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Sialomic Perspectives on the Evolution of Blood-Feeding Behavior in Arthropods: Future Therapeutics by Natural Design

  • B.J. Mans
  • I.M.B. Francischetti
Chapter

Abstract

Blood-feeding behavior evolved more than 20 times independently in Arthropods. This happened at least 6 times in the Arachnida (Acari) and 15 times in the Hexapoda (Neoptera). This is recapitulated when transcriptomes from the secretory component of salivary glands (Sialomes) are compared. As such, unique protein families are found for the different lineages that adapted to a blood-feeding lifestyle with only a limited number of protein families conserved across all lineages. Closely related lineages might share similar sets of protein families in their sialomes, even if no apparent orthologous or conserved functional relationships exist. This suggests that sialomes of such lineages where already defined before adaptation to a blood-feeding lifestyle, with subsequent innovation. In this regard, the same sets of shared protein families tend to be abundant and prone to lineage specific expansion (gene duplication) with specialized functions associated with various gene duplicates. Perhaps not surprisingly, all sialomes show evidence of convergent evolution in regard modulatory strategies that targets host defenses, even if the molecular mechanisms differ. As such, a checklist of expected functions can be composed for any blood-feeding arthropod not yet characterized. The diversity of mechanisms that counteract vertebrate host immune and hemostatic systems is a veritable pharmacopoeia, optimized by natural evolution, that can be exploited for therapeutic use.

Keywords

Salivary Gland Tissue Factor Pathway Inhibitor Salivary Protein Edman Degradation Hard Tick 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This work was supported by the Intramural Research Program of the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health. Because IMBF is a government employee and this is a government work, the work is in the public domain in the United States. Notwithstanding any other agreements, the NIH reserves the right to provide the work to PubMedCentral for display and use by the public, and PubMedCentral may tag or modify the work consistent with its customary practices. You can establish rights outside of the U.S. subject to a government use license.

References

  1. Alarcon-Chaidez, F.J., Sun, J., Wikel, S.K., 2007. Transcriptome analysis of the salivary glands of Dermacentor andersoni stiles (Acari: Ixodidae). Insect Biochem. Mol. Biol. 37, 48–71.PubMedCrossRefGoogle Scholar
  2. Aljamali, M.N., Hern L., Kupfer D., Downard S., So S., Roe B.A., Sauer J.R., Essenberg R.C., 2009. Transcriptome analysis of the salivary glands of the female tick Amblyomma americanum (Acari: Ixodidae) Insect Mol. Biol. 18, 129–154.PubMedCrossRefGoogle Scholar
  3. Andersen, J.F., Champagne, D.E., Weichsel, A., Ribeiro, J.M., Balfour, C.A., Dress, V., Montfort, W.R., 1997. Nitric oxide binding and crystallization of recombinant nitrophorin I, a nitric oxide transport protein from the blood-sucking bug Rhodnius prolixus. Biochemistry 36, 4423–4428.PubMedCrossRefGoogle Scholar
  4. Andersen, J.F., Francischetti, I.M., Valenzuela, J.G., Schuck, P., Ribeiro, J.M., 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.PubMedCrossRefGoogle Scholar
