1932

Abstract

Throughout evolution, numerous proteins have been convergently recruited into the venoms of various animals, including centipedes, cephalopods, cone snails, fish, insects (several independent venom systems), platypus, scorpions, shrews, spiders, toxicoferan reptiles (lizards and snakes), and sea anemones. The protein scaffolds utilized convergently have included AVIT/colipase/prokineticin, CAP, chitinase, cystatin, defensins, hyaluronidase, Kunitz, lectin, lipocalin, natriuretic peptide, peptidase S1, phospholipase A, sphingomyelinase D, and SPRY. Many of these same venom protein types have also been convergently recruited for use in the hematophagous gland secretions of invertebrates (e.g., fleas, leeches, kissing bugs, mosquitoes, and ticks) and vertebrates (e.g., vampire bats). Here, we discuss a number of overarching structural, functional, and evolutionary generalities of the protein families from which these toxins have been frequently recruited and propose a revised and expanded working definition for venom. Given the large number of striking similarities between the protein compositions of conventional venoms and hematophagous secretions, we argue that the latter should also fall under the same definition.

Keyword(s): convergenceevolutionphylogenytoxin
Loading

Article metrics loading...

/content/journals/10.1146/annurev.genom.9.081307.164356
2009-09-22
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/genom/10/1/annurev.genom.9.081307.164356.html?itemId=/content/journals/10.1146/annurev.genom.9.081307.164356&mimeType=html&fmt=ahah

Literature Cited

  1. Abdel-Mottaleb Y, Corzo G, Martin-Eauclaire MF, Satake H, Ceard B. 1.  et al. 2008. A common “hot spot” confers hERG blockade activity to α-scorpion toxins affecting K+ channels. Biochem. Pharmacol. 76:805–15 [Google Scholar]
  2. Alape-Giron A, Persson B, Cederlund E, Flores-Diaz M, Gutierrez JM. 2.  et al. 1999. Elapid venom toxins: multiple recruitments of ancient scaffolds. Eur. J. Biochem. 259:225–34 [Google Scholar]
  3. Amarant T, Burkhart W, Levine H, Arochapinango CL, Parikh I. 3.  1991. Isolation and complete amino-acid-sequence of 2 fibrinolytic proteinases from the toxic saturnid caterpillar Lonomia achelous. Biochim. Biophys. Acta 1079:214–21 [Google Scholar]
  4. Ameri M, Wang X, Wilkerson MJ, Kanost MR, Broce AB. 4.  2008. An immunoglobulin binding protein (Antigen 5) of the stable fly (Diptera: Muscidae) salivary gland stimulates bovine immune responses. J. Med. Entomol. 45:94–101 [Google Scholar]
  5. Andersen JF, Champagne DE, Weichsel A, Ribeiro JMC, Balfour CA. 5.  et al. 1997. Nitric oxide binding and crystallization of recombinant nitrophorin I, a nitric oxide transport protein from the blood-sucking bug Rhodnius prolixus. Biochemistry 36:4423–28 [Google Scholar]
  6. Andersen JF, Francischetti IMB, Valenzuela JG, Schuck P, Ribeiro JMC. 6.  2003. Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect. J. Biol. Chem. 278:4611–17 [Google Scholar]
  7. Andersen JF, Gudderra NP, Francischetti IMB, Ribeiro JMC. 7.  2005. The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch. Insect Biochem. Physiol. 58:97–105 [Google Scholar]
  8. Andersen JF, Gudderra NP, Francischetti IMB, Valenzuela JG, Ribeiro JMC. 8.  2004. Recognition of anionic phospholipid membranes by an antihemostatic protein from a blood-feeding insect. Biochemistry 43:6987–94 [Google Scholar]
  9. Andersen JF, Hinnebusch BJ, Lucas DA, Conrads TP, Veenstra TD. 9.  et al. 2007. An insight into the sialome of the oriental rat flea, Xenopsylla cheopis (Rots). BMC Genomics 8:102 [Google Scholar]
  10. Antuch W, Berndt KD, Chavez MA, Delfin J, Wuthrich K. 10.  1993. The NMR solution structure of a kunitz-type proteinase-inhibitor from the sea-anemone Stichodactyla helianthus. Eur. J. Biochem. 212:675–84 [Google Scholar]
  11. Arca B, Lombardo F, Francischetti IMB, Pham VM, Mestres-Simon M. 11.  et al. 2007. An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem. Mol. Biol. 37:107–27 [Google Scholar]
  12. Arca B, Lombardo F, Valenzuela JG, Francischetti IMB, Marinotti O. 12.  et al. 2005. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J. Exp. Biol. 208:3971–86 [Google Scholar]
  13. Asgari S, Zhang GM, Zareie R, Schmidt O. 13.  2003. A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. Insect Biochem. Mol. Biol. 33:1017–24 [Google Scholar]
  14. Assumpcao TCF, Francischetti IMB, Andersen JF, Schwarz A, Santana JM, Ribeiro JMC. 14.  2008. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas’ disease. Insect Biochem. Mol. Biol. 38:213–32 [Google Scholar]
