An insight into the sialome of blood-feeding Nematocera

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 11, 2010, Pages 767-784

  Ribeiro, José M C ^a   Mans, Ben J ^b,c   Arcà, Bruno ^d  

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

^b ONDERSTEPOORT VETERINARY INSTITUTE   (South Africa)

^c UNIVERSITY OF PRETORIA   (South Africa)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Biting midges; Black flies; Feeding; Hematophagy; Mosquitoes; Salivary glands; Sand flies; Vector

Indexed keywords

INSECT PROTEIN;

ANIMAL; EVOLUTION; FEEDING BEHAVIOR; FLY; GENETICS; METABOLISM; REVIEW; SALIVA; SPECIES DIFFERENCE;

ANIMALS; BIOLOGICAL EVOLUTION; DIPTERA; FEEDING BEHAVIOR; INSECT PROTEINS; SALIVA; SPECIES SPECIFICITY;

ANURA; BRACHYCERA; CERATOPOGONIDAE; CORETHRELLIDAE; CULICIDAE; CULICOMORPHA; DIPTERA; HEXAPODA; NEMATOCERA; PHLEBOTOMINAE; SIMULIIDAE; VERTEBRATA;

EID: 77957315351     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.08.002     Document Type: Review

References (174)

1. Abebe M., Cupp M.S., Champagne D., Cupp E.W. Simulidin: a black fly (Simulium vittatum) salivary gland protein with anti-thrombin activity. J. Insect Physiol. 1995, 41:1001-1006.
2. Abrahamson M., Alvarez-Fernandez M., Nathanson C.M. Cystatins. Biochem. Soc. Symp. 2003, 179-199.
3. Albert S., Bhattacharya D., Klaudiny J., Schmitzova J., Simuth J. The family of major royal jelly proteins and its evolution. J. Mol. Evol. 1999, 49:290-297.
4. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
5. Ameri M., Wang X., Wilkerson M.J., Kanost M.R., Broce A.B. An immunoglobulin binding protein (antigen 5) of the stable fly (Diptera: Muscidae) salivary gland stimulates bovine immune responses. J. Med. Entomol. 2008, 45:94-101.
6. Andersen J.F., Pham V.M., Meng Z., Champagne D.E., Ribeiro J.M. Insight into the sialome of the black fly, Simulium vittatum. J. Proteome Res. 2009.
7. Anderson J.M., Oliveira F., Kamhawi S., Mans B.J., Reynoso D., Seitz A.E., Lawyer P., Garfield M., Pham M., Valenzuela J.G. Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 2006, 7:52.
8. Arca B., Lombardo F., de Lara Capurro M., della Torre A., Dimopoulos G., James A.A., Coluzzi M. Trapping cDNAs encoding secreted proteins from the salivary glands of the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1516-1521.
9. Arca B., Lombardo F., Lanfrancotti A., Spanos L., Veneri M., Louis C., Coluzzi M. A cluster of four D7-related genes is expressed in the salivary glands of the African malaria vector Anopheles gambiae. Insect Mol. Biol. 2002, 11:47-55.
10. Arca B., Lombardo F., Valenzuela J.G., Francischetti I.M., Marinotti O., Coluzzi M., Ribeiro J.M. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J. Exp. Biol. 2005, 208:3971-3986.
11. Arca B., Lombardo F., Francischetti I.M., Pham V.M., Mestres-Simon M., Andersen J.F., Ribeiro J.M. An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem. Mol. Biol. 2007, 37:107-127.
12. Argentine J.A., James A.A. Characterization of a salivary gland-specific esterase in the vector mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 1995, 25:621-630.
13. Ascenzi P., Bocedi A., Bolognesi M., Spallarossa A., Coletta M., De Cristofaro R., Menegatti E. The bovine basic pancreatic trypsin inhibitor (Kunitz inhibitor): a milestone protein. Curr. Protein Pept. Sci. 2003, 4:231-251.
14. Bahia D., Gontijo N.F., Leon I.R., Perales J., Pereira M.H., Oliveira G., Correa-Oliveira R., Reis A.B. Antibodies from dogs with canine visceral leishmaniasis recognise two proteins from the saliva of Lutzomyia longipalpis. Parasitol. Res. 2007, 100:449-454.
15. Barral A., Honda E., Caldas A., Costa J., Vinhas V., Rowton E.D., Valenzuela J.G., Charlab R., Barral-Netto M., Ribeiro J.M. Human immune response to sand fly salivary gland antigens: a useful epidemiological marker?. Am. J. Trop. Med. Hyg. 2000, 62:740-745.