  5. Andersen, J.F., Gudderra, N.P., Francischetti, I.M., Ribeiro, J.M., 2005. The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch. Insect Biochem. Physiol. 58, 97–105.PubMedCrossRefGoogle Scholar
  6. Andersen, J.F., Ribeiro, J.M., 2006. A secreted salivary inositol polyphosphate 5-phosphatase from a blood-feeding insect: allosteric activation by soluble phosphoinositides and phosphatidylserine. Biochemistry 45, 5450–5457.PubMedCrossRefGoogle Scholar
  7. Andersen, J.F., Hinnebusch, B.J., Lucas, D.A., Conrads, T.P., Veenstra, T.D., Pham, V.M., Ribeiro, J.M., 2007. An insight into the sialome of the oriental rat flea, Xenopsylla cheopis (Rots). BMC Genomics 8, 102.PubMedCrossRefGoogle Scholar
  8. Andersen, J.F., Pham, V.M., Meng, Z., Champagne, D.E., Ribeiro, J.M., 2009. Insight into the sialome of the Black Fly, Simulium vittatum. J. Proteome Res. 8, 1474–1488.PubMedCrossRefGoogle Scholar
  9. Andersen, J.F., 2010. Structure and mechanism in salivary proteins from blood-feeding arthropods. Toxicon (In press).Google Scholar
  10. Anderson, J.M., Oliveira, F., Kamhawi, S., Mans, B.J., Reynoso, D., Seitz, A.E., Lawyer, P., Garfield, M., Pham, M., Valenzuela, J.G., 2006. Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 7, 52.PubMedCrossRefGoogle Scholar
  11. Arca, B., Lombardo, F., Valenzuela, J.G., Francischetti, I.M., Marinotti, O., Coluzzi, M., Ribeiro, J.M., 2005. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J. Exp. Biol. 208, 3971–3986.Google Scholar
  12. Arca, B., Lombardo, F., Francischetti, I.M., Pham, V.M., Mestres-Simon, M., Andersen, J.F., Ribeiro, J.M., 2007. An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem. Mol. Biol. 37, 107–127.PubMedCrossRefGoogle Scholar
  13. Assumpcao, T.C., Francischetti, I.M., Andersen, J.F., Schwarz, A., Santana, J.M., Ribeiro, J.M., 2008. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease. Insect Biochem. Mol. Biol. 38, 213–232.PubMedCrossRefGoogle Scholar
  14. Batista, I.F.C., Chudzinski-Tavassi, A.M., Faria, F., Simons, S.M., Barros-Batestti, D.M., Labruna, M.B., Leão, L.I., Ho, P.L., Junqueira-de-Azevedo, I.L., 2008. Expressed sequence tags (ESTs) from the salivary glands of the tick Amblyomma cajannense (Acari: Ixodidae). Toxicon 51, 823–834.PubMedCrossRefGoogle Scholar
  15. Beaufays, J., Adam, B, Menten-Dedoyart, C, Fievez, L., Grosjean, A., Decrem, Y., Prevot, P., Santini, S., Brasseur, R., Brossard, M., Vanhaeverbeek, M., Bureau, F., Heinen, E., Lins, L., Vanhamme, L., Godfroid, E., 2008. Ir-LBP, an Ixodes ricinus tick salivary LTB4-binding lipocalin, interferes with host neutrophil function. PLoS 3, 1–13.Google Scholar
  16. Binnington, K.C., 1978. Sequenctial changes in salivary gland structure during attachment and feeding of the cattle tick, Boophilus microplus. Int. J. Parasitol. 8, 97–115.PubMedCrossRefGoogle Scholar
  17. Binnington, K.C., Stone, B.F., 1981. Developmental changes in morphology and toxin content of the salivary gland of the australian paralysis tick Ixodes holocyclus. Int. J. Parasitol. 11, 343–351.CrossRefGoogle Scholar
  18. Bochkov, A.V., Connor, B.M., Wauthy, G., 2008. Phylogenetic position of the mite family Myobiidae within the infraorder Eleutherengona (Acariformes) and origins of parasitism in eleutherengone mites. Zool. Anz. 247, 15–45.CrossRefGoogle Scholar
