Identification and characterization of a new kallikrein-kinin system inhibitor from the salivary glands of the malaria vector mosquito Anopheles stephensi

Insect Biochemistry and Molecular Biology

Volumn 37, Issue 5, 2007, Pages 466-477

  Isawa, Haruhiko ^a,b   Orito, Yuki ^b   Iwanaga, Shiroh ^c   Jingushi, Naruhiro ^b   Morita, Akihiro ^b   Chinzei, Yasuo ^b   Yuda, Masao ^b  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b MIE UNIVERSITY   (Japan)

^c KOBE UNIVERSITY   (Japan)

Author keywords

Anopheles stephensi; Blood feeding; Bradykinin; Kallikrein kinin system; Mosquito; Salivary glands

Indexed keywords

BLOOD CLOTTING FACTOR 12; BRADYKININ; COMPLEMENTARY DNA; HIGH MOLECULAR WEIGHT KININOGEN; INSECT PROTEIN; ZINC;

AMINO ACID SEQUENCE; ANIMAL; ANOPHELES; ARTICLE; BINDING SITE; CELL CULTURE; CHEMISTRY; DISEASE CARRIER; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; KALLIKREIN KININ SYSTEM; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SALIVARY GLAND; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; BINDING SITES; BRADYKININ; CELLS, CULTURED; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FACTOR XII; HUMANS; INSECT PROTEINS; INSECT VECTORS; KALLIKREIN-KININ SYSTEM; KININOGEN, HIGH-MOLECULAR-WEIGHT; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SALIVARY GLANDS; SEQUENCE ALIGNMENT; ZINC;

ANIMALIA; ANOPHELES STEPHENSI; HEXAPODA;

EID: 34247119281     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2007.02.002     Document Type: Article

References (40)

