Unravelling the complex venom landscapes of lethal Australian funnel-web spiders (Hexathelidae: Atracinae) using LC-MALDI-TOF mass spectrometry

Journal of Proteomics

Volumn 80, Issue , 2013, Pages 292-310

  Palagi, Alexandre ^a   Koh, Jennifer M S ^b   Leblanc, Mathieu ^a   Wilson, David ^c   Dutertre, Sébastien ^c   King, Glenn F ^c   Nicholson, Graham M ^b   Escoubas, Pierre ^a  

^a VenomeTech   (France)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Atrax species; Hadronyche species; Illawarra wisharti; LC MALDI TOF mass spectrometry; Spider venom; Venom landscapes

Indexed keywords

SPIDER VENOM;

ARACHNID; ARBOREAL SPECIES; ARTICLE; ATRAX ROBUSTUS; FEMALE; HADRONYCHE CERBEREA; HADRONYCHE FORMIDABILIS; HADRONYCHE INFENSA; HADRONYCHE VERSUTA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ILLAWARRA WISHARTI; LIQUID CHROMATOGRAPHY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPIDER;

ANIMALS; ARACHNIDISM; AUSTRALIA; FEMALE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MALE; MOLECULAR WEIGHT; PEPTIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPIDER VENOMS; SPIDERS;

EID: 84874812314     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.01.002     Document Type: Article

References (55)

