Structure and mechanism in salivary proteins from blood-feeding arthropods

Toxicon

Volumn 56, Issue 7, 2010, Pages 1120-1129

  Andersen, John F ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 9; BLOOD CLOTTING FACTOR 9A; BRADYKININ; COMPLEMENT COMPONENT C5; KININOGEN; LIPOCALIN; NITRIC OXIDE; NITROPHORIN; ODORANT BINDING PROTEIN; PROTEIN OMC1; PROTEOME; SALIVA PROTEIN; TRIABIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTHROPOD; BINDING AFFINITY; BINDING SITE; CIMEX; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENDOTHELIUM CELL; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; LIGAND BINDING; MACROPHAGE; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; TAXONOMY; THROMBOCYTE AGGREGATION; TICK;

ANIMALS; ARTHROPODS; FEEDING BEHAVIOR; HEMEPROTEINS; INSECT BITES AND STINGS; INSECT PROTEINS; LIPOCALINS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; SALIVA; SALIVARY PROTEINS AND PEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

ARTHROPODA;

EID: 77957914111     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.11.002     Document Type: Review

References (52)

1. Andersen J.F., Ding X.D., Balfour C., Shokhireva T.K., Champagne D.E., Walker F.A., Montfort W.R. Kinetics and equilibria in ligand binding by nitrophorins 1-4: evidence for stabilization of a nitric oxide-ferriheme complex through a ligand-induced conformational trap. Biochemistry 2000, 39:10118-10131.
2. Andersen J.F., Francischetti I.M., Valenzuela J.G., Schuck P., Ribeiro J.M. Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect. J Biol Chem 2003, 278:4611-4617.
3. Andersen J.F., Gudderra N.P., Francischetti I.M., Ribeiro J.M. The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch Insect Biochem Physiol 2005, 58:97-105.
4. Andersen J.F., Gudderra N.P., Francischetti I.M., Valenzuela J.G., Ribeiro J.M. Recognition of anionic phospholipid membranes by an antihemostatic protein from a blood-feeding insect. Biochemistry 2004, 43:6987-6994.
5. Andersen J.F., Montfort W.R. The crystal structure of nitrophorin 2. A trifunctional antihemostatic protein from the saliva of Rhodnius prolixus. J Biol Chem 2000, 275:30496-30503.
6. Andersen J.F., Ribeiro J.M. A secreted salivary inositol polyphosphate 5-phosphatase from a blood-feeding insect: allosteric activation by soluble phosphoinositides and phosphatidylserine. Biochemistry 2006, 45:5450-5457.
7. Andersen J.F., Weichsel A., Balfour C.A., Champagne D.E., Montfort W.R. The crystal structure of nitrophorin 4 at 1.5 A resolution: transport of nitric oxide by a lipocalin-based heme protein. Structure 1998, 6:1315-1327.
8. Assumpcao T.C., Francischetti I.M., Andersen J.F., Schwarz A., Santana J.M., Ribeiro J.M. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochem Mol Biol 2008, 38:213-232.
9. Berry R.E., Shokhirev M.N., Ho A.Y., Yang F., Shokhireva T.K., Zhang H., Weichsel A., Montfort W.R., Walker F.A. Effect of mutation of carboxyl side-chain amino acids near the heme on the midpoint potentials and ligand binding constants of nitrophorin 2 and its NO, histamine, and imidazole complexes. J Am Chem Soc 2009, 131:2313-2327.
10. Calvo E., deBianchi A.G., James A.A., Marinotti O. The major acid soluble proteins of adult female Anopheles darlingi salivary glands include a member of the D7-related family of proteins. Insect Biochem Mol Biol 2002, 32:1419-1427.
11. Calvo E., Mans B.J., Andersen J.F., Ribeiro J.M. Function and evolution of a mosquito salivary protein family. J Biol Chem 2006, 281:1935-1942.
12. Calvo E., Mans B.J., Ribeiro J.M., Andersen J.F. Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc Natl Acad Sci U S A 2009, 106:3728-3733.