  15. Batista CVF, Roman-Gonzalez SA, Salas-Castillo SP, Zamudio FZ, Gomez-Lagunas F, Possani LD. 15.  2007. Proteomic analysis of the venom from the scorpion Tityus stigmurus: biochemical and physiological comparison with other Tityus species. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 146:147–57 [Google Scholar]
  16. Bayrhuber M, Vijayan V, Ferber M, Graf R, Korukottu J. 16.  et al. 2005. Conkunitzin-S1 is the first member of a new Kunitz-type neurotoxin family: structural and functional characterization. J. Biol. Chem. 280:23766–70 [Google Scholar]
  17. Beress L. 17.  1982. Biologically-active compounds from coelenterates. Pure Appl. Chem. 54:1981–94 [Google Scholar]
  18. Binford GJ, Cordes MHJ, Wells MA. 18.  2005. Sphingomyelinase D from venoms of Loxosceles spiders: evolutionary insights from cDNA sequences and gene structure. Toxicon 45:547–60 [Google Scholar]
  19. Binford GJ, Wells MA. 19.  2003. The phylogenetic distribution of sphingomyelinase D activity in venoms of Haplogyne spiders. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 135:25–33 [Google Scholar]
  20. Birkemo GA, Luders T, Andersen O, Nes IF, Nissen-Meyer J. 20.  2003. Hipposin, a histone-derived antimicrobial peptide in Atlantic halibut (Hippoglossus hippoglossus L.). Biochim. Biophys. Acta-Proteins Proteomics 1646:207–15 [Google Scholar]
  21. Boisbouvier J, Albrand JP, Blackledge M, Jaquinod M, Schweitz H. 21.  et al. 1998. A structural homologue of colipase in black mamba venom revealed by NMR floating disulphide bridge analysis. J. Mol. Biol. 283:205–19 [Google Scholar]
  22. Bradley KN. 22.  2000. Muscarinic toxins from the green mamba. Pharmacol. Ther. 85:87–109 [Google Scholar]
  23. Brown RL, Haley TL, West KA, Crabb JW. 23.  1999. Pseudechetoxin: a peptide blocker of cyclic nucleotide-gated ion channels. Proc. Natl. Acad. Sci. USA 96:754–59 [Google Scholar]
  24. Brown RL, Lynch LL, Haley TL, Arsanjani R. 24.  2003. Pseudechetoxin binds to the pore turret of cyclic nucleotide-gated ion channels. J. Gen. Physiol. 122:749–60 [Google Scholar]
  25. Campbell CL, Vandyke KA, Letchworth GJ, Drolet BS, Hanekamp T, Wilson WC. 25.  2005. Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol. Biol. 14:121–36 [Google Scholar]
  26. Campbell CL, Wilson WC, Manninen K. 26.  2005. Characterization of differentially expressed midge genes in orbivirus vector populations. Am. J. Trop. Med. Hyg. 73:144 [Google Scholar]
  27. Champagne DE, Nussenzveig RH, Ribeiro JMC. 27.  1995. Purification, partial characterization, and cloning of nitric oxide-carrying heme-proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus. J. Biol. Chem. 270:8691–95 [Google Scholar]
  28. Charlab R, Valenzuela JG, Rowton ED, Ribeiro JMC. 28.  1999. Toward an understanding of the biochemical and pharmacological complexity of the saliva of a hematophagous sand fly Lutzomyia longipalpis. Proc. Natl. Acad. Sci. USA 96:15155–60 [Google Scholar]
  29. Chen DS, Kini RM, Yuen R, Khoo HE. 29.  1997. Haemolytic activity of stonustoxin from stonefish (Synanceja horrida) venom: pore formation and the role of cationic amino acid residues. Biochem. J. 325:685–91 [Google Scholar]
  30. Chen TB, Farragher S, Bjourson AJ, Orr DF, Rao P, Shaw C. 30.  2003. Granular gland transcriptomes in stimulated amphibian skin secretions. Biochem. J. 371:125–30 [Google Scholar]
  31. Chen TB, Xue YZ, Zhou M, Shaw C. 31.  2005. Molecular cloning of mRNA from toad granular gland secretion and lyophilized skin: identification of Bo8—a novel prokineticin from Bombina orientalis. Peptides 26:377–83 [Google Scholar]
  32. Cordes MHJ, Binford GJ. 32.  2006. Lateral gene transfer of a dermonecrotic toxin between spiders and bacteria. Bioinformatics 22:264–68 [Google Scholar]
  33. Dauplais M, Gilquin B, Possani LD, GurrolaBriones G, Roumestand C, Menez A. 33.  1995. Determination of the three-dimensional solution structure of noxiustoxin: analysis of structural differences with related short-chain scorpion toxins. Biochemistry 34:16563–73 [Google Scholar]
  34. Dauplais M, Lecoq A, Song JX, Cotton J, Jamin N. 34.  et al. 1997. On the convergent evolution of animal toxins: conservation of a diad of functional residues in potassium channel-blocking toxins with unrelated structures. J. Biol. Chem. 272:4302–9 [Google Scholar]
  35. Davidson FF, Dennis EA. 35.  1990. Evolutionary relationships and implications for the regulation of phospholipase A2 from snake venom to human secreted forms. J. Mol. Evol. 31:228–38 [Google Scholar]
  36. De La Vega RCR. 36.  2005. A note on the evolution of spider toxins containing the ICK-motif. Toxin Rev. 24:385–97 [Google Scholar]