1. Nicholson G.M., Graudins A., Wilson H.I., Little M., Broady K.W. Arachnid toxinology in Australia: from clinical toxicology to potential applications. Toxicon 2006, 48:872-898.
2. Vetter R.S., Isbister G.K. Medical aspects of spider bites. Annu Rev Entomol 2008, 53:409-429.
3. Isbister G.K., Fan H.W. Spider bite. Lancet 2011, 378:2039-2047.
4. Bosmans F., Escoubas P., Nicholson G.M. Spider venom peptides as leads for drug and insecticide design. Animal Toxins: State of the Art Perspectives In Health and Biotechnology 2009, 269-290. Federal University of Minas Gerais Press, Belo Horizonte. M.E. de Lima, A.M.C. Pimenta, M.-F. Martin-Eauclaire, R.B. Zingali, H. Rochat (Eds.).
5. Estrada G., Villegas E., Corzo G. Spider venoms: a rich source of acylpolyamines and peptides as new leads for CNS drugs. Natural Prod Reports 2007, 24:145-161.
6. Nicholson G.M. Spider peptides. Handbook of biologically active peptides 2013, 461-472. Elsevier, San Diego. 2nd ed. A. Kastin (Ed.).
7. Saez N.J., Senff S., Jensen J.E., Er S.Y., Herzig V., Rash L.D., et al. Spider-venom peptides as therapeutics. Toxins 2010, 2:2851-2871.
8. Windley M.J., Herzig V., Dziemborowicz S.A., Hardy M.C., King G.F., Nicholson G.M. Spider-venom peptides as bioinsecticides. Toxins 2012, 4:191-227.
9. Klint J.K., Senff S., Rupasinghe D.B., Er S.Y., Herzig V., Nicholson G.M., et al. Spider-venom peptides that target voltage-gated sodium channels: pharmacological tools and potential therapeutic leads. Toxicon 2012, 60:478-491.
10. King G.F. Venoms as a platform for human drugs: translating toxins into therapeutics. Expert Opin Biol Ther 2011, 11:1469-1484.
11. Platnick N.I. The world spider catalog, version 13.0 2012, American Museum of Natural History, [Available online: http://research.amnh.org/iz/spiders/catalog (accessed on 19 August 2012)].
12. Coddington J.A., Levi H.W. Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 1991, 22:565-592.
13. Kuhn-Nentwig L., Stöcklin R., Nentwig W. Venom composition and strategies in spiders: is everything possible?. Adv Insect Physiol 2011, 40:1-86.
14. Vassilevski A.A., Kozlov S.A., Grishin E.V. Molecular diversity of spider venom. Biochemistry (Mosc) 2009, 74:1505-1534.
15. Escoubas P., Rash L.D. Tarantulas: eight-legged pharmacists and combinatorial chemists. Toxicon 2004, 43:555-574.
16. King G.F., Hardy M.C. Spider-venom peptides: structure, pharmacology, and potential for control of insect pests. Annu Rev Entomol. 2013, 58:475-496.
17. Sollod B.L., Wilson D., Zhaxybayeva O., Gogarten J.P., Drinkwater R., King G.F. Were arachnids the first to use combinatorial peptide libraries?. Peptides 2005, 26:131-139.
18. Herzig V., Wood D.L.A., Newell F., Chaumeil P.-A., Kaas Q., Binford G.J., et al. ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures. Nucleic Acids Res 2011, 39:D653-D657.
19. Wood D.L., Miljenovic T., Cai S., Raven R.J., Kaas Q., Escoubas P., et al. ArachnoServer: a database of protein toxins from spiders. BMC Genomics 2009, 10:375.
20. Wilson D., Alewood P.F. Taxonomy of Australian Funnel-web spiders using rp-HPLC/ESI-MS profiling techniques. Toxicon 2006, 47:614-627.
21. Escoubas P., Sollod B., King G.F. Venom landscapes: mining the complexity of spider venoms via a combined cDNA and mass spectrometric approach. Toxicon 2006, 47:650-663.
22. +-channels. Eur J Biochem 1999, 264:287-300.
23. Davis J., Jones A., Lewis R. Remarkable inter- and intra-species complexity of conotoxins revealed by LC/MS. Peptides 2009, 30:1222-1227.
24. Escoubas P., Quinton L., Nicholson G.M. Venomics: unravelling the complexity of animal venoms with mass spectrometry. J Mass Spectrom 2008, 43:279-295.
25. Liang S.P. Proteome and peptidome profiling of spider venoms. Expert Rev Proteomics 2008, 5:731-746.
26. Ueberheide B.M., Fenyö D., Alewood P.F., Chait B.T. Rapid sensitive analysis of cysteine rich peptide venom components. Proc Natl Acad Sci U S A 2009, 106:6910-6915.
27. Gray M.R. A revision of the Australian funnel-web spiders (Hexathelidae: Atracinae). Rec Aust Mus 2010, 62:285-392.
28. Isbister G.K., Gray M.R., Balit C.R., Raven R.J., Stokes B.J., Porges K., et al. Funnel-web spider bite: a systematic review of recorded clinical cases. Med J Aust 2005, 182:407-411.
29. Graudins A., Wilson D., Alewood P.F., Broady K.W., Nicholson G.M. Cross-reactivity of Sydney funnel-web spider antivenom: neutralization of the in vitro toxicity of other Australian funnel-web (Atrax and Hadronyche) spider venoms. Toxicon 2002, 40:259-266.
30. Alewood D., Birinyi-Strachan L.C., Pallaghy P.K., Norton R.S., Nicholson G.M., Alewood P.F. Synthesis and characterization of δ-atracotoxin-Ar1a, the lethal neurotoxin from venom of the Sydney funnel-web spider (Atrax robustus). Biochemistry 2003, 42:12933-12940.
31. Wang X.-H., Smith R., Fletcher J.I., Wilson H., Wood C.J., Howden M.E., et al. Structure-function studies of ω-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur J Biochem 1999, 264:488-494.
