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 Biology

Volumn 8, Issue 11, 2010, Pages

  Alvarenga, Patricia H ^a,b   Francischetti, Ivo M B ^a   Calvo, Eric ^a   Sá Nunes, Anderson ^a,c   Ribeiro, José M C ^a   Andersen, John F ^a  

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

^b FEDERAL RURAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; BIOGENIC AMINE; PEPTIDOLEUKOTRIENE; THROMBOXANE A2; DRUG DERIVATIVE; INSECT PROTEIN; LEUKOTRIENE; LEUKOTRIENE C4;

AMINO TERMINAL SEQUENCE; ANOPHELES STEPHENSI; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; ILEUM CONTRACTION; LIGAND BINDING; MALARIA; NONHUMAN; PARASITE VECTOR; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; SALIVA ANALYSIS; SMOOTH MUSCLE CONTRACTION; STRUCTURE ANALYSIS; THROMBOCYTE AGGREGATION; ANIMAL; ANOPHELES; AORTA; CALORIMETRY; CHEMISTRY; DISEASE CARRIER; DISEASE TRANSMISSION; DRUG EFFECT; GUINEA PIG; HUMAN; ILEUM; METABOLISM; MUSCLE CONTRACTION; PROTEIN SECONDARY STRUCTURE; RAT; SALIVA;

AEDES AEGYPTI; ANOPHELES STEPHENSI; CAVIA; RATTUS;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; ANIMALS; ANOPHELES; AORTA; CALORIMETRY; GUINEA PIGS; HUMANS; ILEUM; INSECT PROTEINS; INSECT VECTORS; LEUKOTRIENE C4; LEUKOTRIENES; MALARIA; MUSCLE CONTRACTION; PLATELET AGGREGATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RATS; SALIVA; THROMBOXANE A2;

EID: 78649975316     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000547     Document Type: Article

References (59)