  37. de la Vega RCR, Garcia BI, D'Ambrosio C, Diego-Garcia E, Scaloni A, Possani LD. 37.  2004. Antimicrobial peptide induction in the haemolymph of the Mexican scorpion Centruroides limpidus limpidus in response to septic injury. Cell. Mol. Life Sci. 61:1507–19 [Google Scholar]
  38. de la Vega RCR, Merino E, Becerril B, Possani LD. 38.  2003. Novel interactions between K+ channels and scorpion toxins. Trends Pharmacol. Sci. 24:222–27 [Google Scholar]
  39. de la Vega RCR, Possani LD. 39.  2005. On the evolution of invertebrate defensins. Trends Genet. 21:330–32 [Google Scholar]
  40. de la Vega RCR, Possani LD. 40.  2007. Novel paradigms on scorpion toxins that affects the activating mechanism of sodium channels. Toxicon 49:171–80 [Google Scholar]
  41. de Plater GM, Martin RL, Milburn PJ. 41.  1998. A C-type natriuretic peptide from the venom of the platypus (Ornithorhynchus anatinus): structure and pharmacology. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 120:99–110 [Google Scholar]
  42. de Weille JR, Schweitz H, Maes P, Tartar A, Lazdunski M. 42.  1991. Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the L-type calcium channel. Proc. Natl. Acad. Sci. USA 88:2437–40 [Google Scholar]
  43. Diego-Garcia E, Abdel-Mottaleb Y, Schwartz EF, de la Vega RCR, Tytgat J, Possani LD. 43.  2008. Cytolytic and K+ channel blocking activities of β-KTx and scorpine-like peptides purified from scorpion venoms. Cell. Mol. Life Sci. 65:187–200 [Google Scholar]
  44. Dryer SE, Chiappinelli VA. 44.  1983. Kappa-bungarotoxin: an intracellular study demonstrating blockade of neuronal nicotinic receptors by a snake neurotoxin. Brain Res. 289:317–21 [Google Scholar]
  45. Dubin G. 45.  2005. Proteinaceous cysteine protease inhibitors. Cell. Mol. Life Sci. 62:653–69 [Google Scholar]
  46. Ehret-Sabatier L, Loew D, Goyffon M, Fehlbaum P, Hoffmann JA. 46.  et al. 1996. Characterization of novel cysteine-rich antimicrobial peptides from scorpion blood. J. Biol. Chem. 271:29537–44 [Google Scholar]
  47. Fang KSY, Vitale M, Fehlner P, King TP. 47.  1988. cDNA cloning and primary structure of a white-face hornet venom allergen, antigen 5. Proc. Natl. Acad. Sci. USA 85:895–99 [Google Scholar]
  48. Filippovich I, Sorokina N, Masci PP, de Jersey J, Whitaker AN. 48.  et al. 2002. A family of textilinin genes, two of which encode proteins with antihaemorrhagic properties. Br. J. Haematol. 119:376–84 [Google Scholar]
  49. Fox JW, Serrano SMT. 49.  2008. Exploring snake venom proteomes: multifaceted analyses for complex toxin mixtures. Proteomics 8:909–20 [Google Scholar]
  50. Francischetti IMB, Andersen JF, Ribeiro JMC. 50.  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 41:3810–18 [Google Scholar]
  51. Francischetti IMB, Ribeiro JMC, Champagne D, Andersen J. 51.  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. 275:12639–50 [Google Scholar]
  52. Francischetti IMB, Valenzuela JG, Andersen JF, Mather TN, Ribeiro JMC. 52.  2002. 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 99:3602–12 [Google Scholar]
  53. Froy O, Gurevitz M. 53.  1998. Membrane potential modulators: a thread of scarlet from plants to humans. FASEB J. 12:1793–96 [Google Scholar]
  54. Fry BG. 54.  2005. From genome to “venome”: molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res. 15:403–20 [Google Scholar]
  55. Fry BG, Scheib H, Van Der Weerd L, Young B, McNaughtan J. 55.  et al. 2008. Evolution of an arsenal. Mol. Cell. Proteomics 7:215–46 [Google Scholar]
  56. Fry BG, Vidal N, Norman JA, Vonk FJ, Scheib H. 56.  et al. 2006. Early evolution of the venom system in lizards and snakes. Nature 439:584–88 [Google Scholar]
  57. Fry BG, Wickramaratana JC, Lemme S, Beuve A, Garbers D. 57.  et al. 2005. Novel natriuretic peptides from the venom of the inland taipan (Oxyuranus microlepidotus): isolation, chemical and biological characterisation. Biochem. Biophys. Res. Commun. 327:1011–15 [Google Scholar]
  58. Fry BG, Wuster W. 58.  2004. Assembling an arsenal: origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences. Mol. Biol. Evol. 21:870–83 [Google Scholar]
  59. Fry BG, Wuster W, Kini RM, Brusic V, Khan A. 59.  et al. 2003. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J. Mol. Evol. 57:110–29 [Google Scholar]
  60. Gasparini S, Gilquin B, Menez A. 60.  2004. Comparison of sea anemone and scorpion toxins binding to KV1 channels: an example of convergent evolution. Toxicon 43:901–8 [Google Scholar]
  61. Gmachl M, Kreil G. 61.  1993. Bee venom hyaluronidase is homologous to a membrane-protein of mammalian sperm. Proc. Natl. Acad. Sci. USA 90:3569–73 [Google Scholar]