16. Baskova I.P., Nikonov G.I. Destabilase, the novel epsilon-(gamma-Glu)-Lys isopeptidase with thrombolytic activity. Blood Coagul. Fibrinolysis 1991, 2:167-172.
17. Beerntsen B.T., Champagne D.E., Coleman J.L., Campos Y.A., James A.A. Characterization of the Sialokinin I gene encoding the salivary vasodilator of the yellow fever mosquito, Aedes aegypti. Insect Mol. Biol. 1999, 8:459-467.
18. Bendtsen J.D., Jensen L.J., Blom N., Von Heijne G., Brunak S. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 2004, 17:349-356.
19. Boppana V.D., Thangamani S., Adler A.J., Wikel S.K. SAAG-4 is a novel mosquito salivary protein that programmes host CD4 T cells to express IL-4. Parasite Immunol. 2009, 31:287-295.
20. Calvo E., Ribeiro J.M. A novel secreted endonuclease from Culex quinquefasciatus salivary glands. J. Exp. Biol. 2006, 209:2651-2659.
21. Calvo E., Andersen J., Francischetti I.M., de L.C.M., deBianchi A.G., James A.A., Ribeiro J.M., Marinotti O. The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol. Biol. 2004, 13:73-88.
22. 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.
23. Calvo E., Pham V.M., Lombardo F., Arca B., Ribeiro J.M. The sialotranscriptome of adult male Anopheles gambiae mosquitoes. Insect Biochem. Mol. Biol. 2006, 36:570-575.
24. Calvo E., Dao A., Pham V.M., Ribeiro J.M. An insight into the sialome of Anopheles funestus reveals an emerging pattern in anopheline salivary protein families. Insect Biochem. Mol. Biol. 2007, 37:164-175.
25. 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.
26. Calvo E., Pham V.M., Ribeiro J.M. An insight into the sialotranscriptome of the non-blood feeding Toxorhynchites amboinensis mosquito. Insect Biochem. Mol. Biol. 2008, 38:499-507.
27. 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.
28. Calvo E., Pham V.M., Marinotti O., Andersen J.F., Ribeiro J.M. The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics 2009, 10:57.
29. Calvo E., Tokumasu F., Mizurini D.M., McPhie P., Narum D.L., Ribeiro J.M., Monteiro R.Q., Francischetti I.M. Aegyptin displays high-affinity for the von Willebrand factor binding site (RGQOGVMGF) in collagen and inhibits carotid thrombus formation in vivo. FEBS J. 2010, 277:413-427.
30. Calvo E., Sanchez-Vargas I., Favreau A.J., Barbian K.D., Pham V.M., Olson K.E., Ribeiro J.M. An insight into the sialotranscriptome of the West Nile mosquito vector, Culex tarsalis. BMC Genomics 2010, 11:51.
31. Calvo E., Sanchez-Vargas I., Kotsyfakis M., Favreau A.J., Barbian K.D., Pham V.M., Olson K.E., Ribeiro J.M. The salivary gland transcriptome of the eastern tree hole mosquito, Ochlerotatus triseriatus. J. Med. Entomol. 2010, 47:376-386.
32. Campbell C.L., Vandyke K.A., Letchworth G.J., Drolet B.S., Hanekamp T., Wilson W.C. Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol. Biol. 2005, 14:121-136.
33. Castaneda O., Harvey A.L. Discovery and characterization of cnidarian peptide toxins that affect neuronal potassium ion channels. Toxicon 2009.
34. Cazares-Raga F.E., Gonzalez-Lazaro M., Montero-Solis C., Gonzalez-Ceron L., Zamudio F., Martinez-Barnetche J., Torres-Monzon J.A., Ovilla-Munoz M., Aguilar-Fuentes J., Rodriguez M.H., et al. GP35 ANOAL, an abundant acidic glycoprotein of female Anopheles albimanus saliva. Insect Mol. Biol. 2007, 16:187-198.
35. Cerna P., Mikes L., Volf P. Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera: psychodidae). Insect Biochem. Mol. Biol. 2002, 32:1691-1697.
36. Champagne D., Ribeiro J.M.C. Sialokinins I and II: two salivary tachykinins from the Yellow Fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:138-142.
37. Champagne D.E., Smartt C.T., Ribeiro J.M., James A.A. The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5'-nucleotidase family. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:694-698.
38. Charlab R., Valenzuela J.G., Rowton E.D., Ribeiro J.M. Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:15155-15160.
39. Charlab R., Rowton E.D., Ribeiro J.M. The salivary adenosine deaminase from the sand fly Lutzomyia longipalpis. Exp. Parasitol. 2000, 95:45-53.
40. Charlab R., Valenzuela J.G., Andersen J., Ribeiro J.M. The invertebrate growth factor/CECR1 subfamily of adenosine deaminase proteins. Gene 2001, 267:13-22.
