Novel family of insect salivary inhibitors blocks contact pathway activation by binding to polyphosphate, heparin, and dextran sulfate

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 12, 2013, Pages 2759-2770

  Alvarenga, Patricia H ^a,b   Xu, Xueqing ^a   Oliveira, Fabiano ^a   Chagas, Andrezza C ^a   Nascimento, Clarissa R ^b   Francischetti, Ivo M B ^a   Juliano, Maria A ^c   Juliano, Luiz ^c   Scharfstein, Julio ^b   Valenzuela, Jesus G ^a   Ribeiro, José M C ^a   Andersen, John F ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Blood coagulation factor inhibitors; Bradykinin; Factor XI; Factor XII; Inflammation; Kallikreins; Leishmania

Indexed keywords

ANTIINFLAMMATORY AGENT; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12A; DEXTRAN SULFATE; HEPARIN; HIGH MOLECULAR WEIGHT KININOGEN; PDSP15A PROTEIN; PDSP15B PROTEIN; POLYPHOSPHATE; PREKALLIKREIN; THROMBIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; DRUG MECHANISM; MOLECULAR INTERACTION; NONHUMAN; PHLEBOTOMOUS DUBOSCQI; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PSYCHODIDAE; SURFACE PROPERTY; X RAY;

BLOOD COAGULATION FACTOR INHIBITORS; BRADYKININ; FACTOR XI; FACTOR XII; INFLAMMATION; KALLIKREINS; LEISHMANIA;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; BLOOD COAGULATION TESTS; CAPILLARY PERMEABILITY; CRYSTALLOGRAPHY, X-RAY; DEXTRAN SULFATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR XIA; FACTOR XIIA; HEPARIN; HUMANS; INSECT PROTEINS; KININOGEN, HIGH-MOLECULAR-WEIGHT; MICE; MODELS, MOLECULAR; POLYPHOSPHATES; PREKALLIKREIN; PROTEIN CONFORMATION; PSYCHODIDAE; SALIVA; STRUCTURE-ACTIVITY RELATIONSHIP; THROMBIN; TIME FACTORS;

EID: 84888198078     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302482     Document Type: Article

References (53)