  62. Gracy J, Le-Nguyen D, Gelly JC, Kaas Q, Heitz A, Chiche L. 62.  2008. KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007. Nucleic Acids Res. 36:D314–19 [Google Scholar]
  63. Grunclova L, Horn M, Vancova M, Sojka D, Franta Z. 63.  et al. 2006. Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity. Biol. Chem. 387:1635–44 [Google Scholar]
  64. Gudderra NP, Ribeiro JMC, Andersen JF. 64.  2005. Structural determinants of factor IX(a) binding in nitrophorin 2, a lipocalin inhibitor of the intrinsic coagulation pathway. J. Biol. Chem. 280:25022–28 [Google Scholar]
  65. Harrison RA, Ibison F, Wilbraham D, Wagstaff SC. 65.  2007. Identification of cDNAs encoding viper venom hyaluronidases: cross-generic sequence conservation of full-length and unusually short variant transcripts. Gene 392:22–33 [Google Scholar]
  66. Harvey AL, Robertson B. 66.  2004. Dendrotoxins: structure-activity relationships and effects on potassium ion channels. Curr. Med. Chem. 11:3065–72 [Google Scholar]
  67. Hawdon JM, Jones BF, Hoffman DR, Hotez PJ. 67.  1996. Cloning and characterization of Ancylostoma secreted protein: a novel protein associated with the transition to parasitism by infective hookworm larvae. J. Biol. Chem. 271:6672–78 [Google Scholar]
  68. Hisada M, Satake H, Masuda K, Aoyama M, Murata K. 68.  et al. 2005. Molecular components and toxicity of the venom of the solitary wasp, Anoplius samariensis. Biochem. Biophys. Res. Commun. 330:1048–54 [Google Scholar]
  69. Honma T, Shiomi K. 69.  2006. Peptide toxins in sea anemones: structural and functional aspects. Mar. Biotechnol. 8:1–10 [Google Scholar]
  70. Huang LF, Zheng HB, Xu Y, Song HT, Yu CX. 70.  2008. A snake venom phospholipase A(2) with high affinity for muscarinic acetylcholine receptors acts on guinea pig ileum. Toxicon 51:1008–16 [Google Scholar]
  71. Ibanez-Tallon I, Miwa JM, Wang HL, Adams NC, Crabtree GW. 71.  et al. 2002. Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron 33:893–903 [Google Scholar]
  72. Inceoglu B, Lango J, Jing J, Chen LL, Doymaz F. 72.  et al. 2003. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc. Natl. Acad. Sci. USA 100:922–27 [Google Scholar]
  73. Ito N, Mita M, Takahashi Y, Matsushima A, Watanabe YG. 73.  et al. 2007. Novel cysteine-rich secretory protein in the buccal gland secretion of the parasitic lamprey, Lethehteron japonicum. Biochem. Biophys. Res. Commun. 358:35–40 [Google Scholar]
  74. Kamiguti AS, Zuzel M, Theakston RDG. 74.  1998. Snake venom metalloproteinases and disintegrins: interactions with cells. Braz. J. Med. Biol. Res. 31:853–62 [Google Scholar]
  75. Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG. 75.  et al. 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 [Google Scholar]
  76. Kim HS, Park CB, Kim MS, Kim SC. 76.  1996. cDNA cloning and characterization of buforin I, an antimicrobial peptide: a cleavage product of histone H2A. Biochem. Biophys. Res. Commun. 229:381–87 [Google Scholar]
  77. King TP, Lu G, Gonzalez M, Qian NF, Soldatova L. 77.  1996. Yellow jacket venom allergens, hyaluronidase and phospholipase: sequence similarity and antigenic cross-reactivity with their hornet and wasp homologs and possible implications for clinical allergy. J. Allergy Clin. Immunol. 98:588–600 [Google Scholar]
  78. Kini RM. 78.  2003. Excitement ahead: structure, function and mechanism of snake venom phospholipase A2 enzymes. Toxicon 42:827–40 [Google Scholar]
  79. Kita M, Nakamura Y, Okumura Y, Ohdachi SD, Oba Y. 79.  et al. 2004. Blarina toxin, a mammalian lethal venom from the short-tailed shrew Blarina brevicauda: isolation and characterization. Proc. Natl. Acad. Sci. USA 101:7542–47 [Google Scholar]
  80. Kita M, Okumura Y, Ohdachi SD, Oba Y, Yoshikuni M. 80.  et al. 2005. Purification and characterisation of blarinasin, a new tissue kallikrein-like protease from the short-tailed shrew Blarina brevicauda: comparative studies with blarina toxin. Biol. Chem. 386:177–82 [Google Scholar]
  81. Kordis D, Gubenek F. 81.  2000. Adaptive evolution of animal toxin multigene families. Gene 261:43–52 [Google Scholar]
  82. Kratzschmar J, Haendler B, Langer G, Boidol W, Bringmann P. 82.  et al. 1991. The plasminogen activator family from the salivary-gland of the vampire bat Desmodus rotundus: cloning and expression. Gene 105:229–37 [Google Scholar]
  83. Krezel AM, Ulmer JS, Wagner G, Lazarus RA. 83.  2000. Recombinant decorsin: dynamics of the RGD recognition site. Protein Sci. 9:1428–38 [Google Scholar]
