R.M.O. Watanabe et al. / Biochimie 92 (2010) 933e939
939
for performing platelet aggregation test. This work was supported by
grants from Fundação de Amparo à Pesquisa do Estado de São Paulo
[16] T. Friedrich, B. Kroger, S. Bialojan, H.G. Lemaire, H.W. Hoffken,
P. Reuschenbach, M. Otte, J. Dodt, A Kazal-type inhibitor with thrombin
specificity from Rhodnius prolixus. J. Biol. Chem. 268 (1993) 16216e16222.
(
05/03514-9) and Conselho Nacional de Desenvolvimento Científico
[
17] K. Mende, O. Petoukhova, V. Koulitchkova, G.A. Schaub, U. Lange, R. Kaufmann,
G. Nowak, Dipetaliogastin, a potent thrombin inhibitor from the blood-
sucking insect. Dipetalogaster maximus cDNA cloning, expression and char-
acterization. Eur. J. Biochem. 266 (1999) 583e590.
e Tecnológico (470070/2004-8; 575829/2008-7). R.M.O Watanabe
was supported with a fellowship by FAPESP (07/56614-6).
[
18] I.T. Campos, R. Amino, C.A. Sampaio, E.A. Auerswald, T. Friedrich, H.G. Lemaire,
S. Schenkman, A.S. Tanaka, 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)
References
991e997.
[
[
[
[
[
1] H. Briegel, Excretion of proteolytic enzymes by Aedes aegypti after a blood
[19] I.T. Campos, A.M. Tanaka-Azevedo, A.S. Tanaka, Identification and character-
ization of a novel factor XIIa inhibitor in the hematophagous insect, Triatoma
infestans (Hemiptera: Reduviidae). FEBS Lett. 577 (2004) 512e516.
[20] D.J. Gubler, The global emergence/resurgence of arboviral diseases as public
health problems. Arch. Med. Res. 33 (2002) 330e342.
[21] J.M. Ribeiro, B. Arca, F. Lombardo, E. Calvo, V.M. Phan, P.K. Chandra, S.K. Wikel,
An annotated catalogue of salivary gland transcripts in the adult female
mosquito, Aedes aegypti. BMC Genomics 8 (2007) 6.
meal. J. Insect Physiol. 21 (1975) 1681e1684.
2] M. Eguchi, Protein protease inhibitors in insects and comparison with
mammalian inhibitors. Comp. Biochem. Physiol. B. 105 (1993) 449e456.
3] M.R. Kanost, Serine proteinase inhibitors in arthropod immunity. Dev. Comp.
Immunol. 23 (1999) 291e301.
4] J. Travis, J. Potempa, H. Maeda, Are bacterial proteinases pathogenic factors?
Trends Microbiol. 3 (1995) 405e407.
5] E.W. Davie, K. Fujikawa, K. Kurachi, W. Kisiel, The role of serine proteases in
the blood coagulation cascade. Adv. Enzymol. Relat. Areas Mol. Biol. 48 (1979)
[22] R. Chenna, H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins,
J.D. Thompson, Multiple sequence alignment with the clustal series of
programs. Nucleic Acids Res. 31 (2003) 3497e3500.
277e318.
[
[
[
6] N.D. Rawlings, F.R. Morton, C.Y. Kok, J. Kong, A.J. Barrett, MEROPS: the
peptidase database. Nucleic Acids Res. 36 (2008) D320eD325.
7] M. Laskowski Jr., I. Kato, Protein inhibitors of proteinases. Annu. Rev. Biochem.
[23] U.K. Laemmli, Cleavage of structural proteins during the assembly of the head
of bacteriophage T4. Nature 227 (1970) 680e685.
[24] M.M. Bradford, A rapid and sensitive method for the quantitation of micro-
gram quantities of protein utilizing the principle of protein-dye binding. Anal.
Biochem. 72 (1976) 248e254.
[25] J.F. Morrison, Kinetics of the reversible inhibition of enzyme-catalysed
reactions by tight-binding inhibitors. Biochim. Biophys. Acta 185 (1969)
269e286.
[26] M. Dixon, The determination of enzyme inhibitor constants. Biochem. J. 55
(1953) 170e171.
4
9 (1980) 593e626.
8] Z. Liang, L. Sottrup-Jensen, A. Aspan, M. Hall, K. Soderhall, Pacifastin, a novel
55-kDa heterodimeric proteinase inhibitor containing a unique transferrin
1
chain. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 6682e6687.