  19. Calvo, E., Andersen, J., Francischetti, I.M., de, L.C.M., deBianchi, A.G., James, A.A., Ribeiro, J.M., Marinotti, O., 2004. The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol. Biol. 13, 73–88.PubMedCrossRefGoogle Scholar
  20. Calvo, E., Mans, B.J., Andersen, J.F., Ribeiro, J.M., 2006. Function and evolution of a mosquito salivary protein family. J. Biol. Chem. 281, 1935–1942.PubMedCrossRefGoogle Scholar
  21. Calvo, E., Dao, A., Pham, V.M., Ribeiro, J.M., 2007a. An insight into the sialome of Anopheles funestus reveals an emerging pattern in anopheline salivary protein families. Insect Biochem. Mol. Biol. 37, 164–175.PubMedCrossRefGoogle Scholar
  22. Calvo, E., Tokumasu, F., Marinotti, O., Villeval, J.L., Ribeiro, J.M., Francischetti, I.M., 2007b. 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. 282, 26928–26938.PubMedCrossRefGoogle Scholar
  23. Calvo, E., Mans, B.J., Ribeiro, J.M., Andersen, J.F., 2009a. Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc. Natl. Acad. Sci., U.S.A. 106, 3728–3733.PubMedCrossRefGoogle Scholar
  24. Calvo, E., Pham, V.M., Marinotti, O., Andersen, J.F., Ribeiro, J.M., 2009b. The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics 10, 57.PubMedCrossRefGoogle Scholar
  25. Calvo, E., Tokumasu, F., Mizurini, D.M., McPhie, P., Narum, D.L., Ribeiro, J.M., Monteiro, R.Q., Francischetti, I.M., 2010. Aegyptin displays high-affinity for the von Willebrand factor binding site (RGQOGVMGF) in collagen and inhibits carotid thrombus formation in vivo. FEBS J. 277, 413–427.PubMedCrossRefGoogle Scholar
  26. Campbell, C.L., Vandyke, K.A., Letchworth, G.J., Drolet, B.S., Hanekamp, T., Wilson, W.C., 2005. Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol. Biol. 14, 121–136.PubMedCrossRefGoogle Scholar
  27. Champagne, D.E., 2004. Antihemostatic strategies of blood-feeding arthropods. Curr. Drug Targets – Cardiovasc. Haematol. Dis. 4, 375–396.CrossRefGoogle Scholar
  28. Charlab, R., Valenzuela, J.G., Rowton, E.D., Ribeiro, J.M., 1999. 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 96, 15155–15160.Google Scholar
  29. Chmelař, J., Anderson, J.M., Mu, J., Jochim, R.C., Valenzuela, J.G., Kopecký, J., 2008. Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 9, 233.PubMedCrossRefGoogle Scholar
  30. Cornwall, J.W., Patton, W.S., 1914. Some observations on the salivary secretion of the commoner blood-cuking insects and ticks. Ind. J. Med. Res. 2, 569–593.Google Scholar
  31. Corral-Rodrıguez, C.A., Macedo-Ribeiro, S., Pereira P.J.B., Fuentes-Prior, P., 2009. Tick-derived Kunitz-type inhibitors as antihemostatic factors. Insect Biochem. Mol. Biol. 39, 579–595.PubMedCrossRefGoogle Scholar
  32. Dai, J., Liu, J., Deng, Y., Smith, T.M., Lu, M., 2004. Structure and protein design of a human platelet function inhibitor. Cell 116, 649–659.PubMedCrossRefGoogle Scholar
  33. Decrem, Y., Rath, G., Blasioli, V., Cauchie, P., Robert, S., Beaufays, J., Frere, J.M., Feron, O., Dogne, J.M., Dessy, C., Vanhamme, L., Godfroid, E., 2009. Ir-CPI, a coagulation contact phase inhibitor from the tick Ixodes ricinus, inhibits thrombus formation without impairing hemostasis. J. Exp. Med. 206, 2381–2395.PubMedCrossRefGoogle Scholar
  34. Fox, J.W., Serrano, S.M., 2007. Approaching the golden age of natural product pharmaceuticals from venom libraries: an overview of toxins and toxin-derivatives currently involved in therapeutic or diagnostic applications. Curr. Pharm. Des. 13, 2927–2934.PubMedCrossRefGoogle Scholar