  84. Krishnan A, Nair PN, Jones D. 84.  1994. Isolation, cloning, and characterization of new chitinase stored in active form in chitin-lined venom reservoir. J. Biol. Chem. 269:20971–76 [Google Scholar]
  85. Lewis RJ. 85.  2004. Conotoxins as selective inhibitors of neuronal ion channels, receptors and transporters. IUBMB Life 56:89–93 [Google Scholar]
  86. Li S, Kwon J, Aksoy S. 86.  2001. Characterization of genes expressed in the salivary glands of the tsetse fly, Glossina morsitans morsitans. Insect Mol. Biol. 10:69–76 [Google Scholar]
  87. Liang SP. 87.  2004. An overview of peptide toxins from the venom of the Chinese bird spider Selenocosmia huwena Wang [=Ornithoctonus huwena (Wang)]. Toxicon 43:575–85 [Google Scholar]
  88. Low KSY, Gwee MCE, Yuen R, Gopalakrishnakone P, Khoo HE. 88.  1994. Stonustoxin: effects on neuromuscular function in vitro and in vivo. Toxicon 32:573–81 [Google Scholar]
  89. Magalhaes GS, Junqueira-de-Azevedo ILM, Lopes-Ferreira M, Lorenzini DM, Ho PL, Moura-da-Silva AM. 89.  2006. Transcriptome analysis of expressed sequence tags from the venom glands of the fish Thalassophryne nattereri. Biochimie 88:693–99 [Google Scholar]
  90. Mans BJ, Andersen JF, Francischetti IMB, Valenzuel JG, Schwan TG. 90.  et al. 2008. Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem. Mol. Biol. 38:42–58 [Google Scholar]
  91. Mans BJ, Andersen JF, Schwan TG, Ribeiro JMC. 91.  2008. Characterization of anti-hemostatic factors in the argasid, Argas monolakensis: implications for the evolution of blood-feeding in the soft tick family. Insect Biochem. Mol. Biol. 38:22–41 [Google Scholar]
  92. Mans BJ, Louw AI, Neitz AWH. 92.  2002. Savignygrin, a platelet aggregation inhibitor from the soft tick Ornithodoros savignyi, presents the RGD integrin recognition motif on the Kunitz-BPTI fold. J. Biol. Chem. 277:21371–78 [Google Scholar]
  93. Mans BJ, Louw AI, Neitz AWH. 93.  2003. The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the tick lipocalin family: implications for the origins of tick toxicoses. Mol. Biol. Evol. 20:1158–67 [Google Scholar]
  94. 94.  Deleted in proof
  95. Mans BJ, Ribeiro JMC. 95.  2008. A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem. Mol. Biol. 38:862–70 [Google Scholar]
  96. Mans BJ, Ribeiro JMC. 96.  2008. Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem. Mol. Biol. 38:841–52 [Google Scholar]
  97. Mans BJ, Ribeiro JMC, Andersen JF. 97.  2008. Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J. Biol. Chem. 283:18721–33 [Google Scholar]
  98. McDowell RS, Dennis MS, Louie A, Shuster M, Mulkerrin MG, Lazarus RA. 98.  1992. Mambin, a potent glycoprotein-IIb-IIIa antagonist and platelet-aggregation inhibitor structurally related to the short neurotoxins. Biochemistry 31:4766–72 [Google Scholar]
  99. Menendez A, Finlay BB. 99.  2007. Defensins in the immunology of bacterial infections. Curr. Opin. Immunol. 19:385–91 [Google Scholar]
  100. Milne TJ, Abbenante G, Tyndall JDA, Halliday J, Lewis RJ. 100.  2003. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily. J. Biol. Chem. 278:31105–10 [Google Scholar]
  101. Minagawa S, Ishida M, Shimakura K, Nagashima Y, Shiomi K. 101.  1997. Isolation and amino acid sequences of two Kunitz-type protease inhibitors from the sea anemone Anthopleura aff. xanthogrammica. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 118:381–86 [Google Scholar]
  102. Mollay C, Wechselberger C, Mignogna G, Negri L, Melchiorri P. 102.  et al. 1999. Bv8, a small protein from frog skin and its homologue from snake venom induce hyperalgesia in rats. Eur. J. Pharmacol. 374:189–96 [Google Scholar]
  103. Morita A, Isawa H, Orito Y, Iwanaga S, Chinzei Y, Yuda M. 103.  2006. Identification and characterization of a collagen-induced platelet aggregation inhibitor, triplatin, from salivary glands of the assassin bug, Triatoma infestans. FEBS J. 273:2955–62 [Google Scholar]
  104. Morita T. 104.  2005. Structures and functions of snake venom CLPs (C-type lectin-like proteins) with anticoagulant-, procoagulant-, and platelet-modulating activities. Toxicon 45:1099–114 [Google Scholar]
  105. Morrissette J, Kratzschmar J, Haendler B, Elhayek R, Mochcamorales J. 105.  et al. 1995. Primary structure and properties of helothermine, a peptide toxin that blocks ryanodine receptors. Biophys. J. 68:2280–88 [Google Scholar]
  106. Mouhat S, Jouirou B, Mosbah A, De Waard M, Sabatier JM. 106.  2004. Diversity of folds in animal toxins acting on ion channels. Biochem. J. 378:717–26 [Google Scholar]
  107. Nagaraju S, Devaraja S, Kemparaju K. 107.  2007. Purification and properties of hyaluronidase from Hippasa partita (funnel web spider) venom gland extract. Toxicon 50:383–93 [Google Scholar]