41. Cornelie S., Remoue F., Doucoure S., Ndiaye T., Sauvage F.X., Boulanger D., Simondon F. An insight into immunogenic salivary proteins of Anopheles gambiae in African children. Malar. J. 2007, 6:75.
42. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.F., Kohara Y., Ewbank J.J. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 2004, 5:488-494.
43. Cupp, M.S., Cupp, E.W., 2000. Antithrombin protein and DNA sequences from black fly. USA.
44. Cupp E.W., Cupp M.S., Ramberg F.B. Salivary apyrase in african and New-World vectors of Plasmodium species and its relationship to malaria transmission. Am. J. Trop. Med. Hyg. 1994, 50:235-240.
45. Cupp M.S., Cupp E.W., Ochoa A.J., Moulton J.K. Salivary apyrase in New World blackflies (Diptera: Simuliidae) and its relationship to onchocerciasis vector status. Med. Vet. Entomol. 1995, 9:325-330.
46. Cupp M.S., Ribeiro J.M., Champagne D.E., Cupp E.W. Analyses of cDNA and recombinant protein for a potent vasoactive protein in saliva of a blood-feeding black fly, Simulium vittatum. J. Exp. Biol. 1998, 201:1553-1561.
47. Didisheim P., Hattori K., Lewis J.H. Hematologic and coagulation studies in various animal species. J. Lab. Clin. Med. 1959, 53:866-875.
48. Docena G.H., Benitez P., Campos R.E., Macia A., Fernandez R., Fossati C.A. Detection of allergens in Aedes albifasciatus mosquito (Diptera: Culicidae) extracts by immunological methods. J. Investig. Allergol. Clin. Immunol. 1999, 9:165-171.
49. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
50. Faudry E., Lozzi S.P., Santana J.M., D'Souza-Ault M., Kieffer S., Felix C.R., Ricart C.A., Sousa M.V., Vernet T., Teixeira A.R. Triatoma infestans apyrases belong to the 5'-nucleotidase family. J. Biol. Chem. 2004, 279:19607-19613.
51. Ferrandon D., Imler J.L., Hoffmann J.A. Sensing infection in Drosophila: toll and beyond. Semin. Immunol. 2004, 16:43-53.
52. Ferrer-Sueta G., Radi R. Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem. Biol. 2009, 4:161-177.
53. Fradkov A., Berezhnoy S., Barsova E., Zavalova L., Lukyanov S., Baskova I., Sverdlov E.D. Enzyme from the medicinal leech (Hirudo medicinalis) that specifically splits endo-epsilon(-gamma-Glu)-Lys isopeptide bonds: cDNA cloning and protein primary structure. FEBS Lett. 1996, 390:145-148.
54. Francischetti I.M., Valenzuela J.G., Ribeiro J.M. Anophelin: kinetics and mechanism of thrombin inhibition. Biochemistry 1999, 38:16678-16685.
55. Francischetti I.M., Valenzuela J.G., Pham V.M., Garfield M.K., Ribeiro J.M. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J. Exp. Biol. 2002, 205:2429-2451.
56. Francischetti I.M., Mather T.N., Ribeiro J.M. Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochem. Biophys. Res. Commun. 2003, 305:869-875.
57. Francischetti I.M.B., Sá-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M.C. The role of saliva in tick feeding. Front. Biosci. 2009, 14:2051-2088.
58. Fry B.G., Roelants K., Champagne D.E., Scheib H., Tyndall J.D., King G.F., Nevalainen T.J., Norman J.A., Lewis R.J., Norton R.S., et al. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics Hum. Genet. 2009, 10:483-511.
59. Fujita T., Matsushita M., Endo Y. The lectin-complement pathway - its role in innate immunity and evolution. Immunol. Rev. 2004, 198:185-202.
60. Gasmi L., McLennan A.G., Edwards S.W. Neutrophil apoptosis is delayed by the diadenosine polyphosphates, Ap5A and Ap6A: synergism with granulocyte-macrophage colony-stimulating factor. Br. J. Haematol. 1996, 95:637-639.
61. Geyer P.K., Spana C., Corces V.G. On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J. 1986, 5:2657-2662.
62. Gibbs G.M., Roelants K., O'Bryan M.K. The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins - roles in reproduction, cancer, and immune defense. Endocr. Rev. 2008, 29:865-897.
63. Grimaldi D., Engel M. Evolution of the Insects 2005, Cambridge University Press, New York.
64. Han Q., Fang J., Ding H., Johnson J.K., Christensen B.M., Li J. Identification of Drosophila melanogaster yellow-f and yellow-f2 proteins as dopachrome-conversion enzymes. Biochem. J. 2002, 368:333-340.