  35. Francischetti, I.M., Valenzuela, J.G., Ribeiro, J.M., 1999. Anophelin: kinetics and mechanism of thrombin inhibition. Biochemistry 38, 16678–16685.PubMedCrossRefGoogle Scholar
  36. Francischetti, I.M., Valenzuela, J.G., Pham, V.M., Garfield, M.K., Ribeiro, J.M., 2002a. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J. Exp. Biol. 205, 2429–2451.PubMedGoogle Scholar
  37. Francischetti, I.M., Valenzuela, J.G., Andersen, J.F., Mather, T.N., Ribeiro, J.M., 2002b. Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex. Blood 99, 3602–3612.PubMedCrossRefGoogle Scholar
  38. Francischetti, I.M., Andersen, J.F., Ribeiro, J.M., 2002c. 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.PubMedCrossRefGoogle Scholar
  39. Francischetti, I.M., My Pham, V., Mans, B.J., Andersen, J.F., Mather, T.N., Lane, R.S., Ribeiro, J.M., 2005. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem. Mol. Biol. 35, 1142–1161.PubMedCrossRefGoogle Scholar
  40. Francischetti, I.M., Mans, B.J., Meng, Z., Gudderra, N., Veenstra, T.D., Pham, V.M., Ribeiro, J.M., 2008a. An insight into the sialome of the soft tick, Ornithodorus parkeri. Insect Biochem. Mol. Biol. 38, 1–21.PubMedCrossRefGoogle Scholar
  41. Francischetti, I.M., Meng, Z., Mans, B.J., Gudderra, N., Hall, M., Veenstra, T.D., Pham, V.M., Kotsyfakis, M., Ribeiro, J.M., 2008b. An insight into the salivary transcriptome and proteome of the soft tick and vector of epizootic bovine abortion, Ornithodoros coriaceus. J. Proteomics 71, 493–512.PubMedCrossRefGoogle Scholar
  42. Francischetti, I.M.B., Sa-Nunes, A., Mans, B.J., Santos, I.M., Ribeiro J.M.C., 2009. The role of saliva in tick feeding. Front. Biosci. 14, 2051–2088.PubMedCrossRefGoogle Scholar
  43. Frauenschuh, A., Power, C.A., Deruaz, M., Ferreira, B.R., Silva, J.S., Teixeira, M.M., Dias, J.M., Martin, T., Wells, T.N., Proudfoot, A.E., 2007. Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. J. Biol. Chem. 282, 27250–27258.PubMedCrossRefGoogle Scholar
  44. Fry, B.G., Roelants, K., Champagne, D.E., Scheib, H., Tyndall, J.D.A., King, G.F., Nevalainen, T.J., Norman, J.A., Lewis, R.J., Norton, R.S., Renjifo, C., Rodriguez de la Vega, R.C.R., 2009. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Gen. Hum. Genet. 10, 23.1–23.29.Google Scholar
  45. Giribet, G., Edgecombe, G.D., Wheeler, W.C., Babbitt, C., 2002. Phylogeny and systematic position of opiliones: a combined analysis of chelicerate relationships using morphological and molecular data. Cladistics 18, 5–70.PubMedGoogle Scholar
  46. Greinacher, A., Warkentin, T.E., 2008. The direct thrombin inhibitor hirudin. Thromb. Haemost. 99, 819–829.PubMedGoogle Scholar
  47. Grimaldi D., Engel, M.S., 2005. Evolution of the Insects, first ed. Cambridge University Press, New York.Google Scholar
  48. Guo, Y., Ribeiro, J.M., Anderson, J.M., Bour, S., 2009. dCas: a desktop application for cDNA sequence annotation. Bioinformatics 25, 1195–1196.PubMedCrossRefGoogle Scholar
  49. Gutierrez, J.M., Lomonte, B., Leon, G., Alape-Giron, A., Flores-Diaz, M., Sanz, L., Angulo, Y., Calvete, J.J., 2009. Snake venomics and antivenomics: proteomic tools in the design and control of antivenoms for the treatment of snakebite envenoming. J. Proteomics 72, 165–182.PubMedCrossRefGoogle Scholar