  108. Negri L, Lattanzi R, Giannini E, Melchiorri P. 108.  2007. Bv8/prokineticin proteins and their receptors. Life Sci. 81:1103–16 [Google Scholar]
  109. Nevalainen TJ. 109.  2008. Phospholipases A2 in the genome of the sea anemone Nematostella vectensis. Comp. Biochem. Physiol. D-Genomics Proteomics 3:226–33 [Google Scholar]
  110. Ng HC, Ranganathan S, Chua KL, Khoo HE. 110.  2005. Cloning and molecular characterization of the first aquatic hyaluronidase, SFHYA1, from the venom of stonefish (Synanceja horrida). Gene 346:71–81 [Google Scholar]
  111. Nicholson GM. 111.  2007. Insect-selective spider toxins targeting voltage-gated sodium-channels. Toxicon 49:490–512 [Google Scholar]
  112. Nobile M, Magnelli V, Lagostena L, Mochcamorales J, Possani LD, Prestipino G. 112.  1994. The toxin helothermine affects potassium currents in newborn rat cerebellar granule cells. J. Membr. Biol. 139:49–55 [Google Scholar]
  113. Nobile M, Noceti F, Prestipino G, Possani LD. 113.  1996. Helothermine, a lizard venom toxin, inhibits calcium current in cerebellar granules. Exp. Brain Res. 110:15–20 [Google Scholar]
  114. Noeske-Jungblut C, Haendler B, Donner P, Alagon A, Possani L, Schleuning WD. 114.  1995. Triabin, a highly potent exosite inhibitor of thrombin. J. Biol. Chem. 270:28629–34 [Google Scholar]
  115. Noeske-Jungblut C, Kratzschmar J, Haendler B, Alagon A, Possani L. 115.  et al. 1994. An inhibitor of collagen-induced platelet-aggregation from the saliva of Triatoma pallidipennis. J. Biol. Chem. 269:5050–53 [Google Scholar]
  116. Nunn MA, Sharma A, Paesen GC, Adamson S, Lissina O. 116.  et al. 2005. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J. Immunol. 174:2084–91 [Google Scholar]
  117. Olivera BM, Teichert RW. 117.  2007. Diversity of the neurotoxic Conus peptides: a model for concerted pharmacological discovery. Mol. Interv. 7:251–60 [Google Scholar]
  118. Paesen GA, Adams PL, Nuttall PA, Stuart DL. 118.  2000. Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochim. Biophys. Acta-Protein Struct. Mol. Enzymol. 1482:92–101 [Google Scholar]
  119. Paesen GC, Adams PL, Harlos K, Nuttall PA, Stuart DI. 119.  1999. Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol. Cell 3:661–71 [Google Scholar]
  120. Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS. 120.  1994. A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci. 3:1833–39 [Google Scholar]
  121. Park IY, Park CB, Kim MS, Kim SC. 121.  1998. Parasin I, an antimicrobial peptide derived from histone H2A in the catfish, Parasilurus asotus. FEBS Lett. 437:258–62 [Google Scholar]
  122. Patthy L. 122.  2003. Modular assembly of genes and the evolution of new functions. Genetica 118:217–31 [Google Scholar]
  123. Possani LD, Becerril B, Delepierre M, Tytgat J. 123.  1999. Scorpion toxins specific for Na+-channels. Eur. J. Biochem. 264:287–300 [Google Scholar]
  124. Possani LD, Merino E, Corona M, Bolivar F, Becerril B. 124.  2000. Peptides and genes coding for scorpion toxins that affect ion-channels. Biochimie 82:861–68 [Google Scholar]
  125. Pung YF, Wong PTH, Kumar PP, Hodgson WC, Kini RM. 125.  2005. Ohanin, a novel protein from king cobra venom, induces hypolocomotion and hyperalgesia in mice. J. Biol. Chem. 280:13137–47 [Google Scholar]
  126. Pungercar J, Krizaj I. 126.  2007. Understanding the molecular mechanism underlying the presynaptic toxicity of secreted phospholipases A2. Toxicon 50:871–92 [Google Scholar]
  127. Reis CV, Andrade SA, Ramos OHP, Ramos CRR, Ho PL. 127.  et al. 2006. Lopap, a prothrombin activator from Lonomia obliqua belonging to the lipocalin family: recombinant production, biochemical characterization and structure-function insights. Biochem. J. 398:295–302 [Google Scholar]
  128. Ribeiro JMC, Alarcon-Chaidez F, Francischetti IMB, Mans BJ, Mather TN. 128.  et al. 2006. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol. 36:111–29 [Google Scholar]
  129. Ribeiro JMC, Andersen J, Silva-Neto MAC, Pham VM, Garfield MK, Valenzuela JG. 129.  2004. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem. Mol. Biol. 34:61–79 [Google Scholar]
  130. Ribeiro JMC, Arca B, Lombardo F, Calvo E, Phan VM. 130.  et al. 2007. An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8:6 [Google Scholar]
  131. Ribeiro JMC, Charlab R, Pham VM, Garfield M, Valenzuela JG. 131.  2004. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem. Mol. Biol. 34:543–63 [Google Scholar]
  132. Ribeiro JMC, Schneider M, Guimaraes JA. 132.  1995. Purification and characterization of prolixin-S (nitrophorin 2), the salivary anticoagulant of the bloodsucking bug Rhodnius prolixus. Biochem. J. 308:243–49 [Google Scholar]