13. Calvo E., Tokumasu F., Marinotti O., Villeval J.L., Ribeiro J.M., Francischetti I.M. 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.
14. Corral-Rodriguez M.A., Macedo-Ribeiro S., Barbosa Pereira P.J., Fuentes-Prior P. Tick-derived Kunitz-type inhibitors as antihemostatic factors. Insect Biochem Mol Biol 2009, 39:579-595.
15. Ding X.D., Weichsel A., Andersen J.F., Shokhireva T.K., Balfour C., Pierik A.J., Averill B.A., Montfort W.R., Walker F.A. Nitric oxide binding to the ferri- and ferroheme states of nitrophorin 1, a reversible NO-binding heme protein from the saliva of the blood-sucking insect, Rhodnius prolixus. J. Am. Chem. Soc. 1999, 121:128-138.
16. Francischetti I.M., Ribeiro J.M., 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.
17. Francischetti I.M., Sa-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M. The role of saliva in tick feeding. Front Biosci 2009, 14:2051-2088.
18. Fredslund F., Laursen N.S., Roversi P., Jenner L., Oliveira C.L., Pedersen J.S., Nunn M.A., Lea S.M., Discipio R., Sottrup-Jensen L., Andersen G.R. Structure of and influence of a tick complement inhibitor on human complement component 5. Nat Immunol 2008, 9:753-760.
19. Fry B.G., Roelants K., Champagne D.E., Scheib H., Tyndall J.D., King G.F., Nevalainen R.J., Norman J.A., Lewis R.J., Norton R.S., Renjifo C., de la Vega R.C. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 2009, 10:483-511.
20. Fuentes-Prior P., Noeske-Jungblut C., Donner P., Schleuning W.D., Huber R., Bode W. Structure of the thrombin complex with triabin, a lipocalin-like exosite-binding inhibitor derived from a triatomine bug. Proc Natl Acad Sci U S A 1997, 94:11845-11850.
21. Gudderra N.P., Ribeiro J.M., Andersen J.F. Structural determinants of factor IX(a) binding in nitrophorin 2, a lipocalin inhibitor of the intrinsic coagulation pathway. J Biol Chem 2005, 280:25022-25028.
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. Isawa H., Yuda M., Yoneda K., Chinzei Y. The insect salivary protein, prolixin-S, inhibits factor IXa generation and Xase complex formation in the blood coagulation pathway. J Biol Chem 2000, 275:6636-6641.
24. James A.A., Blackmer K., Marinotti O., Ghosn C.R., Racioppi J.V. Isolation and characterization of the gene expressing the major salivary gland protein of the female mosquito, Aedes aegypti. Mol Biochem Parasitol 1991, 44:245-253.
25. Knipp M., Yang F., Berry R.E., Zhang H., Shokhirev M.N., Walker F.A. Spectroscopic and functional characterization of nitrophorin 7 from the blood-feeding insect Rhodnius prolixus reveals an important role of its isoform-specific N-terminus for proper protein function. Biochemistry 2007, 46:13254-13268.
26. Knipp M., Zhang H., Berry R.E., Walker F.A. Overexpression in Escherichia coli and functional reconstitution of the liposome binding ferriheme protein nitrophorin 7 from the bloodsucking bug Rhodnius prolixus. Protein Expr Purif 2007, 54:183-191.
27. Koh C.Y., Kini R.M. Molecular diversity of anticoagulants from haematophagous animals. Thromb Haemost 2009, 102:437-453.
28. Malafronte R.S., Calvo E., James A.A., Marinotti O. The major salivary gland antigens of Culex quinquefasciatus are D7-related proteins. Insect Biochem Mol Biol 2003, 33:63-71.
29. Mans B.J., Calvo E., Ribeiro J.M., Andersen J.F. The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J Biol Chem 2007, 282:36626-36633.
30. Mans B.J., Ribeiro J.M. Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem Mol Biol 2008, 38:841-852.
31. Mans B.J., Ribeiro J.M. A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem Mol Biol 2008, 38:862-870.
32. Mans B.J., Ribeiro J.M., Andersen J.F. Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J Biol Chem 2008, 283:18721-18733.
