Kazal-type inhibitors in the stomach of Panstrongylus megistus (Triatominae, Reduviidae)

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 4, 2010, Pages 345-353

  Meiser, Christian Karl ^a   Piechura, Heike ^b   Werner, Tanja ^a   Dittmeyer Schäfer, Saskia ^a   Meyer, Helmut E ^b   Warscheid, Bettina ^b,c   Schaub, Günter A ^a   Balczun, Carsten ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c Clinical and Cellular Proteomics   (Germany)

Author keywords

Chromatography; Kazal type inhibitors; MALDI TOF MS; Panstrongylus megistus; Serine proteases; Triatominae; Zymography

Indexed keywords

INSECT PROTEIN; SERINE PROTEINASE INHIBITOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BLOOD CLOTTING TEST; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; OPEN READING FRAME; PANSTRONGYLUS; STOMACH; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; BLOOD COAGULATION TESTS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HUMANS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; OPEN READING FRAMES; PANSTRONGYLUS; SERINE PROTEINASE INHIBITORS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STOMACH;

PANSTRONGYLUS; PANSTRONGYLUS MEGISTUS; REDUVIIDAE; TRIATOMINAE;

EID: 77950368589     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.02.011     Document Type: Article

References (55)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
2. Andrade B.B., Teixeira C.R., Barral A., and Barral-Netto M. Haematophagous arthropod saliva and host defense system: a tale of tear and blood. Ann. Acad. Bras. Cienc 77 (2005) 665-693
3. Araujo R.N., Campos I.T.N., Tanaka A.S., Santos A., Gontijo N.F., Lehane M.J., and Pereira M.H. Brasiliensin: a novel intestinal thrombin inhibitor from Triatoma brasiliensis (Hemiptera: Reduviidae) with an important role in blood intake. Int. J. Parasitol. 37 (2007) 1351-1358
4. Azambuja P., Feder D., and Garcia E.S. Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp. Parasitol. 107 (2004) 89-96
5. Barbosa S.E., Soares R.P.P., Pires H.H.R., and Diotaiuti L. Experimental evidence for a demographic cline in Panstrongylus megistus populations. Mem. Inst. Oswaldo Cruz 96 (2001) 773-775
6. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340 (2004) 783-795
7. Britton H.T.S., and Robinson R.A. Universal buffer solution and the dissociation constant of veronal. J. Chem. Soc. 198 (1931) 1456-1462
8. Campos I.T.N., Amino R., Sampaio C.A.M., Auerswald E.A., Friedrich T., Lemaire H.-G., Schenkman S., and 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 Biochem. Mol. Biol. 32 (2002) 991-997
9. Campos I.T., Tanaka-Azevedo A.M., and Tanaka A.S. Identification and characterization of a novel factor XIIa inhibitor in the hematophagous insect, Triatoma infestans (Hemiptera: Reduviidae). FEBS Lett. 577 (2004) 512-516
10. Chagas C. Über eine neue Trypanosomiasis des Menschen. Mem. Inst. Oswaldo Cruz 1 (1909) 159-218
11. Eichler S., and Schaub G.A. Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Exp. Parasitol. 100 (2002) 17-27
12. Eichler S., Reintjes N., Jung M., Yassin A.F., Schaal K.P., Junqueira A., Coura J.R., and Schaub G.A. Identification of bacterial isolates and symbionts from wild populations of Triatoma infestans and T. sordida. XXIII. Annual Meeting on Basic Research in Chagas' Disease, Caxambu 1996. Mem. Inst. Oswaldo Cruz 91 Suppl. (1996) 125
13. Figueiredo A.R., Peregrino da Silva M.A., Hofer E., de Moraes A.M.L., Oliveira P.C., and Coura J.R. Microorganisms of the Triatominae vectors of Trypanosoma cruzi. Microorganismos de triatomíneos vetores do Trypanosoma cruzi. III-Isolamento e caracterizaçao de bactérias e fungos do trato digestivo de P. megistus negativos e positivos para T. cruzi. Mem. Inst. Oswaldo Cruz 85 Suppl. 1 (1990) 114
14. Forattini O.P. Biogeografia, origem e distribuição da domiciliação de triatomíneos no Brasil. Rev. Saúde Pública 14 (1980) 265-299