  133. Ribeiro JMC, Walker FA. 133.  1994. High-affinity histamine-binding and antihistaminic activity of the salivary nitric oxide-carrying heme protein (nitrophorin) of Rhodnius prolixus. J. Exp. Med. 180:2251–57 [Google Scholar]
  134. Ricci-Silva ME, Valente RH, Leon IR, Tambourgi DV, Ramos OHP. 134.  et al. 2008. Immunochemical and proteomic technologies as tools for unravelling toxins involved in envenoming by accidental contact with Lonomia obliqua caterpillars. Toxicon 51:1017–28 [Google Scholar]
  135. Sangamnatdej S, Paesen GC, Slovak M, Nuttall PA. 135.  2002. A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Mol. Biol. 11:79–86 [Google Scholar]
  136. Santos A, Ribeiro JMC, Lehane MJ, Gontijo NF, Veloso AB. 136.  et al. 2007. The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae). Insect Biochem. Mol. Biol. 37:702–12 [Google Scholar]
  137. Schaloske RH, Dennis EA. 137.  2006. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta-Mol. Cell Biol. Lipids 1761:1246–59 [Google Scholar]
  138. Schleuning WD, Alagon A, Boidol W, Bringmann P, Petri T. 138.  et al. 1992. Plasminogen activators from the saliva of Desmodus rotundus (common vampire bat): unique fibrin specificity. Ann. N. Y. Acad. Sci. 667:395–403 [Google Scholar]
  139. Schwartz EF, Diego-Garcia E, de la Vega RCR, Possani LD. 139.  2007. Transcriptome analysis of the venom gland of the Mexican scorpion Hadrurus gertschi (Arachnida: Scorpiones). BMC Genomics 8:116 [Google Scholar]
  140. Schweitz H, Bruhn T, Guillemare E, Moinier D, Lancelin JM. 140.  et al. 1995. Kalicludines and kaliseptine: Two different classes of sea-anemone toxins for voltage-sensitive K+ channels. J. Biol. Chem. 270:25121–26 [Google Scholar]
  141. Schweitz H, Heurteaux C, Bois P, Moinier D, Romey G, Lazdunski M. 141.  1994. Calcicludine, a venom peptide of the kunitz-type protease inhibitor family, is a potent blocker of high-threshold Ca2+ channels with a high-affinity for L-type channels in cerebellar granule neurons. Proc. Natl. Acad. Sci. USA 91:878–82 [Google Scholar]
  142. Schweitz H, Pacaud P, Diochot S, Moinier D, Lazdunski M. 142.  1999. MIT1, a black mamba toxin with a new and highly potent activity on intestinal contraction. FEBS Lett. 461:183–88 [Google Scholar]
  143. Soares MR, Oliveira-Carvalho AL, Wermelinger LS, Zingali RB, Ho PL. 143.  et al. 2005. Identification of novel bradykinin-potentiating peptides and C-type natriuretic peptide from Lachesis muta venom. Toxicon 46:31–38 [Google Scholar]
  144. Sollod BL, Wilson D, Zhaxybayeva O, Gogarten JP, Drinkwater R, King GF. 144.  2005. Were arachnids the first to use combinatorial peptide libraries?. Peptides 26:131–39 [Google Scholar]
  145. Stone BF. 145.  1988. Tick paralysis, particularly involving Ixodes holocyclus and other Ixodes species. Advances in Disease Vector Research KF Harris 561–85 New York: Springer-Verlag [Google Scholar]
  146. Sung JML, Low KSY, Khoo HE. 146.  2002. Characterization of the mechanism underlying stonustoxin-mediated relaxant response in the rat aorta in vitro. Biochem. Pharmacol. 63:1113–18 [Google Scholar]
  147. Sutherland S, Lane WR. 147.  1969. Toxins and mode of envenomation of common ringed or blue-banded octopus. Med. J. Aust. 1:893–97 [Google Scholar]
  148. Szeto TH, Wang XH, Smith R, Connor M, Christie MJ. 148.  et al. 2000. Isolation of a funnel-web spider polypeptide with homology to mamba intestinal toxin 1 and the embryonic head inducer Dickkopf-1. Toxicon 38:429–42 [Google Scholar]
  149. Tamiya T, Fujimi TJ. 149.  2006. Molecular evolution of toxin genes in Elapidae snakes. Mol. Divers. 10:529–43 [Google Scholar]
  150. Todd SM, Sonenshine DE, Hynes WL. 150.  2007. Tissue and life-stage distribution of a defensin gene in the Lone Star tick, Amblyomma americanum. Med. Vet. Entomol. 21:141–47 [Google Scholar]
  151. Torres AM, Kuchel PW. 151.  2004. The β-defensin-fold family of polypeptides. Toxicon 44:581–88 [Google Scholar]
  152. Torres AM, Wang XH, Fletcher JI, Alewood D, Alewood PF. 152.  et al. 1999. Solution structure of a defensin-like peptide from platypus venom. Biochem. J. 341:785–94 [Google Scholar]
  153. Tu AT, Hendon RR. 153.  1983. Characterization of lizard venom hyaluronidase and evidence for its action as a spreading factor. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 76:377–83 [Google Scholar]
  154. Valenzuela JG, Garfield M, Rowton ED, Pham VM. 154.  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. 207:3717–29 [Google Scholar]