1. Ribeiro JM (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 4: 143-152.
2. Ribeiro JM, Francischetti IM (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48: 73-88.
3. Champagne DE (2005) Antihemostatic molecules from saliva of blood-feeding arthropods. Pathophysiol Haemost Thromb 34: 221-227.
4. Valenzuela JG (2002) High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochem Mol Biol 32: 1199-1209.
5. Titus RG, Ribeiro JM (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239: 1306-1308.
6. Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, et al. (2001) Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med 194: 331-342.
7. de Moura TR, Oliveira F, Novais FO, Miranda JC, Clarencio J, et al. (2007) Enhanced Leishmania braziliensis infection following pre-exposure to sandfly saliva. PLoS Negl Trop Dis 1: e84. doi:10.1371/journal.pntd.0000084.
8. Donovan MJ, Messmore AS, Scrafford DA, Sacks DL, Kamhawi S, et al. (2007) Uninfected mosquito bites confer protection against infection with malaria parasites. Infect Immun 75: 2523-2530.
9. Edwards JF, Higgs S, Beaty BJ (1998) Mosquito feeding-induced enhancement of Cache Valley Virus (Bunyaviridae) infection in mice. J Med Entomol 35: 261-265.
10. Limesand KH, Higgs S, Pearson LD, Beaty BJ (2000) Potentiation of vesicular stomatitis New Jersey virus infection in mice by mosquito saliva. Parasite Immunol 22: 461-467.
11. Sutherland GB, Ewen AB (1974) Fecundity decrease in mosquitoes ingesting blood from specifically sensitized mammals. J Insect Physiol 20: 655-660.
12. Francischetti IM (2009) Platelet aggregation inhibitors from hematophagous animals. Toxicon, in press.
13. Andersen JF (2009) Structure and mechanism in salivary proteins from blood-feeding arthropods. Toxicon, in press.
14. Calvo E, Mans BJ, Andersen JF, Ribeiro JM (2006) Function and evolution of a mosquito salivary protein family. J Biol Chem 281: 1935-1942.
15. Calvo E, Mans BJ, Ribeiro JM, Andersen JF (2009) Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc Natl Acad Sci U S A 106: 3728-3733.
16. Mans BJ, Calvo E, Ribeiro JM, Andersen JF (2007) The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J Biol Chem 282: 36626-36633.
17. Mans BJ, Ribeiro JM (2008) A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem Mol Biol 38: 862-870.
18. Mans BJ, Ribeiro JM, Andersen JF (2008) Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J Biol Chem 283: 18721-18733.
19. Ribeiro JM, Walker FA (1994) High affinity histamine-binding and antihista-minic activity of the salivary nitric oxide-carrying heme protein (nitrophorin) of Rhodnius prolixus. J Exp Med 180: 2251-2257.
20. Andersen JF, Gudderra NP, Francischetti IM, Ribeiro JM (2005) The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch Insect Biochem Physiol 58: 97-105.
21. Ribeiro JM, Arca B (2009) From Sialomes to the Sialoverse: an insight into salivary potion of blood-feeding insects. Advances in Insect Physiology. San Diego: Elsevier Academic Press. pp 59-118.
22. Francischetti IM, Ribeiro JM, Champagne D, Andersen J (2000) 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 275: 12639-12650.
23. Isawa H, Yuda M, Orito Y, Chinzei Y (2002) 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: 27651-27658.
24. Boyce JA (2005) Eicosanoid mediators of mast cells: receptors, regulation of synthesis, and pathobiologic implications. Chem Immunol Allergy 87: 59-79.
25. Hanna CJ, Bach MK, Pare PD, Schellenberg RR (1981) Slow-reacting substances (leukotrienes) contract human airway and pulmonary vascular smooth muscle in vitro. Nature 290: 343-344.
26. Findlay SR, Lichtenstein LM, Siegel H, Triggle DJ (1981) Mechanisms of contraction induced by partially purified slow reacting substance from human polymorphonuclear leukocytes and leukotriene D in guinea pig ileal smooth muscle. J Immunol 126: 1728-1730.
27. Nakahata N (2008) Thromboxane A2: physiology/pathophysiology, cellular signal transduction and pharmacology. Pharmacol Ther 118: 18-35.
28. Andrews RK, Berndt MC (2004) Platelet physiology and thrombosis. Thromb Res 114: 447-453.
29. Canobbio I, Balduini C, Torti M (2004) Signalling through the platelet glycoprotein Ib-V-IX complex. Cell Signal 16: 1329-1344.
30. Clemetson KJ, Clemetson JM (2001) Platelet collagen receptors. Thromb Haemost 86: 189-197.
31. Nieswandt B, Watson SP (2003) Platelet-collagen interaction: is GPVI the central receptor? Blood 102: 449-461.
32. Surin WR, Barthwal MK, Dikshit M (2008) Platelet collagen receptors, signaling and antagonism: emerging approaches for the prevention of intravascular thrombosis. Thromb Res 122: 786-803.
33. Kahner BN, Shankar H, Murugappan S, Prasad GL, Kunapuli SP (2006) Nucleotide receptor signaling in platelets. J Thromb Haemost 4: 2317-2326.
34. Francischetti IM, Andersen JF, Ribeiro JM (2002) Biochemical and functional characterization of recombinant Rhodnius prolixus platelet aggregation inhibitor 1 as a novel lipocalin with high affinity for adenosine diphosphate and other adenine nucleotides. Biochemistry 41: 3810-3818.
35. Ohkubo S, Nakahata N, Ohizumi Y (1996) Thromboxane A2-mediated shape change: independent of Gq-phospholipase C-Ca2+ pathway in rabbit platelets. Br J Pharmacol 117: 1095-1104.
36. Soter NA, Lewis RA, Corey EJ, Austen KF (1983) Local effects of synthetic leukotrienes (LTC4, LTD4, LTE4, and LTB4) in human skin. J Invest Dermatol 80: 115-119.
37. Boyce JA (2007) Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol Rev 217: 168-185.
38. Murphy RC, Gijon MA (2007) Biosynthesis and metabolism of leukotrienes. Biochem J 405: 379-395.
39. Camp RD, Coutts AA, Greaves MW, Kay AB, Walport MJ (1983) Responses of human skin to intradermal injection of leukotrienes C4, D4 and B4. Br J Pharmacol 80: 497-502.
40. Bisgaard H (1987) Vascular effects of leukotriene D4 in human skin. J Invest Dermatol 88: 109-114.
41. Bisgaard H, Kristensen J, Sondergaard J (1982) The effect of leukotriene C4 and D4 on cutaneous blood flow in humans. Prostaglandins 23: 797-801.
42. Bisgaard H, Lerche A, Kristensen JK (1985) Leukotriene- and histamine-induced increases in vascular permeability and interstitial transport in the skin. J Invest Dermatol 84: 427-429.
43. Andoh T, Nishikawa Y, Yamaguchi-Miyamoto T, Nojima H, Narumiya S, et al. (2007) Thromboxane A2 induces itch-associated responses through TP receptors in the skin in mice. J Invest Dermatol 127: 2042-2047.
44. Watson SP (2009) Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr Pharm Des 15: 1358-1372.
45. Jarvis GE, Atkinson BT, Snell DC, Watson SP (2002) Distinct roles of GPVI and integrin alpha(2)beta(1) in platelet shape change and aggregation induced by different collagens. Br J Pharmacol 137: 107-117.
46. Moers A, Wettschureck N, Gruner S, Nieswandt B, Offermanns S (2004) Unresponsiveness of platelets lacking both Galpha(q) and Galpha(13). Implications for collagen-induced platelet activation. J Biol Chem 279: 45354-45359.
47. Mumford AD, Dawood BB, Daly ME, Murden SL, Williams MD, et al. A novel thromboxane A2 receptor D304N variant that abrogates ligand binding in a patient with a bleeding diathesis. Blood 115: 363-369.
48. Choumet V, Carmi-Leroy A, Laurent C, Lenormand P, Rousselle JC, et al. (2007) The salivary glands and saliva of Anopheles gambiae as an essential step in the Plasmodium life cycle: a global proteomic study. Proteomics 7: 3384-3394.
49. Francischetti IM, Saliou B, Leduc M, Carlini CR, Hatmi M, et al. (1997) Convulxin, a potent platelet-aggregating protein from Crotalus durissus terrificus venom, specifically binds to platelets. Toxicon 35: 1217-1228.
50. Andersen JF, Francischetti IM, Valenzuela JG, Schuck P, Ribeiro JM (2003) Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect. J Biol Chem 278: 4611-4617.
51. Webster ME, Prado ES (1970) Glandular kallikreins from horse and human urine and from hog pancreas. In: Perlman GE, Lorand L, eds. Methods in enzymology. San Diego: Academic Press. pp 681-699.
52. Lagrue AH, Francischetti IM, Guimaraes JA, Jandrot-Perrus M (1999) Phosphatidylinositol 39-kinase and tyrosine-phosphatase activation positively modulate Convulxin-induced platelet activation. Comparison with collagen. FEBS Lett 448: 95-100.
53. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M (2006) HKL-3000: the integration of data reduction and structure solution-from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62: 859-866.
54. Schneider TR, Sheldrick GM (2002) Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58: 1772-1779.
55. Sheldrick GM (2002) Macromolecular phasing with SHELXE. Z Kristallogr 217: 644-650.
56. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.
57. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
58. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
59. Kleywegt GJ, Jones TA (1995) Where freedom is given, liberties are taken. Structure 3: 535-540.