[
9] R.A. Boigegrain, H. Mattras, M. Brehelin, P. Paroutaud, M.A. Coletti-Previero,
Insect immunity: two proteinase inhibitors from hemolymph of Locusta
migratoria. Biochem. Biophys. Res. Commun. 189 (1992) 790e793.
[
[
[
[
[
[
10] A. van de Locht, D. Lamba, M. Bauer, R. Huber, T. Friedrich, B. Kroger,
W. Hoffken, W. Bode, 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) 5149e5157.
11] C.P. Sommerhoff, C. Sollner, R. Mentele, G.P. Piechottka, E.A. Auerswald,
H. Fritz, A Kazal-type inhibitor of human mast cell tryptase: isolation from the
medical leech Hirudo medicinalis, characterization, and sequence analysis.
Biol. Chem. Hoppe-Seyler 375 (1994) 685e694.
12] D.V. Lovato, I.T. Nicolau de Campos, R. Amino, A.S. Tanaka, The full-length
cDNA of anticoagulant protein infestin revealed a novel releasable Kazal
domain, a neutrophil elastase inhibitor lacking anticoagulant activity. Bio-
chimie 88 (2006) 673e681.
13] Y. Gonzalez, T. Pons, J. Gil, V. Besada, M. Alonso-del-Rivero, A.S. Tanaka,
M.S. Araujo, M.A. Chavez, Characterization and comparative 3D modeling of
CmPI-II, a novel ‘non-classical’ Kazal-type inhibitor from the marine snail
Cenchritis muricatus (Mollusca). Biol. Chem. 388 (2007) 1183e1194.
14] P. Takac, M.A. Nunn, J. Meszaros, O. Pechanova, N. Vrbjar, P. Vlasakova,
M. Kozanek, M. Kazimirova, G. Hart, P.A. Nuttall, M. Labuda, Vasotab, a vaso-
active peptide from horse fly Hybomitra bimaculata (Diptera, Tabanidae)
salivary glands. J. Exp. Biol. 209 (2006) 343e352.
[27] R.M. Moll, W.S. Romoser, M.C. Modrzakowski, A.C. Moncayo, K. Lerdthusnee,
Meconial peritrophic membranes and the fate of midgut bacteria during
mosquito (Diptera: Culicidae) metamorphosis. J. Med. Entomol. 38 (2001)
29e32.
[28] G. Lipps, R. Fullkrug, E. Beck, Cathepsin B of Schistosoma mansoni. Purification
and activation of the recombinant proenzyme secreted by Saccharomyces
cerevisiae. J. Biol. Chem. 271 (1996) 1717e1725.
[29] W. Gish, D.J. States, Identification of protein coding regions by database
similarity search. Nat. Genet. 3 (1993) 266e272.
[30] H. Nielsen, J. Engelbrecht, S. Brunak, G. von Heijne, A neural network method
for identification of prokaryotic and eukaryotic signal peptides and prediction
of their cleavage sites. Int. J. Neural. Syst. 8 (1997) 581e599.
[31] R.N. Araujo, I.T. Campos, A.S. Tanaka, A. Santos, N.F. Gontijo, M.J. Lehane,
M.H. Pereira, Brasiliensin: a novel intestinal thrombin inhibitor from Triatoma
brasiliensis (Hemiptera: Reduviidae) with an important role in blood intake.
Int. J. Parasitol. 37 (2007) 1351e1358.
[32] F. Jimenez-Vega, F. Vargas-Albores, A four-Kazal domain protein in Litope-
naeus vannamei hemocytes. Dev. Comp. Immunol. 29 (2005) 385e391.
[33] V. Rimphanitchayakit, A. Tassanakajon, Structure and function of invertebrate
Kazal-type serine proteinase inhibitors. Dev. Comp. Immunol. (2009).
[34] F.G. Noriega, M.A. Wells, A molecular view of trypsin synthesis in the midgut
of Aedes aegypti. J. Insect Physiol. 45 (1999) 613e620.
15] S. Donpudsa, A. Tassanakajon, V. Rimphanitchayakit, Domain inhibitory and
bacteriostatic activities of the five-domain Kazal-type serine proteinase
inhibitor from black tiger shrimp Penaeus monodon. Dev. Comp. Immunol. 33
[35] H. Briegel, A.O. Lea, Relationship between protein and proteolytic activity in
the midgut of mosquitoes. J. Insect. Physiol. 21 (1975) 1597e1604.
(
2009) 481e488.