  155. Veiga ABG, Ribeiro JMC, Guimaraes JA, Francischetti IMB. 155.  2005. A catalog for the transcripts from the venomous structures of the caterpillar Lonomia obliqua: identification of the proteins potentially involved in the coagulation disorder and hemorrhagic syndrome. Gene 355:11–27 [Google Scholar]
  156. Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MAG. 156.  et al. 2008. Evolutionary origin and development of snake fangs. Nature 454:630–33 [Google Scholar]
  157. Wagstaff SC, Favreau P, Cheneval O, Laing GD, Wilkinson MC. 157.  et al. 2008. Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem. Biophys. Res. Commun. 365:650–56 [Google Scholar]
  158. Wang J, Shen B, Guo M, Lou XH, Duan YY. 158.  et al. 2005. Blocking effect and crystal structure of natrin toxin, a cysteine-rich secretory protein from Naja atra venom that targets the BKCa channel. Biochemistry 44:10145–52 [Google Scholar]
  159. Wang XH, Connor M, Smith R, Maciejewski MW, Howden MEH. 159.  et al. 2000. Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge. Nat. Struct. Biol. 7:505–13 [Google Scholar]
  160. Waxman L, Connolly TM. 160.  1993. Isolation of an inhibitor selective for collagen-stimulated platelet-aggregation from the soft tick Ornithodoros moubata. J. Biol. Chem. 268:5445–49 [Google Scholar]
  161. Wei AZ, Alexander RS, Duke J, Ross H, Rosenfeld SA, Chang CH. 161.  1998. Unexpected binding mode of tick anticoagulant peptide complexed to bovine factor Xa. J. Mol. Biol. 283:147–54 [Google Scholar]
  162. Wen SP, Wilson DTR, Kuruppu S, Korsinczky MLJ, Hedrick J. 162.  et al. 2005. Discovery of an MIT-like atracotoxin family: spider venom peptides that share sequence homology but not pharmacological properties with AVIT family proteins. Peptides 26:2412–26 [Google Scholar]
  163. Wilczynski AM, Joseph CG, Haskell-Luevano C. 163.  2005. Current trends in the structure activity relationship studies of the endogenous agouti-related protein (AGRP) melanocortin receptor antagonist. Med. Res. Rev. 25:545–56 [Google Scholar]
  164. Wong JH, Xia LX, Ng TB. 164.  2007. A review of defensins of diverse origins. Curr. Protein Pept. Sci. 8:446–59 [Google Scholar]
  165. Xu XQ, Yang HL, Ma DY, Wu J, Wang YP. 165.  et al. 2008. 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 7:582–90 [Google Scholar]
  166. Xu Y, Bruno JF, Luft BJ. 166.  2005. Identification of novel tick salivary gland proteins for vaccine development. Biochem. Biophys. Res. Commun. 326:901–4 [Google Scholar]
  167. Yamazaki Y, Brown RL, Morita T. 167.  2002. Purification and cloning of toxins from elapid venoms that target cyclic nucleotide-gated ion channels. Biochemistry 41:11331–37 [Google Scholar]
  168. Yamazaki Y, Koike H, Sugiyama Y, Motoyoshi K, Wada T. 168.  et al. 2002. Cloning and characterization of novel snake venom proteins that block smooth muscle contraction. Eur. J. Biochem. 269:2708–15 [Google Scholar]
  169. Yasuda O, Morimoto S, Chen YH, Jiang BB, Kimura T. 169.  et al. 1993. Calciseptine binding to a 1,4-dihydropyridine recognition site of the L-type calcium-channel of rat synaptosomal membranes. Biochem. Biophys. Res. Commun. 194:587–94 [Google Scholar]
  170. Yuan CH, He QY, Peng K, Diao JB, Jiang LP. 170.  et al. 2008. Discovery of a distinct superfamily of k-type toxin (KTT) from tarantulas. PLoS ONE 3:e3414 [Google Scholar]
  171. Zasloff M. 171.  2002. Antimicrobial peptides of multicellular organisms. Nature 415:389–95 [Google Scholar]
  172. Zhou J, Liao M, Ueda M, Gong H, Xuan X, Fujisaki K. 172.  2007. Sequence characterization and expression patterns of two defensin-like antimicrobial peptides from the tick Haemaphysalis longicornis. Peptides 28:1304–10 [Google Scholar]
  173. Zhou JL, Ueda M, Umemiya R, Battsetseg B, Boldbaatar D. 173.  et al. 2006. A secreted cystatin from the tick Haemaphysalis longicornis and its distinct expression patterns in relation to innate immunity. Insect Biochem. Mol. Biol. 36:527–35 [Google Scholar]
  174. Zhu S, Gao B, Tytgat J. 174.  2005. Phylogenetic distribution, functional epitopes and evolution of the CSαβ superfamily. Cell. Mol. Life Sci. 62:2257–69 [Google Scholar]
  175. Zhu SY. 175.  2008. Discovery of six families of fungal defensin-like peptides provides insights into origin and evolution of the CSαβ defensins. Mol. Immunol. 45:828–38 [Google Scholar]
  176. Zhu SY, Darbon H, Dyason K, Verdonck F, Tytgat J. 176.  2003. Evolutionary origin of inhibitor cystine knot peptides. FASEB J. 17:1765–67 [Google Scholar]
/content/journals/10.1146/annurev.genom.9.081307.164356
Loading
/content/journals/10.1146/annurev.genom.9.081307.164356
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error