  50. Hepburn, N.J., Williams, A.S., Nunn, M.A., Chamberlain-Banoub, J.C., Hamer, J., Morgan, B.P., Harris, C.L. 2007. In vivo characterization and therapeutic efficacy of a C5-specific inhibitor from the soft tick Ornithodoros moubata. J. Biol. Chem. 282, 8292–8299.PubMedCrossRefGoogle Scholar
  51. Hostomská, J., Volfová, V., Mu, J., Garfield, M., Rohoušová, I., Volf, P., Valenzuela, J.G., Jochim, R.C., 2009. Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics 10, 282.PubMedCrossRefGoogle Scholar
  52. Howlett, R., 1998. Nobel award stirs up debate on nitric oxide breakthrough. Nature 395, 625–626.PubMedCrossRefGoogle Scholar
  53. Kato, G.J., 2008. Novel small molecule therapeutics for sickle cell disease: nitric oxide, carbon monoxide, nitrite, and apolipoprotein A-I. Hematology Am. Soc. Hematol. Educ. Program 186–192.Google Scholar
  54. Kato, H., Anderson, J.M., Kamhawi, S., Oliveira, F., Lawyer, P.G., Pham, V.M., Sangare, C.S., Samake, S., Sissoko, I., Garfield, M., Sigutova, L., Volf, P., Doumbia, S., Valenzuela, J.G., 2006. High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya). BMC Genomics 7, 226.PubMedCrossRefGoogle Scholar
  55. Kato, H., Jochim, R.C., Sakoda, R., Iwata, H., Gomez, E.A., Valenzuela, J.G., Hashiguchi, Y., 2008. A repertoire of the dominant transcripts from the salivary glands of the blood-sucking bug, Triatoma dimidiata, a vector of Chagas disease. Inf. Gen. Evol. 10, 184–191.Google Scholar
  56. Klompen, H., Lekveishvili, M., Black., W.C., 2007. Phylogeny of parasitiform mites (Acari) based on rRNA. Mol. Phyl. Evol. 43, 936–951.CrossRefGoogle Scholar
  57. Koh, C.Y., Kini, R.M., 2009. Molecular diversity of anticoagulants from haematophagous animals. Thromb. Haemost. 102, 437–453.PubMedGoogle Scholar
  58. Krug, S., Sablotzki, A., Hammerschmidt, S., Wirtz, H., Seyfarth, H.J., 2009. Inhaled iloprost for the control of pulmonary hypertension. Vasc. Health Risk Manag. 5, 465–474.PubMedCrossRefGoogle Scholar
  59. Lai, R., Takeuchi, H., Jonczy, J., Rees, H.H., Turner, P.C., 2004. A thrombin inhibitor from the ixodid tick, Amblyomma hebraeum. Gene 342, 243–249.PubMedCrossRefGoogle Scholar
  60. Law, J., Ribeiro, J.M.C., Wells, M., 1992. Biochemical insights derived from diversity in insects. Ann. Rev. Biochem. 61, 87–112.PubMedCrossRefGoogle Scholar
  61. Lehane, M., 2005. The Biology of Blood-Sucking in Insects, first ed. Cambridge University Press, New York.CrossRefGoogle Scholar
  62. Macedo-Ribeiro, S., Almeida, C., Calisto, B.M., Friedrich, T., Mentele, R., Sturzebecher, J., Fuentes-Prior, P., Pereira, P.J.B. 2008. Isolation, cloning and structural characterisation of boophilin, a multifunctional Kunitz-type proteinase inhibitor from the cattle tick. PLoS One 3, 1–17.CrossRefGoogle Scholar
  63. Madden, R.D., Sauer, J.R., Dillwith, J.W., 2002. A proteomics approach to characterizing tick salivary secretions. Exp. Appl. Acarol. 28, 77–87.PubMedCrossRefGoogle Scholar
  64. Mans, B.J., 2005. Tick histamine-binding proteins and related lipocalins: potential as therapeutic agents. Curr. Opin. Investig. Drugs 6, 1131–1135.PubMedGoogle Scholar
  65. Mans, B.J., Louw, A.I., Neitz, A.W., 2002. Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Mol. Biol. Evol. 19, 1695–1705.PubMedCrossRefGoogle Scholar