1. Arcá B., Lombardo F., de Lara Capurro M., della Torre A., Dimopoulos G., James A.A., and Coluzzi M. Trapping cDNAs encoding secreted proteins from the salivary glands of the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. USA 96 (1999) 1516-1521
2. Bernardo M.M., Day D.E., Halvorson H.R., Olson S.T., and Shore J.D. Surface-independent acceleration of factor XII activation by zinc ions. II. Direct binding and fluorescence studies. J. Biol. Chem. 268 (1993) 12477-12483
3. Bernardo M.M., Day D.E., Olson S.T., and Shore J.D. Surface-independent acceleration of factor XII activation by zinc ions. I. Kinetic characterization of the metal ion rate enhancement. J. Biol. Chem. 268 (1993) 12468-12476
4. Calvo E., Mans B.J., Andersen J.F., and Ribeiro J.M. Function and evolution of a mosquito salivary protein family. J. Biol. Chem. 281 (2006) 1935-1942
5. Citarella F., Wuillemin W.A., Lubbers Y.T.P., and Hack C.E. Initiation of contact system activation in plasma is dependent on factor XII autoactivation and not on enhanced susceptibility of factor XII for kallikrein cleavage. Br. J. Haematol. 99 (1997) 197-205
6. Colman R.W. Surface-mediated defense reactions. The plasma contact activation system. J. Clin. Invest. 73 (1984) 1249-1253
7. Colman RW. Are hemostasis and thrombosis two sides of the same coin?. J. Exp. Med. 203 (2006) 493-495
8. Colman R.W., and Schmaier A.H. Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 90 (1997) 3819-3843
9. DeLa Cadena R.A., and Colman R.W. The sequence HGLGHGHEQQHGLGHGH in the light chain of high molecular weight kininogen serves as a primary structural feature for zinc-dependent binding to an anionic surface. Protein Sci. 1 (1992) 151-160
10. Hasan A.A., Cines D.B., Herwald H., Schmaier A.H., and Muller-Esterl W. Mapping the cell binding site on high molecular weight kininogen domain 5. J. Biol. Chem. 270 (1995) 19256-19261
11. Hasan A.A.K., Zisman T., and Schmaier A.H. Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc. Natl. Acad. Sci. USA. 95 (1998) 3615-3620
12. Herwald H., Dedio J., Kellner R., Loos M., and Müller-Esterl W. Isolation and characterization of the kininogen-binding protein p33 from endothelial cells. Identity with the gC1q receptor. J. Biol. Chem. 271 (1996) 13040-13047
13. Herwald H., Mörgelin M., Svensson H.G., and Sjöbring U. Zinc-dependent conformational changes in domain D5 of high molecular mass kininogen modulate contact activation. Eur. J. Biochem. 268 (2001) 396-404
14. Isawa H., Yuda M., Orito Y., and Chinzei Y. A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J. Biol. Chem. 277 (2002) 27651-27658
15. Joseph K., Ghebrehiwet B., Peerschke E.I.B., Reid K.B.M., and Kaplan A.P. Identification of the zinc-dependent endothelial cell binding protein for high molecular weight kininogen and factor XII: identity with the receptor that binds to the globular "heads" of C1q (gC1q-R). Proc. Natl. Acad. Sci. USA 93 (1996) 8552-8557
16. Joseph K., Shibayama Y., Ghebrehiwet B., and Kaplan A.P. Factor XII-dependent contact activation on endothelial cells and binding proteins gC1qR and cytokeratin 1. Thromb. Haemostasis 85 (2001) 119-124
17. Joseph K., Tholanikunnel B.G., and Kaplan A.P. Heat shock protein 90 catalyzes activation of the prekallikrein-kininogen complex in the absence of factor XII. Proc. Natl. Acad. Sci. USA 99 (2002) 896-900
18. Kleinschnitz C., Stoll G., Bendszus M., Schuh K., Pauer H.U., Burfeind P., Renne C., Gailani D., Nieswandt B., and Renne T. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J. Exp. Med. 203 (2006) 513-518
19. Kunapuli S.P., DeLa Cadena R.A., and Colman R.W. Deletion mutagenesis of high molecular weight kininogen light chain. Identification of two anionic surface binding subdomains. J. Biol. Chem. 268 (1993) 2486-2492
20. Lanfrancotti A., Lombardo F., Santolamazza F., Veneri M., Castrignano T., Coluzzi M., and Arca B. Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. FEBS Lett. 517 (2002) 67-71
21. Law J.H., Ribeiro J.M.C., and Wells M.A. Biochemical insights derived from insect diversity. Annu. Rev. Biochem. 61 (1992) 87-111
22. Lin Y., Pixley R.A., and Colman R.W. Kinetic analysis of the role of zinc in the interaction of domain 5 of high-molecular weight kininogen (HK) with heparin. Biochemistry 39 (2000) 5104-5110
23. Mahdi F., Madar Z.S., Figueroa C.D., and Schmaier A.H. Factor XII interacts with the multiprotein assembly of urokinase plasminogen activator receptor, gC1qR, and cytokeratin 1 on endothelial cell membranes. Blood 99 (2002) 3585-3596
24. Motta G., Røjkjær R., Hasan A.A.K., Cines D.B., and Schmaier A.H. High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 91 (1998) 516-528
25. Reddigari S.R., Shibayama Y., Brunnée T., and Kaplan A.P. Human Hageman factor (factor XII) and high molecular weight kininogen compete for the same binding site on human umbilical vein endothelial cells. J. Biol. Chem. 268 (1993) 11982-11987
26. Renne T., Pozgajova M., Gruner S., Schuh K., Pauer H.U., Burfeind P., Gailani D., and Nieswandt B. Defective thrombus formation in mice lacking coagulation factor XII. J. Exp. Med. 202 (2005) 271-281
27. Ribeiro J.M.C. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect. Agents Dis. 4 (1995) 143-152
28. Røjkjær R., and Schousboe I. The surface-dependent autoactivation mechanism of factor XII. Eur. J. Biochem. 243 (1997) 160-166
29. 2 +-binding sites in factor XII and its activation derivatives. Eur. J. Biochem. 247 (1997) 491-496
30. Røjkjær R., Hasan A.A.K., Motta G., Schousboe I., and Schmaier A.H. Factor XII does not initiate prekallikrein activation on endothelial cells. Thromb. Haemost. 80 (1998) 74-81
31. Saito H. Contact factors in health and disease. Semin. Thromb. Hemost. 13 (1987) 36-49
32. Samuel M., Pixley R.A., Villanueva M.A., Colman R.W., and Villanueva G.B. Human factor XII (Hageman factor) autoactivation by dextran sulfate. Circular dichroism, fluorescence, and ultraviolet difference spectroscopic studies. J. Biol. Chem. 267 (1992) 19691-19697
33. Schmaier A.H., Røjkjær R., and Shariat-Madar Z. Activation of the plasma kallikrein/kinin system on cells: a revised hypothesis. Thromb. Haemost. 82 (1999) 226-233
34. Schousboe I. The inositol-phospholipid-accelerated activation of prekallikrein by activated factor XII at physiological ionic strength requires zinc ions and high-Mr kininogen. Eur. J. Biochem. 193 (1990) 495-499
35. Schousboe I., and Halkier T. Zinc ions promote the binding of factor XII/factor XIIA to acidic phospholipids but have no effect on the binding of high-Mr kininogen. Eur. J. Biochem. 197 (1991) 309-314
36. Scott C.F., Silver L.D., Schapira M., and Colman R.W. Cleavage of human high molecular weight kininogen markedly enhances its coagulant activity. Evidence that this molecule exists as a procofactor. J. Clin. Invest. 73 (1984) 954-962
37. Shariat-Madar Z., Mahdi F., and Schmaier A.H. Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J. Biol. Chem. 277 (2002) 17962-17969
38. Shimada T., Kato H., and Iwanaga S. Accelerating effect of zinc ions on the surface-mediated activation of factor XII and prekallikrein. J. Biochem. (Tokyo) 102 (1987) 913-921
39. Valenzuela J.G., Francischetti I.M.B., Pham V.M., Garfield M.K., and Ribeiro J.M.C. Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem. Mol. Biol. 33 (2003) 717-732
40. Yuda M., Higuchi K., Sun J., Kureishi Y., Ito M., and Chinzei Y. Expression reconstitution and characterization of prolixin-S as a vasodilator-a salivary gland nitric-oxide-binding hemoprotein of Rhodnius prolixus. Eur. J. Biochem. 249 (1997) 337-342