32. Wilson D., Alewood P. Australian funnel-web spider venom analyzed with on-line RP-HPLC techniques. Methods Mol Biol 2004, 251:307-322.
33. Escoubas P., Célérier M.L., Nakajima T. High-performance liquid chromatography matrix-assisted laser desorption/ionization time-of-flight mass spectrometry peptide fingerprinting of tarantula venoms in the genus Brachypelma: chemotaxonomic and biochemical applications. Rapid Commun Mass Spectrom 1997, 11:1891-1899.
34. Escoubas P., Chamot-Rooke J., Stöcklin R., Whiteley B.J., Corzo G., Genet R., et al. A comparison of matrix-assisted laser desorption/ionization time-of-flight and liquid chromatography electrospray ionization mass spectrometry methods for the analysis of crude tarantula venoms in the Pterinochilus group. Rapid Commun Mass Spectrom 1999, 13:1861-1868.
35. Legros C., Celerier M.L., Henry M., Guette C. Nanospray analysis of the venom of the tarantula Theraphosa leblondi: a powerful method for direct venom mass fingerprinting and toxin sequencing. Rapid Commun Mass Spectrom 2004, 18:1024-1032.
36. Quistad G.B., Skinner W.S. Isolation and sequencing of insecticidal peptides from the primitive hunting spider, Plectreurys tristis (Simon). J Biol Chem 1994, 269:11098-11101.
37. Senko M.W., Beu S.C., McLafferty F.W. Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions. J Am Soc Mass Spectrom 1995, 6:229-233.
38. Wilson DTR. The identification and characterisation of Australian funnel-web spider venom [PhD Thesis]. Brisbane, QLD: The University of Queensland; 2001.
39. Escoubas P., Corzo G., Whiteley B.J., Célérier M.L., Nakajima T. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and high-performance liquid chromatography study of quantitative and qualitative variation in tarantula spider venoms. Rapid Commun Mass Spectrom 2002, 16:403-413.
40. Gray M.R. Aspects of the systematics of the Australian funnel web spiders (Araneae: Hexathelidae: Atracinae) based upon morphological and electrophoretic data. Australian Arachnology: Aust. Entomol. Soc. 1988, 113-125. M.R. Gray, A.D. Austin, N.W. Heather (Eds.).
41. Gray M.R. Distribution of the funnel web spiders. Toxic plants and animals: a guide for Australia 1987, 313-321. Queensland Museum, South Brisbane. J. Covacevich, P. Davie, J. Pearn (Eds.).
42. Vassilevski A.A., Fedorova I.M., Maleeva E.E., Korolkova Y.V., Efimova S.S., Samsonova O.V., et al. Novel class of spider toxin: active principle from the yellow sac spider Cheiracanthium punctorium venom is a unique two-domain polypeptide. J Biol Chem 2010, 285:32293-32302.
43. Graudins A., Little M.J., Pineda S.S., Hains P.G., King G.F., Broady K.W., et al. Cloning and activity of a novel α-latrotoxin from red-back spider venom. Biochem Pharmacol 2012, 83:170-183.
44. Pekár S., Smerda J., Hrušková M., Sedo O., Muster C., Cardoso P., et al. Prey-race drives differentiation of biotypes in ant-eating spiders. J Anim Ecol 2012, 81:838-848.
45. Boevé J.L., Kuhn-Nentwig L., Keller S., Nentwig W. Quantity and quality of venom released by a spider (Cupiennius salei, Ctenidae). Toxicon 1995, 33:1347-1357.
46. Atkinson R.K., Walker P. The effects of season of collection, feeding, maturation and gender on the potency of funnel-web spider (Atrax infensus) venom. Immunol Cell Biol 1985, 63:555-561.
47. Binford G.J. An analysis of geographic and intersexual chemical variation in venoms of the spider Tegenaria agrestis (Agelenidae). Toxicon 2001, 39:955-968.
48. Gonçalves de Andrade R.M., Christina De Oliveira K.C., Giusti A.L., Dias da Silva W., Tambourgi D.V. Ontogenetic development of Loxosceles intermedia spider venom. Toxicon 1999, 37:627-632.
49. Cristina De Oliveira K., Gonçalves de Andrade R.M., Giusti A.L., Dias da Silva W., Tambourgi D.V. Sex-linked variation of Loxosceles intermedia spider venoms. Toxicon 1998, 37:217-221.
50. Herzig V., Khalife A.A., Chong Y., Isbister G.K., Currie B.J., Churchill T.B., et al. Intersexual variations in Northern (Missulena pruinosa) and Eastern (M. bradleyi) mouse spider venom. Toxicon 2008, 51:1167-1177.
51. Sheumack D.D., Baldo B.A., Carroll P.R., Hampson F., Howden M.E., Skorulis A. A comparative study of properties and toxic constituents of funnel web spider (Atrax) venoms. Comp Biochem Physiol 1984, 78C:55-68.
52. Rash L.D., King R.G., Hodgson W.C. Sex differences in the pharmacological activity of venom from the white-tailed spider (Lampona cylindrata). Toxicon 2000, 38:1111-1127.
53. Rash L.D., Birinyi-Strachan L.C., Nicholson G.M., Hodgson W.C. Neurotoxic activity of venom from the Australian eastern mouse spider (Missulena bradleyi) involves modulation of sodium channel gating. Br J Pharmacol 2000, 130:1817-1824.
54. Dauly C., Escoubas P., King G.F., Nicholson G.M. Characterization of spider venom peptides by high-resolution LC-MS/MS analysis. ThermoScientific Application Note 511 2011, [https://staticthermoscientificcom/images/D20650~pdf].
55. Olivera B.M., Cruz L.J. Conotoxins, in retrospect. Toxicon 2001, 39:7-14.