65. Harvey A.L. Recent studies on dendrotoxins and potassium ion channels. Gen. Pharmacol. 1997, 28:7-12.
66. Hekmat-Scafe D.S., Dorit R.L., Carlson J.R. Molecular evolution of odorant-binding protein genes OS-E and OS-F in Drosophila. Genetics 2000, 155:117-127.
67. Hostomska J., Volfova V., Mu J., Garfield M., Rohousova I., Volf P., Valenzuela J.G., Jochim R.C. Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics 2009, 10:282.
68. 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, 13:13.
69. 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.
70. James A.A., Blackmer K., Racioppi J.V. A salivary gland-specific, maltase-like gene of the vector mosquito, Aedes aegypti. Gene 1989, 75:73-83.
71. 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, 44:245-254.
72. Jariyapan N., Choochote W., Jitpakdi A., Harnnoi T., Siriyasatein P., Wilkinson M.C., Bates P.A. A glycine- and glutamate-rich protein is female salivary gland-specific and abundant in the malaria vector Anopheles dirus B (Diptera: Culicidae). J. Med. Entomol. 2006, 43:867-874.
73. Jennings B., Spearman W., Shephard E. A novel 25 kDa protein from the venom of Bitis arietans with similarity to C-type lectins causes fibrinogen-dependent platelet agglutination. Toxicon 2005, 46:687-698.
74. Johnson J.K., Li J., Christensen B.M. Cloning and characterization of a dopachrome conversion enzyme from the yellow fever mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 2001, 31:1125-1135.
75. Julenius K., Molgaard A., Gupta R., Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005, 15:153-164.
76. Kanost M.R. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 1999, 23:291-301.
77. Kato H., Anderson J.M., Kamhawi S., Oliveira F., Lawyer P.G., Pham V.M., Sangare C.S., Samake S., Sissoko I., Garfield M., et al. 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.
78. Kato H., Jochim R.C., Lawyer P.G., Valenzuela J.G. Identification and characterization of a salivary adenosine deaminase from the sand fly Phlebotomus duboscqi, the vector of Leishmania major in sub-Saharan Africa. J. Exp. Biol. 2007, 210:733-740.
79. Katz O., Waitumbi J.N., Zer R., Warburg A. Adenosine, AMP, and protein phosphatase activity in sandfly saliva. Am. J. Trop. Med. Hyg. 2000, 62:145-150.
80. Korayem A.M., Fabbri M., Takahashi K., Scherfer C., Lindgren M., Schmidt O., Ueda R., Dushay M.S., Theopold U. A Drosophila salivary gland mucin is also expressed in immune tissues: evidence for a function in coagulation and the entrapment of bacteria. Insect Biochem. Mol. Biol. 2004, 34:1297-1304.
81. Kotsyfakis M., Sa-Nunes A., Francischetti I.M., Mather T.N., Andersen J.F., Ribeiro J.M. Antiinflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis. J. Biol. Chem. 2006, 281:26298-26307.
82. Kotsyfakis M., Karim S., Andersen J.F., Mather T.N., Ribeiro J.M. Selective cysteine protease inhibition contributes to blood-feeding success of the tick Ixodes scapularis. J. Biol. Chem. 2007, 282:29256-29263.
83. Kotsyfakis M., Anderson J.M., Andersen J.F., Calvo E., Francischetti I.M., Mather T.N., Valenzuela J.G., Ribeiro J.M. Cutting edge: immunity against a "silent" salivary antigen of the Lyme vector Ixodes scapularis impairs its ability to feed. J. Immunol. 2008, 181:5209-5212.
84. Krzywinski J., Besansky N.J. Molecular systematics of Anopheles: from subgenera to subpopulations. Annu. Rev. Entomol. 2003, 48:111-139.
85. Krzywinski J., Grushko O.G., Besansky N.J. Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Mol. Phylogenet. Evol. 2006, 39:417-423.
86. Lanzaro G.C., Lopes A.H., Ribeiro J.M., Shoemaker C.B., Warburg A., Soares M., Titus R.G. Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex. Insect Mol. Biol. 1999, 8:267-275.
87. Lerner E.A., Shoemaker C.B. Maxadilan: cloning and functional expression of the gene encoding this potent vasodilator peptide. J. Biol. Chem. 1992, 267:1062-1066.
88. Lerner E.A., Ribeiro J.M.C., Nelson R.J., Lerner M.R. Isolation of maxadilan, a potent vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. J. Biol. Chem. 1991, 266:11234-11236.