33. Noeske-Jungblut C., Haendler B., Donner P., Alagon A., Possani L., Schleuning W.D. Triabin, a highly potent exosite inhibitor of thrombin. J Biol Chem 1995, 270:28629-28634.
34. Noeske-Jungblut C., Kratzschmar J., Haendler B., Alagon A., Possani L., Verhallen P., Donner P., Schleuning W.D. An inhibitor of collagen-induced platelet aggregation from the saliva of Triatoma pallidipennis. J Biol Chem 1994, 269:5050-5053.
35. Nunn M.A., Sharma A., Paesen G.C., Adamson S., Lissina O., Willis A.C., Nuttall P.A. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J Immunol 2005, 174:2084-2091.
36. Oldham N.J., Lissina O., Nunn M.A., Paesen G.C. Non-denaturing electrospray ionisation-mass spectrometry reveals ligand selectivity in histamine-binding protein RaHBP2. Org Biomol Chem 2003, 1:3645-3646.
37. Paesen G.C., Adams P.L., Harlos K., Nuttall P.A., Stuart D.I. Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol Cell 1999, 3:661-671.
38. Paesen G.C., Adams P.L., Nuttall P.A., Stuart D.L. Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochim Biophys Acta 2000, 1482:92-101.
39. Ribeiro J.M., Andersen J., Silva-Neto M.A., Pham V.M., Garfield M.K., Valenzuela J.G. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem Mol Biol 2004, 34:61-79.
40. Ribeiro J.M., Hazzard J.M., Nussenzveig R.H., Champagne D.E., Walker F.A. Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect. Science 1993, 260:539-541.
41. Ribeiro J.M., Schneider M., Guimaraes J.A. Purification and characterization of prolixin S (nitrophorin 2), the salivary anticoagulant of the blood-sucking bug Rhodnius prolixus. Biochem J 1995, 308(Pt 1):243-249.
42. Ribeiro J.M., Walker F.A. High affinity histamine-binding and antihistaminic activity of the salivary nitric oxide-carrying heme protein (nitrophorin) of Rhodnius prolixus. J Exp Med 1994, 180:2251-2257.
43. Roberts S.A., Weichsel A., Qiu Y., Shelnutt J.A., Walker F.A., Montfort W.R. Ligand-induced heme ruffling and bent no geometry in ultra-high-resolution structures of nitrophorin 4. Biochemistry 2001, 40:11327-11337.
44. Roversi P., Lissina O., Johnson S., Ahmat N., Paesen G.C., Ploss K., Boland W., Nunn M.A., Lea S.M. The structure of OMCI, a novel lipocalin inhibitor of the complement system. J Mol Biol 2007, 369:784-793.
45. Sangamnatdej S., Paesen G.C., Slovak M., Nuttall P.A. A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Mol Biol 2002, 11:79-86.
46. Valenzuela J.G., Charlab R., Gonzalez E.C., de Miranda-Santos I.K., Marinotti O., Francischetti I.M., Ribeiro J.M. The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 2002, 11:149-155.
47. Valenzuela J.G., Walker F.A., Ribeiro J.M. A salivary nitrophorin (nitric-oxide-carrying hemoprotein) in the bedbug Cimex lectularius. J Exp Biol 1995, 198:1519-1526.
48. Weichsel A., Andersen J.F., Champagne D.E., Walker F.A., Montfort W.R. Crystal structures of a nitric oxide transport protein from a blood-sucking insect. Nat Struct Biol 1998, 5:304-309.
49. Weichsel A., Andersen J.F., Roberts S.A., Montfort W.R. Nitric oxide binding to nitrophorin 4 induces complete distal pocket burial. Nat Struct Biol 2000, 7:551-554.
50. Weichsel A., Maes E.M., Andersen J.F., Valenzuela J.G., Shokhireva T., Walker F.A., Montfort W.R. Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Proc Natl Acad Sci U S A 2005, 102:594-599.
51. Yuda M., Higuchi K., Sun J., Kureishi Y., Ito M., 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 1997, 249:337-342.
52. Zhang Y., Ribeiro J.M., Guimaraes J.A., Walsh P.N. Nitrophorin-2: a novel mixed-type reversible specific inhibitor of the intrinsic factor-X activating complex. Biochemistry 1998, 37:10681-10690.