  66. Mans, B.J., Neitz, A.W., 2004. Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem. Mol. Biol. 34, 1–17.PubMedCrossRefGoogle Scholar
  67. Mans, B.J., Calvo, E., Ribeiro, J.M.C., Andersen, J.F. 2007. The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J. Biol. Chem. 282, 36626–36633.PubMedCrossRefGoogle Scholar
  68. 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., 2008a. Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem. Mol. Biol. 38, 42–58.PubMedCrossRefGoogle Scholar
  69. Mans, B.J., Andersen, J.F., Schwan, T.G., Ribeiro, J.M., 2008b. Characterization of anti-hemostatic factors in the argasid, Argas monolakensis: implications for the evolution of bloodfeeding in the soft tick family. Insect Biochem. Mol. Biol. 38, 22–41.PubMedCrossRefGoogle Scholar
  70. Mans, B.J., Ribeiro, J.M., Andersen, J.F., 2008c. Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J. Biol. Chem. 283, 18721–18733.PubMedCrossRefGoogle Scholar
  71. Mans, B.J., Ribeiro, J.M.C., 2008a. Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem. Mol. Biol. 38, 841–852.PubMedCrossRefGoogle Scholar
  72. Mans B.J., Ribeiro, J.M.C. 2008b. A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem. Mol. Biol. 38, 862–870.PubMedCrossRefGoogle Scholar
  73. Maritz-Olivier, C., Stutzer, C., Jongejan, F., Neitz, A.W., Gaspar, A.R., 2007. Tick anti-hemostatics: targets for future vaccines and therapeutics. Trends Parasitol. 23, 397–407.PubMedCrossRefGoogle Scholar
  74. Montfort, W.R., Weichsel, A., Andersen, J.F. 2000. Nitrophorins and related antihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods. Biochim. Biophys. Acta 1482, 110–118.PubMedCrossRefGoogle Scholar
  75. Nazareth, R.A., Tomaz, L.S., Ortiz-Costa, S., Atella, G.C., Ribeiro, J.M., Francischetti, I.M., Monteiro, R.Q., 2006. Antithrombotic properties of Ixolaris, a potent inhibitor of the extrinsic pathway of the coagulation cascade. Thromb. Haemost. 96, 7–13.PubMedGoogle Scholar
  76. Nene, V., Lee, D., Quackenbush, J., Skilton, R., Mwaura, S., Gardner, M.J., Bishop, R., 2002. AvGI, an index of genes transcribed in the salivary glands of the ixodid tick Amblyomma variegatum. Int. J. Parasitol. 32, 1447–1456.PubMedCrossRefGoogle Scholar
  77. Nene, V., Lee, D., Kang’a, S., Skilton, R., Shah, T., de Villiers, E., Mwaura, S., Taylor, D., Quackenbush, J., Bishop, R., 2004. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem. Mol. Biol. 34, 1117–1128.PubMedCrossRefGoogle Scholar
  78. Nuttall, G.H.F., Strickland, B.A., 1909. On the presence of an anticoagulin in the salivary glands and intestines of Argas persicus. Parasitology 1, 302–310.Google Scholar
  79. Oates, J.A., 1982. The 1982 Nobel Prize in Physiology or Medicine. Science 218, 765–768.PubMedCrossRefGoogle Scholar
  80. Oleaga, A., Escudero-Poblacion, A., Camafeita, E., Perez-Sanchez, R., 2007. A proteomic approach to the identification of salivary proteins from the argasid ticks Ornithodoros moubata and Ornithodoros erraticus. Insect Biochem. Mol. Biol. 37, 1149–1159.PubMedCrossRefGoogle Scholar
  81. Oliveira, F., Kamhawi, S., Seitz, A.E., Pham, V.M., Guigal, P.M., Fischer, L., Ward, J., Valenzuela, J.G. 2006. From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 24, 374–390.PubMedCrossRefGoogle Scholar
  82. Paesen, G.C., Adams, P.L., Harlos, K., Nuttall, P.A., Stuart, D.I., 1999. Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol. Cell 3, 661–671.PubMedCrossRefGoogle Scholar