89. Lombardo F., Di Cristina M., Spanos L., Louis C., Coluzzi M., Arcá B. Promoter sequences of the putative Anopheles gambiae apyrase confer salivary gland expression in Drosophila melanogaster. J. Biol. Chem. 2000, 275:23861-23868.
90. Lanfrancotti A., Lombardo F., Santolamazza F., Veneri M., Castrignanó T., Coluzzi M., Arcá B. Novel cDNAs encoding salivary proteins from the malaria vector Anopheles gambiae. FEBS Lett. 2002, 517:67-71.
91. Lombardo F., Ronca R., Rizzo C., Mestres-Simon M., Lanfrancotti A., Curra C., Fiorentino G., Bourgouin C., Ribeiro J.M., Petrarca V., et al. The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. Insect Biochem. Mol. Biol. 2009, 39:457-466.
92. Mans B.J., Francischetti I.M.B. Sialomic perspectives on the evolution of blood-feeding behavior in Arthropods: future therapeutics by natural design. Toxins and Hemostasis: From Bench to Bed-side 2010, Springer. R.M. Kini, K.J. Clemetson, F.S. Markland, M.A. McLane, T. Morita (Eds.).
93. 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.
94. Mans B.J., Andersen J.F., Francischetti I.M., Valenzuela J.G., Schwan T.G., Pham V.M., Garfield M.K., Hammer C.H., Ribeiro J.M. Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem. Mol. Biol. 2008, 38:42-58.
95. Marchler-Bauer A., Panchenko A.R., Shoemaker B.A., Thiessen P.A., Geer L.Y., Bryant S.H. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002, 30:281-283.
96. Marinotti O., James A.A. An alpha-glucosidase in the salivary glands of the vector mosquito, Aedes aegypti. Insect Biochem. 1990, 20:619-623.
97. Marinotti O., James A., Ribeiro J.M.C. Diet and salivation in female Aedes aegypti mosquitoes. J. Insect Physiol. 1990, 36:545-548.
98. Marinotti O., de Brito M., Moreira C.K. Apyrase and alpha-glucosidase in the salivary glands of Aedes albopictus. Comp. Biochem. Physiol. 1996, 113B:675-679.
99. Milleron R.S., Mutebi J.P., Valle S., Montoya A., Yin H., Soong L., Lanzaro G.C. Antigenic diversity in maxadilan, a salivary protein from the sand fly vector of American visceral leishmaniasis. Am. J. Trop. Med. Hyg. 2004, 70:286-293.
100. Milleron R.S., Ribeiro J.M., Elnaime D., Soong L., Lanzaro G.C. Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. Am. J. Trop. Med. Hyg. 2004, 70:278-285.
101. Milne T.J., Abbenante G., Tyndall J.D., Halliday J., Lewis R.J. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J. Biol. Chem. 2003, 278:31105-31110.
102. Montero-Solis C., Gonzalez-Ceron L., Rodriguez M.H., Cirerol B.E., Zamudio F., Possanni L.D., James A.A., de la Cruz Hernandez-Hernandez F. Identification and characterization of gp65, a salivary-gland-specific molecule expressed in the malaria vector Anopheles albimanus. Insect Mol. Biol. 2004, 13:155-164.
103. Moreira-Ferro C.K., Daffre S., James A.A., Marinotti O. A lysozyme in the salivary glands of the malaria vector Anopheles darlingi. Insect Mol. Biol. 1998, 7:257-264.
104. Morita T. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon 2005, 45:1099-1114.
105. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
106. Nobile M., Noceti F., Prestipino G., Possani L.D. Helothermine, a lizard venom toxin, inhibits calcium current in cerebellar granules. Exp. Brain Res. 1996, 110:15-20.
107. Oliveira F., Kamhawi S., Seitz A.E., Pham V.M., Guigal P.M., Fischer L., Ward J., Valenzuela J.G. From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 2006, 24:374-390.
108. Paesen G.C., Siebold C., Dallas M.L., Peers C., Harlos K., Nuttall P.A., Nunn M.A., Stuart D.I., Esnouf R.M. An ion-channel modulator from the saliva of the brown ear tick has a highly modified Kunitz/BPTI structure. J. Mol. Biol. 2009, 389:734-747.
109. Pawlowski J., Szadziewski R., Kmieciak D., Fahrni J., Bittar G. Phylogeny of the infraorder Culicomorpha (Diptera: Nematocera) based on the 28S RNA gene sequences. Syst. Entomol. 1996, 21.
110. Perez de Leon A., Tabachnick W.J. Apyrase activity and adenosine diphosphate induced platelet aggregation inhibition by the salivary gland proteins of Culicoides variipennis, the North American vector of bluetongue viruses. Vet. Parasitol. 1996, 61:327-338.