1. Renné T, Schmaier AH, Nickel KF, Blombäck M, Maas C. In vivo roles of factor XII. Blood. 2012;120:4296-4303
2. Emsley J, McEwan PA, Gailani D. Structure and function of factor XI. Blood. 2010;115:2569-2577
3. Lämmle B, Wuillemin WA, Huber I, Krauskopf M, Zürcher C, Pflugshaupt R, Furlan M. Thromboembolism and bleeding tendency in congenital factor XII deficiency-A study on 74 subjects from 14 Swiss families. Thromb Haemost. 1991;65:117-121
4. Cheng Q, Tucker EI, Pine MS, Sisler I, Matafonov A, Sun MF, White-Adams TC, Smith SA, Hanson SR, McCarty OJ, Renné T, Gruber A, Gailani D. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood. 2010;116:3981-3989
5. Renné T, Pozgajová M, Grüner S, Schuh K, Pauer HU, Burfeind P, Gailani D, Nieswandt B. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202:271-281
6. Renné T. The procoagulant and proinflammatory plasma contact system. Semin Immunopathol. 2012;34:31-41
7. Samuel M, Pixley RA, Villanueva MA, Colman RW, Villanueva GB. Human factor XII (Hageman factor) autoactivation by dextran sulfate. Circular dichroism, fluorescence, and ultraviolet difference spectroscopic studies. J Biol Chem. 1992;267:19691-19697
8. Brunnée T, Reddigari SR, Shibayama Y, Kaplan AP, Silverberg M. Mast cell derived heparin activates the contact system: A link to kinin generation in allergic reactions. Clin Exp Allergy. 1997;27:653-663
9. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood. 2011;118:6963-6970
10. Morrissey JH, Choi SH, Smith SA. Polyphosphate: An ancient molecule that links platelets, coagulation, and inflammation. Blood. 2012;119:5972-5979
11. Müller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, Schmidbauer S, Gahl WA, Morrissey JH, Renné T. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009;139:1143-1156
12. Oschatz C, Maas C, Lecher B, Jansen T, Björkqvist J, Tradler T, Sedlmeier R, Burfeind P, Cichon S, Hammerschmidt S, Müller-Esterl W, Wuillemin WA, Nilsson G, Renné T. Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity. 2011;34:258-268
13. Moreno-Sanchez D, Hernandez-Ruiz L, Ruiz FA, Docampo R. Polyphosphate is a novel pro-inflammatory regulator of mast cells and is located in acidocalcisomes. J Biol Chem. 2012;287:28435-28444
14. Ruiz FA, Lea CR, Oldfield E, Docampo R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem. 2004;279:44250-44257
15. Smith SA, Morrissey JH. Heparin is procoagulant in the absence of antithrombin. Thromb Haemost. 2008;100:160-162
16. Smith SA, Choi SH, Davis-Harrison R, Huyck J, Boettcher J, Rienstra CM, Reinstra CM, Morrissey JH. Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood. 2010;116:4353-4359
17. Smith SA, Morrissey JH. Polyphosphate as a general procoagulant agent. J Thromb Haemost. 2008;6:1750-1756
18. Smith SA, Morrissey JH. Polyphosphate enhances fibrin clot structure. Blood. 2008;112:2810-2816
19. Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA. 2006;103:903-908
20. Isawa H, Orito Y, Iwanaga S, Jingushi N, Morita A, Chinzei Y, Yuda M. Identification and characterization of a new kallikrein-kinin system inhibitor from the salivary glands of the malaria vector mosquito Anopheles stephensi. Insect Biochem Mol Biol. 2007;37:466-477
21. Isawa H, Orito Y, Jingushi N, Iwanaga S, Morita A, Chinzei Y, Yuda M. Identification and characterization of plasma kallikrein-kinin system inhibitors from salivary glands of the blood-sucking insect Triatoma infestans. FEBS J. 2007;274:4271-4286
22. Isawa H, Yuda M, Orito Y, 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. 2002;277:27651-27658
23. Kato N, Iwanaga S, Okayama T, Isawa H, Yuda M, Chinzei Y. Identification and characterization of the plasma kallikrein-kinin system inhibitor, haemaphysalin, from hard tick, Haemaphysalis longicornis. Thromb Haemost. 2005;93:359-367
24. Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG, Pham VM, Sangare CS, Samake S, Sissoko I, Garfield M, Sigutova L, Volf P, Doumbia S, Valenzuela JG. High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya). BMC Genomics. 2006;7:226
25. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JM. Toward a defined anti-Leishmania vaccine targeting vector antigens: Characterization of a protective salivary protein. J Exp Med. 2001;194:331-342
26. Scott CF, Colman RW. Fibrinogen blocks the autoactivation and thrombinmediated activation of factor XI on dextran sulfate. Proc Natl Acad Sci USA. 1992;89:11189-11193
27. Wu W, Sinha D, Shikov S, Yip CK, Walz T, Billings PC, Lear JD, Walsh PN. Factor XI homodimer structure is essential for normal proteolytic activation by factor XIIa, thrombin, and factor XIa. J Biol Chem. 2008;283:18655-18664
28. Korkmaz B, Attucci S, Juliano MA, Kalupov T, Jourdan ML, Juliano L, Gauthier F. Measuring elastase, proteinase 3 and cathepsin G activities at the surface of human neutrophils with fluorescence resonance energy transfer substrates. Nat Protoc. 2008;3:991-1000
29. Fukumizu A, Tsuda Y, Wanaka K, Tada M, Okamoto S, Hijikata-Okunomiya A, Okada Y. Amino acids and peptides. LIII. Synthesis and biological activities of some pseudo-peptide analogs of PKSI-527, a plasma kallikrein selective inhibitor: The importance of the peptide backbone. Chem Pharm Bull (Tokyo). 1999;47:1141-1144
