, J. Gordon: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354 (1979).
63. Tsang, V. C. W., J. M. Peralta, A. R. Simons: Enzyme-linked immuno-electrotransfer techniques (EITB) for studing specificities of antigens and antibodies separated by gel electrophoresis. Methods Enzymol. 92, 377-391 (1983).
64. Uehara, Y., H. Fukazawa: Use and selectivity of herbimycin A as inhibitor of protein tyrosine kinases. Methods Enzymol. 201, 370-379 (1991).
65. Ullrich, A., J. Schlessinger: Signal transduction by receptors with tyrosine kinase activity. Cell 61, 203-212 (1990).
66. Van der Bruggen, T., P. T. M. Kok, J. A. M. Raaijmakers, A. J. Verhoeven, R. G. C. Kessels, J. W. J. Lammers, L. Koenderman: Cytokine priming of the respiratory burst in eosinophils is Ca2+ independent and accompanied by induction of tyrosine kinase activity. J. Leuk. Biol. 53, 347-353 (1993).
67. Vannier-Santos, M. A., A. Martiny, J. R. Meyer-Fernandes, W. De Souza: Leishmanial protein kinase C modulates host cell infection via secreted acid phosphatase. Eur. J. Cell Biol. 67, 112-119 (1995).
68. Vannier-Santos, M. A., E. M. B. Saraiva, A. Martiny, A. Neves, W. De Souza: Fibronectin shedding by Leishmania may influence the parasite-macrophage interaction. Eur. J. Cell Biol. 59, 389-397 (1992).
69. Yamamoto, Y., T. W. Klein, H. Shinomyia, M. Nakano, N. Friedman: Infection of macrophages with Legionella pneumophila induces phosphorylation of a 76 kDa protein. Infect. Immun. 60, 3452-3455 (1992).
70. Ward, G. E., H. Fugioka, M. Aikawa, L. H. Miller: Staurosporine inhibits invasion of erythrocytes by malarial merozoites. Exp. Parasitol. 79, 480-487 (1994).
71. Wei, H., L. Wei, K. Frenkel, R. Bowen, S. Barnes: Inhibition of tumor promoter-induced hydrogen peroxide formation in vitro and in vivo by genistein. Nutr. Cancer 20, 1-11 (1993).
72. Wick, M. J., J. L. Madara, B. N. Fields, S. J. Normark: Molecular cross talk between epithelial cells and pathogenic microorganisms. Cell 67, 651-659 (1991).
73. Wyler, D. J., J. P. Sypek, J. A. McDonald: In vitro parasite-monocyte interactions in human leishmaniasis: possible role of fibronectin in parasite attachment. Infect. Immun. 49, 305-311 (1985).
74. Zheng, L., P. H. Nibbering, T. P. L. Zomerdijk, R. Van Furth: Protein tyrosine kinase activity is essential for Fcγ receptor-mediated intracellular killing of Staphylococcus aureus by human monocytes. Infect. Immun. 62, 4296-4303 (1994).
75. Zhou, M.-J., E. J. Brown: CR3 (Mac-1, αMβ2, CD11b/CD18) and FcγRIII cooperate in generation of a neutrophil respiratory burst: requirement for FcγRII and tyrosine phosphorylation. J. Cell Biol. 125, 1407-1416 (1994).
76. Zilberstein, D.: Transport of nutrients and ions across membranes of trypanosomatid parasites. Adv. Parasitol. 32, 261-291 (1993).
77. Zilberstein, D., D. M. Dwyer. Identification of a surface membrane proton-translocating ATPase in promastigotes of the parasitic protozoa Leishmania donovani. Biochem. J. 256, 13-21 (1988).