111. Poinsignon A., Cornelie S., Mestres-Simon M., Lanfrancotti A., Rossignol M., Boulanger D., Cisse B., Sokhna C., Arca B., Simondon F., et al. Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS ONE 2008, 3:e2472.
112. Poinsignon A., Cornelie S., Ba F., Boulanger D., Sow C., Rossignol M., Sokhna C., Cisse B., Simondon F., Remoue F. Human IgG response to a salivary peptide, gSG6-P1, as a new immuno-epidemiological tool for evaluating low-level exposure to Anopheles bites. Malar. J. 2009, 8:198.
113. Polgar J., Clemetson J.M., Kehrel B.E., Wiedemann M., Magnenat E.M., Wells T.N.C., Clemetson K.J. Platelet activation and signal transduction by convulxin, a C-type lectin from Crotalus durissus terrificus (tropical rattlesnake) venom via the p62/GPVI collagen receptor. J. Biol. Chem. 1997, 272:13576-13583.
114. Poole S., Lorenzetti B.B., Cunha J.M., Cunha F.Q., Ferreira S.H. Bradykinin B1 and B2 receptors, tumour necrosis factor alpha and inflammatory hyperalgesia. Br. J.Pharmacol. 1999, 126:649-656.
115. Rawlings N.D., Tolle D.P., Barrett A.J. Evolutionary families of peptidase inhibitors. Biochem. J. 2004, 378:705-716.
116. Rayms-Keller A., McGaw M., Oray C., Carlson J.O., Beaty B.J. Molecular cloning and characterization of a metal responsive Aedes aegypti intestinal mucin cDNA. Insect Mol. Biol. 2000, 9:419-426.
117. Remoue F., Cisse B., Ba F., Sokhna C., Herve J.P., Boulanger D., Simondon F. Evaluation of the antibody response to Anopheles salivary antigens as a potential marker of risk of malaria. Trans. R Soc. Trop. Med. Hyg. 2006, 100:363-370.
118. Reno H.E., Novak R.J. Characterization of apyrase-like activity in Ochlerotatus triseriatus, Ochlerotatus hendersoni, and Aedes aegypti. Am. J. Trop. Med. Hyg. 2005, 73:541-545.
119. Ribeiro J.M.C., Arca B. From sialomes to the sialoverse: an insight into the salivary potion of blood feeding insects. Adv. Insect Physiol. 2009, 37:59-118.
120. Ribeiro J.M., Francischetti I.M. Platelet-activating-factor-hydrolyzing phospholipase C in the salivary glands and saliva of the mosquito Culex quinquefasciatus. J. Exp. Biol. 2001, 204:3887-3894.
121. Ribeiro J.M., Modi G. The salivary adenosine/AMP content of Phlebotomus argentipes Annandale and Brunetti, the main vector of human kala-azar. J. Parasitol. 2001, 87:915-917.
122. Ribeiro J.M.C., Nussenzveig R.H. The salivary catechol oxidase/peroxidase activities of the mosquito, Anopheles albimanus. J. Exp. Biol. 1993, 179:273-287.
123. Ribeiro J.M., Valenzuela J.G. Purification and cloning of the salivary peroxidase/catechol oxidase of the mosquito Anopheles albimanus. J. Exp. Biol. 1999, 202:809-816.
124. Ribeiro J.M., Valenzuela J.G. The salivary purine nucleosidase of the mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 2003, 33:13-22.
125. Ribeiro J.M.C., Sarkis J.J.F., Rossignol P.A., Spielman A. Salivary apyrase of Aedes aegypti: characterization and secretory fate. Comp. Biochem. Physiol. 1984, 79B:81-86.
126. Ribeiro J.M.C., Rossignol P.A., Spielman A. Salivary gland apyrase determines probing time in anopheline mosquitoes. J. Insect Physiol. 1985, 9:551-560.
127. Ribeiro J.M.C., Rossignol P.A., Spielman A. Blood finding strategy of a capillary feeding sandfly, Lutzomyia longipalpis. Comp. Biochem. Physiol. 1986, 83A:683-686.
128. Ribeiro J.M.C., Modi G.B., Resh R.B. Salivary apyrase activity of some old world phlebotomine sand flies. Insect Biochem. 1989, 19:409-412.
129. Ribeiro J.M., Katz O., Pannell L.K., Waitumbi J., Warburg A. Salivary glands of the sand fly Phlebotomus papatasi contain pharmacologically active amounts of adenosine and 5'-AMP. J. Exp. Biol. 1999, 202:1551-1559.
130. Ribeiro J.M., Charlab R., Rowton E.D., Cupp E.W. Simulium vittatum (Diptera: Simuliidae) and Lutzomyia longipalpis (Diptera: Psychodidae) salivary gland hyaluronidase activity. J. Med. Entomol. 2000, 37:743-747.