  83. Radovsky, F.J., 1969. Adaptive radiation in the parasitic mesostigmata. Acarologia 11, 450–483.PubMedGoogle Scholar
  84. Ribeiro, J.M., Makoul, G.T., Levine, J., Robinson, D.R., Spielman, A., 1985. Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. J. Exp. Med. 161, 332–344.PubMedCrossRefGoogle Scholar
  85. Ribeiro, J.M.C., Marinotti, O., Gonzales, R., 1990. A salivary vasodilator in the blood-sucking bug, Rhodnius prolixus. Br. J. Pharmacol. 101, 932–936.PubMedCrossRefGoogle Scholar
  86. Ribeiro, J.M., Hazzard, J.M., Nussenzveig, R.H., Champagne, D.E., Walker, F.A., 1993. Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect. Science 260, 539–541.PubMedCrossRefGoogle Scholar
  87. Ribeiro, J.M., 1995. Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect. Agents Dis. 4, 143–152.Google Scholar
  88. Ribeiro, J.M., Francischetti, I.M., 2003. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu. Rev. Entomol. 48, 73–88.PubMedCrossRefGoogle Scholar
  89. Ribeiro, J.M., Andersen, J.F., Silva-Neto, M.A., Pham, V.M., Garfield, M.K., Valenzuela, J.G., 2004a. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem. Mol. Biol. 34, 61–79.PubMedCrossRefGoogle Scholar
  90. Ribeiro, J.M., Charlab, R., Pham, V.M., Garfield, M., Valenzuela, J.G., 2004b. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem. Mol. Biol. 34, 543–563.PubMedCrossRefGoogle Scholar
  91. Ribeiro, J.M., Alarcon-Chaidez, F., Francischetti, I.M., Mans, B.J., Mather, T.N., Valenzuela, J.G., Wikel, S.K., 2006. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol. 36, 111–129.PubMedCrossRefGoogle Scholar
  92. Ribeiro, J.M., Arca, B., Lombardo, F., Calvo, E., Phan, V.M., Chandra, P.K., Wikel, S.K., 2007. An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8, 6.PubMedCrossRefGoogle Scholar
  93. Russell, C.L., Heesom, K.J., Arthur, C.J., Helps, C.R., Mellor, P.S., Day, M.J., Torsteinsdottir, S., Björnsdóttir, T.S., Wilson, A.D., 2009. Identification and isolation of cDNA clones encoding the abundant secreted proteins in the saliva proteome of Culicoides nubeculosus. Insect Mol. Biol. 18, 383–393.PubMedCrossRefGoogle Scholar
  94. Sabbatani, L., 1899. Fermento anticoagulante de l’ “Ixodes ricinus”. Arch. Ital. Biol. 31, 37–53.Google Scholar
  95. Sangamnatdej, S., Paesen, G.C., Slovak, M., Nuttall, P.A., 2002. A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Mol. Biol. 11, 79–86.PubMedCrossRefGoogle Scholar
  96. Santos, A., Ribeiro, J.M.C., Lehane, M.J., Gontijo, N.F., Veloso, A.B., Sant' Anna, M.R.V., Nascimento Araujo, R., Grisard, E.C., Pereira, M.H., 2007. The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae). Insect Biochem. Mol. Biol. 37, 702–712.PubMedCrossRefGoogle Scholar
  97. Schofield, C.J., Galvão, C., 2009. Classification, evolution, and species groups within the Triatominae. Acta. Trop. 110, 88–100.PubMedCrossRefGoogle Scholar
  98. Schuh, R.T., Weirauch, C., Wheeler, W.C., 2009. Phylogenetic relationships within the cimicomorpha (Hemiptera: Heteroptera): a total-evidence analysis. Sys. Entomol. 34, 15–48.CrossRefGoogle Scholar
  99. Skerra, A., 2008. Alternative binding proteins: anticalins – harnessing the structural plasticity of the lipocalin ligand pocket to engineer novel binding activities. FEBS J. 275, 2677–2683.PubMedCrossRefGoogle Scholar