30. Calvo E, Mans BJ, Ribeiro JM, Andersen JF. Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc Natl Acad Sci USA. 2009;106:3728-3733
31. Mans BJ, Calvo E, Ribeiro JM, Andersen JF. The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J Biol Chem. 2007;282:36626-36633
32. Dong J, Peters-Libeu CA, Weisgraber KH, Segelke BW, Rupp B, Capila I, Hernáiz MJ, LeBrun LA, Linhardt RJ. Interaction of the N-Terminal domain of apolipoprotein E4 with heparin. Biochemistry. 2001;40:2826-2834
33. Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, Carrell RW. The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci USA. 1997;94:14683-14688
34. Alvarenga PH, Francischetti IM, Calvo E, Sá-Nunes A, Ribeiro JM, Andersen JF. The function and three-dimensional structure of a thromboxane A2/cysteinyl leukotriene-binding protein from the saliva of a mosquito vector of the malaria parasite. PLoS Biol. 2010;8:e1000547
35. Francischetti IM, Ribeiro JM, Champagne D, Andersen J. Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of the blood-sucking bug, Rhodnius prolixus. J Biol Chem. 2000;275:12639-12650
36. Calvo E, Tokumasu F, Marinotti O, Villeval JL, Ribeiro JM, Francischetti IM. Aegyptin, a novel mosquito salivary gland protein, specifically binds to collagen and prevents its interaction with platelet glycoprotein VI, integrin alpha2beta1, and von Willebrand factor. J Biol Chem. 2007;282:26928-26938
37. Xu X, Chang BW, Mans BJ, Ribeiro JM, Andersen JF. Structure and ligand-binding properties of the biogenic amine-binding protein from the saliva of a blood-feeding insect vector of Trypanosoma cruzi. Acta Crystallogr D Biol Crystallogr. 2013;69(Pt 1):105-113
38. Xu X, Oliveira F, Chang BW, Collin N, Gomes R, Teixeira C, Reynoso D, My Pham V, Elnaiem DE, Kamhawi S, Ribeiro JM, Valenzuela JG, Andersen JF. Structure and function of a yellow protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection. J Biol Chem. 2011;286: 32383-32393
39. Choumet V, Attout T, Chartier L, Khun H, Sautereau J, Robbe-Vincent A, Brey P, Huerre M, Bain O. Visualizing non infectious and infectious Anopheles gambiae blood feedings in naive and saliva-immunized mice. PLoS One. 2012;7:e50464
40. Ribeiro JM, Arca B. From Sialomes to the Sialoverse: An Insight into Salivary Potion of Blood-Feeding Insects. Adv Insect Physiol. 2009;37:59-118
41. Ribeiro JM, Modi GB, Tesh RB. Salivary apyrase activity of some old world phlebotomine sand flies. Insect Biochem Mol Biol. 1989;19: 409-412
42. Collin N, Assumpção TC, Mizurini DM, Gilmore DC, Dutra-Oliveira A, Kotsyfakis M, Sá-Nunes A, Teixeira C, Ribeiro JM, Monteiro RQ, Valenzuela JG, Francischetti IM. Lufaxin, a novel factor Xa inhibitor from the salivary gland of the sand fly Lutzomyia longipalpis blocks proteaseactivated receptor 2 activation and inhibits inflammation and thrombosis in vivo. Arterioscler Thromb Vasc Biol. 2012;32:2185-2198
43. Andersen JF, Gudderra NP, Francischetti IM, Valenzuela JG, Ribeiro JM. Recognition of anionic phospholipid membranes by an antihemostatic protein from a blood-feeding insect. Biochemistry. 2004;43: 6987-6994
44. Decrem Y, Rath G, Blasioli V, Cauchie P, Robert S, Beaufays J, Frère JM, Feron O, Dogné JM, Dessy C, Vanhamme L, Godfroid E. Ir-CPI, a coagulation contact phase inhibitor from the tick Ixodes ricinus, inhibits thrombus formation without impairing hemostasis. J Exp Med. 2009;206: 2381-2395
45. Hagedorn I, Schmidbauer S, Pleines I, Kleinschnitz C, Kronthaler U, Stoll G, Dickneite G, Nieswandt B. Factor XIIa inhibitor recombinant human albumin Infestin-4 abolishes occlusive arterial thrombus formation without affecting bleeding. Circulation. 2010;121:1510-1517
46. Jain S, Pitoc GA, Holl EK, Zhang Y, Borst L, Leong KW, Lee J, Sullenger BA. Nucleic acid scavengers inhibit thrombosis without increasing bleeding. Proc Natl Acad Sci USA. 2012;109:12938-12943
47. Smith SA, Choi SH, Collins JN, Travers RJ, Cooley BC, Morrissey JH. Inhibition of polyphosphate as a novel strategy for preventing thrombosis and inflammation. Blood. 2012;120:5103-5110
48. Lee J, Sohn JW, Zhang Y, Leong KW, Pisetsky D, Sullenger BA. Nucleic acid-binding polymers as anti-inflammatory agents. Proc Natl Acad Sci USA. 2011;108:14055-14060
49. Montilla M, Hernandez-Ruiz L, Garcia-Cozar FJ, Alvarez-Laderas I, Rodriguez-Martorell J, Ruiz A. Polyphosphate binds to human von Willebrand factor in vivo and modulates its interaction with Glycoprotein Ib. J Thromb Haemost. 2012;10:2315-2323
50. Belkaid Y, Valenzuela JG, Kamhawi S, Rowton E, Sacks DL, Ribeiro JM. Delayed-Type hypersensitivity to Phlebotomus papatasi sand fly bite: An adaptive response induced by the fly? Proc Natl Acad Sci USA. 2000;97:6704-6709
51. Lerner EA, Ribeiro JM, Nelson RJ, Lerner MR. Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. J Biol Chem. 1991;266:11234-11236
52. Soares MB, Titus RG, Shoemaker CB, David JR, Bozza M. The vasoactive peptide maxadilan from sand fly saliva inhibits TNF-Alpha and induces IL-6 by mouse macrophages through interaction with the pituitary adenylate cyclase-Activating polypeptide (PACAP) receptor. J Immunol. 1998;160:1811-1816
53. Titus RG, Ribeiro JM. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science. 1988;239:1306-1308