Infestin 1R, an intestinal subtilisin inhibitor from Triatoma infestans able to impair mammalian cell invasion by Trypanosoma cruzi

Experimental Parasitology

Volumn 129, Issue 4, 2011, Pages 362-367

  Lovato, Diogo V ^a   Amino, Rogerio ^a   González, Yamile ^b   Miranda, Antonio ^a   Schenkman, Sergio ^a   Tanaka, Aparecida S ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF HAVANA   (Cuba)

Author keywords

Protease inhibitor; Subtilisin A; Triatoma infestans; Trypanosoma cruzi

Indexed keywords

INFESTIN 1R; MESSENGER RNA; NATURAL PRODUCT; RECOMBINANT PROTEIN; SERINE PROTEINASE INHIBITOR; SUNFLOWER TRYPSIN INHIBITOR 1; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIPROTOZOAL ACTIVITY; ARTICLE; CELL INVASION; CONTROLLED STUDY; DRUG ISOLATION; DRUG MECHANISM; DRUG SYNTHESIS; DRUG TARGETING; HOST PARASITE INTERACTION; HYBRIDIZATION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; TRIATOMA INFESTANS; TRYPANOSOMA CRUZI; TRYPANOSOMIASIS; TRYPOMASTIGOTE;

ANIMALS; CELLS, CULTURED; CHAGAS DISEASE; EPITHELIAL CELLS; HUMANS; INSECT PROTEINS; INSECT VECTORS; MICE; RNA, MESSENGER; SUBTILISIN; TRIATOMA; TRYPANOSOMA CRUZI;

HELIANTHUS; MAMMALIA; TRIATOMA INFESTANS; TRYPANOSOMA CRUZI;

EID: 80455143582     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.09.002     Document Type: Article

References (46)

1. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., Kafatos F.C., Jacobs-Lorena M., Michel K. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:16327-16332.
2. Aparicio I.M., Scharfstein J., Lima A.P. A new cruzipain-mediated pathway of human cell invasion by Trypanosoma cruzi requires trypomastigote membranes. Infection and Immunity 2004, 72:5892-5902.
3. Araujo R.N., Campos I.T., Tanaka A.S., Santos A., Gontijo N.F., Lehane M.J., Pereira M.H. Brasiliensin: A novel intestinal thrombin inhibitor from Triatoma brasiliensis (Hemiptera: Reduviidae) with an important role in blood intake. International Journal for Parasitology 2007, 37:1351-1358.
4. Armstrong P.B., Quigley J.P. A role for protease inhibitors in immunity of long-lived animals. Advances in Experimental Medicine and Biology 2001, 484:141-160.
5. Augustin R., Siebert S., Bosch T.C. Identification of a kazal-type serine protease inhibitor with potent anti-staphylococcal activity as part of Hydra's innate immune system. Developmental and Comparative Immunology 2009, 33:830-837.
6. Bastos I.M., Grellier P., Martins N.F., Cadavid-Restrepo G., de Souza-Ault M.R., Augustyns K., Teixeira A.R., Schrével J., Maigret B., da Silveira J.F., Santana J.M. Molecular, functional and structural properties of the prolyl oligopeptidase of Trypanosoma cruzi (POP Tc80), which is required for parasite entry into mammalian cells. Biochemical Journal 2005, 388:29-38.
7. Burleigh B.A., Andrews N.W. A 120-kDa alkaline peptidase from Trypanosoma cruzi is involved in the generation of a novel Ca(2+)-signaling factor for mammalian cells. The Journal of Biological Chemistry 1995, 270:5172-5180.
8. Burleigh B.A., Caler E.V., Webster P., Andrews N.W. A cytosolic serine endopeptidase from Trypanosoma cruzi is required for the generation of Ca2+ signaling in mammalian cells. The Journal of Cell Biology 1997, 136:609-620.
9. Campos I.T., Amino R., Sampaio C.A., Auerswald E.A., Friedrich T., Lemaire H.G., Schenkman S., Tanaka A.S. Infestin, a thrombin inhibitor presents in Triatoma infestans midgut, a Chagas' disease vector: gene cloning, expression and characterization of the inhibitor. Insect Biochemistry and Molecular Biology 2002, 32:991-997.
10. da Silva-Lopez R.E., Morgado-Díaz J.A., dos Santos P.T., Giovanni-De-Simone S. Purification and subcellular localization of a secreted 75 kDa Trypanosoma cruzi serine oligopeptidase. Acta Tropica 2008, 107:159-167.
11. Danielli A., Kafatos F.C., Loukeris T.G. Cloning and characterization of four Anopheles gambiae serpin isoforms, differentially induced in the midgut by Plasmodium berghei invasion. The Journal of Biological Chemistry 2003, 278:4184-4193.
12. de Marco R., Lovato D.V., Torquato R.J., Clara R.O., Buarque D.S., Tanaka A.S. The first pacifastin elastase inhibitor characterized from a blood sucking animal. Peptides 2010, 31:1280-1286.
13. Dias J.C. Elimination of Chagas disease transmission: perspectives. Memórias do Instituto Oswaldo Cruz 2009, 104(Suppl. 1):41-45.
14. Donpudsa S., Tassanakajon A., Rimphanitchayakit V. Domain inhibitory and bacteriostatic activities of the five-domain Kazal-type serine proteinase inhibitor from black tiger shrimp Penaeus monodon. Developmental and Comparative Immunology 2009, 33:481-488.
15. Ellman G.L. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 1959, 82:70-77.
16. Faudry E., Rocha P.S., Vernet T., Lozzi S.P., Teixeira A.R. Kinetics of expression of the salivary apyrases in Triatoma infestans. Insect Biochemistry and Molecular Biology 2004, 34:1051-1058.
17. Fields G.B., Noble R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. International Journal of Peptide and Protein Research 1990, 35:161-214.
18. Frobius A.C., Kanost M.R., Gotz P., Vilcinskas A. Isolation and characterization of novel inducible serine protease inhibitors from larval hemolymph of the greater wax moth Galleria mellonella. European Journal of Biochemistry 2000, 267:2046-2053.
19. Gonzalez Y., Tanaka A.S., Hirata I.Y., Rivero M.A., Oliva M.L.O., Araujo M.S., Chavez M.A. Purification and preliminary characterization of human neutrophil elastase inhibitors isolated from the marine snail Cenchritis muricatus (Mollusca). Comparative Biochemistry and Physiology. B, Biochemistry & Molecular Biology 1997, 146:506-513.
20. Grellier P., Vendeville S., Joyeau R., Bastos I.M., Drobecq H., Frappier F., Teixeira A.R., Schrevel J., Davioud-Charvet E., Sergheraert C., Santana J.M. Trypanosoma cruzi prolyl oligopeptidase Tc80 is involved in nonphagocytic mammalian cell invasion by trypomastigotes. The Journal of Biological Chemistry 2001, 276:47078-47086.
21. Jannin J., Villa L. An overview of Chagas disease treatment. Memórias do Instituto Oswaldo Cruz 2007, 102(Suppl. 1):95-97.
22. Kanost M.R., Jiang H., Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunology Reviews 2004, 198:97-105.