131. Ribeiro J.M., Rowton E.D., Charlab R. The salivary 5'-nucleotidase/phosphodiesterase of the hematophagous sand fly, Lutzomyia longipalpis. Insect Biochem. Mol. Biol. 2000, 30:279-285.
132. Ribeiro J.M., Charlab R., Valenzuela J.G. The salivary adenosine deaminase activity of the mosquitoes Culex quinquefasciatus and Aedes aegypti. J. Exp. Biol. 2001, 204:2001-2010.
133. Ribeiro J.M., Charlab R., Pham V.M., Garfield M., Valenzuela J.G. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem. Mol. Biol. 2004, 34:543-563.
134. Ribeiro J.M., Arca B., Lombardo F., Calvo E., Phan V.M., Chandra P.K., Wikel S.K. An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 2007, 8:6.
135. Ribeiro J.M., Valenzuela J.G., Pham V.M., Kleeman L., Barbian K.D., Favreau A.J., Eaton D.P., Aoki V., Hans-Filho G., Rivitti E.A., et al. An insight into the sialotranscriptome of Simulium nigrimanum, a black fly associated with fogo selvagem in South America. Am. J. Trop. Med. Hyg. 2010, 82:1060-1075.
136. Ribeiro J.M.C. Blood-feeding arthropods: live syringes or invertebrate pharmacologists?. Infect. Agents Dis. 1995, 4:143-152.
137. Ribeiro J.M. Blood-feeding in mosquitoes: probing time and salivary gland anti- haemostatic activities in representatives of three genera (Aedes, Anopheles, Culex). Med. Vet. Entomol. 2000, 14:142-148.
138. Rossignol P.A., Lueders A.M. Bacteriolytic factor in the salivary glands of Aedes aegypti. Comp. Biochem. Physiol. 1986, 83B:819-822.
139. Russell C.L., Heesom K.J., Arthur C.J., Helps C.R., Mellor P.S., Day M.J., Torsteinsdottir S., Bjornsdottir T.S., Wilson A.D. Identification and isolation of cDNA clones encoding the abundant secreted proteins in the saliva proteome of Culicoides nubeculosus. Insect Mol. Biol. 2009, 18:383-393.
140. Sarauer B.L., Gillott C., Hegedus D. Characterization of an intestinal mucin from the peritrophic matrix of the diamondback moth, Plutella xylostella. Insect Mol. Biol. 2003, 12:333-343.
141. Schluter H., Tepel M., Zidek W. Vascular actions of diadenosine phosphates. J. Auton. Pharmacol. 1996, 16:357-362.
142. Schwartz B.S., Ribeiro J.M., Goldstein M.D. Anti-tick antibodies: an epidemiologic tool in Lyme disease research. Am. J. Epidemiol 1990, 132:58-66.
143. Schwartz B.S., Ford D.P., Childs J.E., Thomas R.J. Anti-tick saliva antibody: a biologic marker of tick exposure that is a risk factor for Lyme disease seropositivity. Am. J. Epidemiol. 1991, 134:86-95.
144. Shi L., Paskewitz S.M. Identification and molecular characterization of two immune-responsive chitinase-like proteins from Anopheles gambiae. Insect Mol. Biol. 2004, 13:387-398.
145. Simons F.E., Peng Z. Mosquito allergy: recombinant mosquito salivary antigens for new diagnostic tests. Int. Arch. Allergy Immunol. 2001, 124:403-405.
146. Sonnhammer E.L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1998, 6:175-182.
147. Stark K.R., James A.A. A factor Xa-directed anticoagulant from the salivary glands of the yellow fever mosquito Aedes aegypti. Exp. Parasitol. 1995, 81:321-331.
148. Stark K.R., James A.A. Isolation and characterization of the gene encoding a novel factor Xa-directed anticoagulant from the yellow fever mosquito, Aedes aegypti. J. Biol. Chem. 1998, 273:20802-20809.
149. Stutzer C., Mans B.J., Gaspar A.R., Neitz A.W., Maritz-Olivier C. Ornithodoros savignyi: soft tick apyrase belongs to the 5'-nucleotidase family. Exp. Parasitol. 2009, 122:318-327.
150. Sun D., McNicol A., James A.A., Peng Z. Expression of functional recombinant mosquito salivary apyrase: a potential therapeutic platelet aggregation inhibitor. Platelets 2006, 17:178-184.
151. Thiel S. Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol. Immunol. 2007, 44:3875-3888.
152. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
153. Tilley S.L., Wagoner V.A., Salvatore C.A., Jacobson M.A., Koller B.H. Adenosine and inosine increase cutaneous vasopermeability by activating A(3) receptors on mast cells. J. Clin. Invest. 2000, 105:361-367.