15. Friedrich T., Kröger B., Bialojan S., Lemaire H.G., Höffken H.W., Reuschenbach P., Otte M., and Dodt J. A Kazal-type inhibitor with thrombin specificity from Rhodnius prolixus. J. Biol. Chem. 268 (1993) 16216-16222
16. Friend W.G., and Smith J.J.B. La fisiologia de los triatominos con especial referencia a la alimentacion por sangre. In: Carcavallo R.U., Rabinovich J.E., and Tonn R.J. (Eds). Factores biologicos y ecologicos en la enfermedad de Chagas (1985), OPS/ECO, MSAS/SNCh, Buenos Aires, Argentinia 55-72
17. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., and Bairoch A. Protein identification and analysis tools on the ExPASy server. In: Walker J.M. (Ed). The Proteomics Protocols Handbook (2005), Humana, New York 571-607
18. Hellmann K., and Hawkins R.I. Anticoagulant and fibrinolytic activities from Rhodnius prolixus Stål. Nature 201 (1964) 1008-1009
19. Hellmann K., and Hawkins R.I. Prolixins-S and prolixin-G; two anticoagulants from Rhodnius prolixus Stål. Nature 207 (1965) 265-267
20. Hellmann K., and Hawkins R.I. An antithrombin (maculatin) and a plasminogen activator extractable from the blood-sucking hemipteran, Eutriatoma maculatus. Br. J. Haematol. 12 (1966) 376-384
21. Henning L. WinPep 2.11: novel software for PC-based analyses of amino acids sequences. Prep. Biochem. Biotechnol. 31 (2001) 201-207
22. Johansson M.W., Keyser P., and Söderhäll K. Purification and cDNA cloning of a four-domain Kazal proteinase inhibitor from crayfish blood cells. Eur. J. Biochem. 223 (1994) 389-394
23. Kazal L.A., Spicer D.S., and Brahinsky R.A. Isolation of a crystalline trypsin inhibitor-anticoagulant protein from pancreas. J. Am. Chem. Soc. 70 (1948) 3034-3040
24. Kazimírová M., Sulanová M., Trimnellt A.R., Kozánek M., Vidlicka L., Labuda M., and Nuttall P.A. Anticoagulant activities in salivary glands of tabanid flies. Med. Vet. Entomol 16 (2002) 301-309
25. Kollien A.H., and Schaub G.A. The development of Trypanosoma cruzi in Triatominae. Parasitol. Today 16 (2000) 381-387
26. Lange U., Keilholz W., Schaub G.A., Landmann H., Markwardt F., and Nowak G. Biochemical characterization of a thrombin inhibitor from the bloodsucking bug Dipetalogaster maximus. Haemostasis 29 (1999) 204-211
27. Laskowski M., and Kato I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 49 (1980) 593-626
28. Lovato D.V., de Campos I.T.N., Amino R., and 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 88 (2006) 673-681
29. Mägert H.-J., Ständker L., Kreutzmann P., Zucht H.-D., Reinecke M., Sommerhoff C.P., Fritz H., and Forssmann W.-G. LEKTI, a novel 15-domain type of human serine proteinase inhibitor. J. Biol. Chem. 274 (1999) 21499-21502
30. Mende K., Petoukhova O., Koulitchkova V., Schaub G.A., Lange U., Kaufmann R., and Nowak G. Dipetalogastin, a potent thrombin inhibitor from the blood-sucking insect Dipetalogaster maximus: cDNA cloning, expression and characterization. Eur. J. Biochem. 266 (1999) 583-590
31. Mende K., Lange U., and Nowak G. Three recombinant serine proteinase inhibitors expressed from the coding region of the thrombin inhibitor dipetalogastin. Insect Biochem. Mol. Biol. 34 (2004) 971-979
32. Moraes A.M.L., Junqueira A.C.V., Costa G.L., Celano V., Oliveira P.C., and Coura J.R. Fungal flora of the digestive tract of 5 species of triatomines vectors of Trypanosoma cruzi, Chagas 1909. Mycopathologia 151 (2001) 41-48
33. Neuhoff V., Arold N., Taube D., and Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9 (1988) 255-262
34. Nicholas K.B., Nicholas H.B., and Deerfield D.W. GeneDoc, analysis and visualization of genetic variation. Embnet News 4 (1997) 1-4
35. Noeske-Jungblut C., Haendler B., Donner P., Alagon A., Possani L., and Schleuning W.-D. Triabin, a highly potent exosite inhibitor of thrombin. J. Biol. Chem. 270 (1995) 28629-28634