23. Kazal L.A., Spicer D.S., Brahinsky R.A. Isolation of a crystalline trypsin inhibitor-anticoagulant protein from pancreas. Journal of American Chemical Society 1948, 70:3034-3040.
24. Korsinczky M.L., Schirra H.J., Rosengren K.J., West J., Condie B.A., Otvos L., Anderson M.A., Craik D.J. Solution structures by 1H NMR of the novel cyclic trypsin inhibitor SFTI-1 from sunflower seeds and an acyclic permutant. Journal Molecular Biology 2001, 311:579-591.
25. Lalmanach G. Proteolytic enzymes: from structures to transport pathways. Biochimie 2008, 90:191-193.
26. Lehane M.J., Aksoy S., Gibson W., Kerhornou A., Berriman M., Hamilton J., Soares M.B., Bonaldo M.F., Lehane S., Hall N. Adult midgut expressed sequence tags from the tsetse fly Glossina morsitans morsitans and expression analysis of putative immune response genes. Genome Biology 2003, 4:R63.
27. Lent H., Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas' disease. Bulletin of the American Museum of Natural History 1979, 163:125-520.
28. Levashina E.A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J.A., Reichhart J.M. Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 1999, 285:1917-1919.
29. Lovato D.V., Nicolau de Campos I.T., Amino R., Tanaka A.S. The full-length cDNA of anticoagulant protein infestin revealed a novel releasable Kazal domain, a neutrophil elastase inhibitor lacking anticoagulant activity. Biochimie 2006, 88:673-681.
30. Martinez J., Campetella O., Frasch A.C., Cazzulo J.J. The major cysteine proteinase (cruzipain) from Trypanosoma cruzi is antigenic in human infections. Infection and Immunity 1991, 59:4275-4277.
31. McKerrow J.H., Doyle P.S., Engel J.C., Podust L.M., Robertson S.A., Ferreira R., Saxton T., Arkin M., Kerr I.D., Brinen L.S., Craik C.S. Two approaches to discovering and developing new drugs for Chagas disease. Memórias do Instituto Oswaldo Cruz 2009, 104(Suppl. 1):263-269.
32. Miranda A., Koerber S.C., Gulyas J., Lahrichi S.L., Craig A.G., Corrigan A., Hagler A., Rivier C., Vale W., Rivier J. Conformationally restricted competitive antagonists of human/rat corticotropin-releasing factor. Journal of Medicinal Chemistry 1994, 37:1450-1459.
33. Monteiro A.C., Abrahamson M., Lima A.P., Vannier-Santos M.A., Scharfstein J. Identification, characterization and localization of chagasin, a tight-binding cysteine protease inhibitor in Trypanosoma cruzi. Journal of Cell Science 2001, 114:3933-3942.
34. Nirmala X., Kodrik D., Zurovec M., Sehnal F. Insect silk contains both a Kunitz-type and a unique Kazal-type proteinase inhibitor. European Journal of Biochemistry 2001, 268:2064-2073.
35. Pinto S.B., Kafatos F.C., Michel K. The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cellular Microbiology 2008, 10:891-898.
36. Rawlings N.D., Tolle D.P., Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Research 2004, 32:D160-164.
37. Rawlings N.D., Morton F.R., Kok C.Y., Kong J., Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Research 2008, 36:D320-325.
38. Remme J.H., Feenstra P., Lever P.R., Médici A., Morel C., Noma M., Ramaiah K.D., Richards F., Seketeli A., Schmunis G., van Brakel W.H., Vassall A. Tropical diseases targeted for elimination: Chagas disease, lymphatic filariasis, onchocerciasis and leprosy 2006, Disease Control Priorities in Developing Countries, pp. 433-449.
39. Rimphanitchayakit V., Tassanakajon A. Structure and function of invertebrate Kazal-type serine proteinase inhibitors. Developmental and Comparative Immunology 2010, 34:377-386.
40. Rubin-de-Celis S.S., Uemura H., Yoshida N., Schenkman S. Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cellular Microbiology 2006, 8:1888-1898.
41. Scharfstein J., Schmitz V., Morandi V., Capella M.M., Lima A.P., Morrot A., Juliano L., Muller-Esterl W. Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B(2) receptors. The Journal of Experimental Medicine 2000, 192:1289-1300.
42. Schechter I., Berger A. On the size of the active site in proteases. I. Papain. Biochemical and Biophysical Research Communications 1967, 27:157-162.
43. Tomas A.M., Miles M.A., Kelly J.M. Overexpression of cruzipain, the major cysteine proteinase of Trypanosoma cruzi, is associated with enhanced metacyclogenesis. European Journal of Biochemistry 1997, 244:596-603.
44. Ursic-Bedoya R.J., Lowenberger C.A. Rhodnius prolixus: identification of immune-related genes up-regulated in response to pathogens and parasites using suppressive subtractive hybridization. Developmental and Comparative Immunology 2007, 31:109-120.
45. Wedde M., Weise C., Kopacek P., Franke P., Vilcinskas A. Purification and characterization of an inducible metalloprotease inhibitor from the hemolymph of greater wax moth larvae, Galleria mellonella. European Journal of Biochemistry 1998, 255:535-543.
46. Whitten M., Sun F., Tew I., Schaub G., Soukou C., Nappi A., Ratcliffe N. Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli, T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 2007, 37:440-452.