154. Torres A.M., Kuchel P.W. The beta-defensin-fold family of polypeptides. Toxicon 2004, 44:581-588.
155. Trujillo M., Ferrer-Sueta G., Thomson L., Flohe L., Radi R. Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite. Subcell. Biochem. 2007, 44:83-113.
156. Valenzuela J.G., Charlab R., Galperin M.Y., Ribeiro J.M. Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme. J. Biol. Chem. 1998, 273:30583-30590.
157. Valenzuela J.G., Francischetti I.M., Ribeiro J.M. Purification, cloning, and synthesis of a novel salivary anti-thrombin from the mosquito Anopheles albimanus. Biochemistry 1999, 38:11209-11215.
158. Valenzuela J.G., Belkaid Y., Garfield M.K., Mendez S., Kamhawi S., Rowton E.D., Sacks D.L., Ribeiro J.M. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J. Exp. Med. 2001, 194:331-342.
159. Valenzuela J.G., Belkaid Y., Rowton E., Ribeiro J.M. The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases. J. Exp. Biol. 2001, 204:229-237.
160. Valenzuela J.G., Charlab R., Gonzalez E.C., Miranda-Santos I.K.F., Marinotti O., Francischetti I.M., Ribeiro J.M.C. The D7 family of salivary proteins in blood sucking Diptera. Insect Mol. Biol. 2002, 11:149-155.
161. Valenzuela J.G., Pham V.M., Garfield M.K., Francischetti I.M., Ribeiro J.M.C. Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 2002, 32:1101-1122.
162. Valenzuela J.G., Francischetti I.M., Pham V.M., Garfield M.K., Ribeiro J.M. Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem. Mol. Biol. 2003, 33:717-732.
163. Valenzuela J.G., Garfield M., Rowton E.D., Pham V.M. Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J. Exp. Biol. 2004, 207:3717-3729.
164. Vizioli J., Bulet P., Hoffmann J.A., Kafatos F.C., Muller H.M., Dimopoulos G. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12630-12635.
165. Volfova V., Hostomska J., Cerny M., Votypka J., Volf P. Hyaluronidase of bloodsucking insects and its enhancing effect on leishmania infection in mice. PLoS Negl. Trop. Dis. 2008, 2:e294.
166. Wang X., Ribeiro J.M., Broce A.B., Wilkerson M.J., Kanost M.R. An insight into the transcriptome and proteome of the salivary gland of the stable fly, Stomoxys calcitrans. Insect Biochem. Mol. Biol. 2009.
167. Wilson A.D., Heesom K.J., Mawby W.J., Mellor P.S., Russell C.L. Identification of abundant proteins and potential allergens in Culicoides nubeculosus salivary glands. Vet. Immunol. Immunopathol. 2008, 122:94-103.
168. Xu X., Yang H., Ma D., Wu J., Wang Y., Song Y., Wang X., Lu Y., Yang J., Lai R. Toward an understanding of the molecular mechanism for successful blood feeding by coupling proteomics analysis with pharmacological testing of horsefly salivary glands. Mol. Cell. Proteomics 2008, 7:582-590.
169. Yamazaki Y., Koike H., Sugiyama Y., Motoyoshi K., Wada T., Hishinuma S., Mita M., Morita T. Cloning and characterization of novel snake venom proteins that block smooth muscle contraction. Eur. J. Biochem. 2002, 269:2708-2715.
170. Yeates D.K., Wiegmann B.M. Congruence and controversy: toward a higher-level phylogeny of Diptera. Annu. Rev. Entomol. 1999, 44:397-428.
171. Yoshida S., Watanabe H. Robust salivary gland-specific transgene expression in Anopheles stephensi mosquito. Insect Mol. Biol. 2006, 15:403-410.
172. Yoshida S., Sudo T., Niimi M., Tao L., Sun B., Kambayashi J., Watanabe H., Luo E., Matsuoka H. Inhibition of collagen-induced platelet aggregation by anopheline antiplatelet protein, a saliva protein from a malaria vector mosquito. Blood 2008, 111:2007-2014.
173. Zavalova L.L., Baskova I.P., Lukyanov S.A., Sass A.V., Snezhkov E.V., Akopov S.B., Artamonova, Archipova V.S., Nesmeyanov V.A., Kozlov D.G., et al. Destabilase from the medicinal leech is a representative of a novel family of lysozymes. Biochim. Biophys. Acta 2000, 1478:69-77.
174. Zeidner N.S., Higgs S., Happ C.M., Beaty B.J., Miller B.R. Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunol. 1999, 21:35-44.