36. Pereira M.H., Souza M.E.L., Vargas A.P., Martins M.S., Penido C.M., and Diotaiuti L. Anticoagulant activity of Triatoma infestans and Panstrongylus megistus saliva (Hemiptera/Triatominae). Acta Trop. 61 (1996) 255-261
37. Pereira M.H., Gontijo N.F., Guarneri A.A., Sant'Anna M.R.V., and Diotaiuti L. Competitive displacement in Triatominae: the Triatoma infestans success. Trends Parasitol. 22 (2006) 516-520
38. Pszenny V., Angel S.O., Duschak V.G., Paulino M., Ledesma B., Yabo M.I., Guarnera E., Ruiz A.M., and Bontempi E.J. Molecular cloning, sequencing and expression of a serine proteinase inhibitor gene from Toxoplasma gondii. Mol. Biochem. Parasitol. 107 (2000) 241-249
39. Ribeiro J.M.C., Schneider M., and Guimarães J.A. Purification and characterization of prolixin S (nitrophorin 2), the salivary anticoagulant of the blood-sucking bug Rhodnius prolixus. Biochem. J. 308 (1995) 243-249
40. Ribeiro J.M., Schneider M., Isaias T., Jurberg J., Galvão C., and Guimarães J.A. Role of salivary antihemostatic components in blood feeding by triatomine bugs (Heteroptera). J. Med. Entomol. 35 (1998) 599-610
41. Sant'Anna M.R.V., Diotaiuti L., de Figueiredo Gontijo A., de Figueiredo Gontijo N., and Pereira M.H. Feeding behaviour of morphologically similar Rhodnius species: influence of mechanical characteristics and salivary function. J. Insect Physiol. 47 (2001) 1459-1465
42. Schägger H., and von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166 (1987) 368-379
43. Schaub G.A. Trypanosoma cruzi: quantitative studies of development of two strains in small intestine and rectum of the vector Triatoma infestans. Exp. Parasitol. 68 (1989) 260-273
44. Schaub G.A. Kissing bugs. In: Mehlhorn H. (Ed). Encyclopedia of Parasitology. third ed. vol. 1 (2008), Springer-Verlag, Heidelberg 684-686
45. Schlott B., Wöhnert J., Icke C., Hartmann M., Ramachandran R., Gührs K.-H., Glusa E., Flemming J., Görlach M., Große F., and Ohlenschläger O. Interaction of Kazal-type inhibitor domains with serine proteinases: biochemical and structural studies. J. Mol. Biol. 318 (2002) 533-546
46. Schofield C.J., and Dias J.C. The Southern Cone initiative against Chagas disease. Adv. Parasitol. 42 (1999) 1-27
47. Schofield C.J., Diotaiuti L., and Dujardin J.P. The process of domestication in Triatominae. Mem. Inst. Oswaldo Cruz 94 Suppl. 1 (1999) 375-378
48. Sørensen S.P.L. Enzymstudien. II: Mitteilung. Über die Messung und die Bedeutung der Wasserstoffionenkonzentration bei enzymatischen Prozessen. Biochem. Z. 21 (1909) 131-304
49. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
50. Tian M., Huitema E., Da Cunha L., Torto-Alalibo T., and Kamoun S. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279 (2004) 26370-26377
51. van de Locht A., Lamba D., Bauer M., Huber R., Friedrich T., Kröger B., Höffken W., and Bode W. Two heads are better than one: crystal structure of the insect derived double domain Kazal inhibitor rhodniin in complex with thrombin. EMBO J. 14 (1995) 5149-5157
52. Villela M.M., Souza J.B., Mello V.P., Azeredo B.V.M., and Dias J.C.P. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad. Saúde Pública 21 (2005) 878-886
53. Voigt C.C., Fassbender M., Dehnhard M., Wibbelt G., Jewgenow K., Hofer H., and Schaub G.A. Validation of a minimally invasive blood-sampling technique for the analysis of hormones in domestic rabbits, Oryctolagus cuniculus (Lagomorpha). Gen. Comp. Endocrinol. 135 (2004) 100-107
54. Wang Z.-H., Zhao X.-F., and Wang J.-X. Characterization, kinetics, and possible function of Kazal-type proteinase inhibitors of Chinese white shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol. 26 (2009) 885-897
55. Whitelock J.M., O'Grady R.L., and Gibbins J.R. The identification, purification and characterisation of an inhibitor of collagenase (20 K) produced by neoplastic epithelial cells. Biochim. Biophys. Acta 1073 (1991) 107-113