  100. Steen, N.A., Barker, S.C., Alewood, P.F., 2006. Proteins in the saliva of the ixodida (ticks): pharmacological features and biological significance. Toxicon 47, 1–20.PubMedCrossRefGoogle Scholar
  101. Valenzuela, J.G., Charlab, R., Galperin, M.Y., Ribeiro, J.M., 1998. Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme. J. Biol. Chem. 273, 30583–30590.PubMedCrossRefGoogle Scholar
  102. Valenzuela, J.G., Francischetti, I.M., Ribeiro, J.M., 1999. Purification, cloning, and synthesis of a novel salivary anti-thrombin from the mosquito Anopheles albimanus. Biochemistry 38, 11209–11215.PubMedCrossRefGoogle Scholar
  103. Valenzuela, J.G., Francischetti, I.M., Pham, V.M., Garfield, M.K., Mather, T.N., Ribeiro, J.M., 2002a. Exploring the sialome of the tick Ixodes scapularis. J. Exp. Biol. 205, 2843–2864.PubMedGoogle Scholar
  104. Valenzuela, J.G., Pham, V.M., Garfield, M.K., Francischetti, I.M., Ribeiro, J.M.C., 2002b. Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem. Mol. Biol. 32, 1101–1122.PubMedCrossRefGoogle Scholar
  105. Valenzuela, J.G., Francischetti, I.M., Pham, V.M., Garfield, M.K., Ribeiro, J.M., 2003. Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem. Mol. Biol. 33, 717–732.PubMedCrossRefGoogle Scholar
  106. Valenzuela, J.G., Garfield, M., Rowton, E.D., Pham, V.M., 2004. Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J. Exp. Biol. 207, 3717–3729.PubMedCrossRefGoogle Scholar
  107. Van Den Abbeele, J., Caljon, G., Dierick, J.F., Moens, L., De Ridder, K., Coosemans, M., 2007. The Glossina morsitans tsetse fly saliva: general characteristics and identification of novel salivary proteins. Insect Biochem. Mol. Biol. 37, 1075–1085.CrossRefGoogle Scholar
  108. Vieira, A.T., Fagundes, C.T., Alessandri, A.L., Castor, M.G., Guabiraba, R., Borges, V.O., Silveira, K.D., Vieira, E.L., Goncalves, J.L., Silva, T.A., Deruaz, M., Proudfoot, A.E., Sousa, L.P., Teixeira, M.M., 2009. Treatment with a novel chemokine-binding protein or eosinophil lineage-ablation protects mice from experimental colitis. Am. J. Pathol. 175, 2382–2391.PubMedCrossRefGoogle Scholar
  109. Walter, D.E., Proctor, H.C., 1999. Mites: Ecology, Evolution and Behaviour, first ed. CABI Publishing, Wallingford.Google Scholar
  110. Wang X., Ribeiro J.M.C., Broce A.B., Wilkerson M.J., Kanost M.R., 2009a. An insight into the transcriptome and proteome of the salivary gland of the stable fly, Stomoxys calcitrans. Insect Biochem. Mol. Biol. 39, 607–614.PubMedCrossRefGoogle Scholar
  111. Wang M., Guerrero F.D., Pertea G., Nene V.M., 2009b. Global comparative analysis of ESTs from the southern cattle tick, Rhipicephalus (Boophilus) microplus. BMC Genomics 8, 368.CrossRefGoogle Scholar
  112. Weichsel, A., Maes, E.M., Andersen, J.F., Valenzuela, J.G., Shokhireva, T., Walker, F.A., Montfort, W.R., 2005. Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Proc. Natl. Acad. Sci., U.S.A. 102, 594–599.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Parasites, Vectors and Vector-Borne DiseasesOnderstepoort Veterinary InstitutePretoriaSouth Africa
  2. 2.Department of Veterinary Tropical DiseasesUniversity of PretoriaPretoriaSouth Africa
  3. 3.Section of Vector Biology, Laboratory of Malaria and Vector ResearchNational Institute of Allergy and Infectious Diseases, National Institutes of HealthRockvilleUSA

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