Aphicidal efficacy of scorpion- and spider-derived neurotoxins

Toxicon

Volumn 70, Issue , 2013, Pages 114-122

  Pal, Narinder ^a   Yamamoto, Takashi ^b   King, Glenn F ^c   Waine, Clement ^b,d   Bonning, Bryony ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b DuPont Electronic Technologies   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d NiuGenie Biotechnology   (Papua New Guinea)

Author keywords

Agatoxin IVA; Grammotoxin SIA; Hexatoxin Hv1a; hexatoxin Hv1a; Acyrthosiphon pisum; Aphid; Charybdotoxin; Chlorotoxin; Leiurus quinquestriatus hebraeus insect toxin; Maurotoxin; Melanization; Neurotoxin; Paralysis

Indexed keywords

BACTERIAL TOXIN; CHARYBDOTOXIN; CHLOROTOXIN; CYT1AA TOXIN; HEBRAEUS ALPHA INSECT TOXIN; MAUROTOXIN; NEUROTOXIN; OMEGA AGATOXIN IVA; OMEGA HEXATOXIN HV1A; OMEGA THERAPHOTOXIN GR1A; SCORPION VENOM; SPIDER VENOM; UNCLASSIFIED DRUG;

ARTICLE; BIOASSAY; CHEMICAL PEST CONTROL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; INSECTICIDAL ACTIVITY; LD 50; MYZUS PERSICAE; NONHUMAN; PEA APHID; PRIORITY JOURNAL; TOXIN ANALYSIS;

ANIMALS; APHIDS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BIOLOGICAL CONTROL AGENTS; CALCIUM CHANNELS; CHARYBDOTOXIN; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECT CONTROL; LETHAL DOSE 50; NEUROTOXINS; POTASSIUM CHANNELS; SCORPION VENOMS; SCORPIONS; SODIUM CHANNELS; SPIDER VENOMS; SPIDERS;

EID: 84878180392     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2013.04.015     Document Type: Article

References (87)

1. Adams M.E. Agatoxins: ion channel specific toxins from the American funnel web spider, Agelenopsis aperta. Toxicon 2004, 43:509-525.
2. Atkinson R.K., Vonarx E.J., Howden M.E.H. Effects of whole venom and venom fractions from several Australian spiders, including Atrax (Hadronyche) species, when injected into insects. Comp. Biochem. Phys. C 1996, 114:113-117.
3. Avdonin V., Nolan B., Sabatier J.M., De Waard M., Hoshi T. Mechanisms of maurotoxin action on Shaker potassium channels. Biophys. J. 2000, 79:776-787.
4. Benkhalifa R., Lapied B., Kharrat R., Ayeb M.E., Pelhate M. Paradoxical maurotoxin activity on insect nervous system. Toxicon 1998, 36:1731.
5. 2+ currents in embryonic cockroach brain neurons. J. Neurophysiol. 1999, 82:2284-2293.
6. Bhatia V., Uniyal P.L., Bhattacharya R. Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities. Biotechnol. Adv. 2011, 29:879-888.
7. Bickmeyer U., Rossler W., Wiegand H. ω-AGA toxin IVA blocks high-voltage-activated calcium channel currents in cultured pars intercerebralis neurosecretory cells of adult Locusta migratoria. Neurosci. Lett. 1994, 181:113-116.
8. Bloomquist J.R. Mode of action of atracotoxin at central and peripheral synapses of insects. Invertebr. Neurosci. 2003, 5:45-50.
9. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
10. Chong Y., Hayes J.L., Sollod B., Wen S., Wilson D.T., Hains P.G., Hodgson W.C., Broady K.W., King G.F., Nicholson G.M. The ω-atracotoxins: selective blockers of insect M-LVA and HVA calcium channels. Biochem. Pharmacol. 2007, 74:623-638.
11. Chougule N.P., Bonning B.C. Toxins for transgenic resistance to hemipteran pests. Toxins 2012, 4:405-429.
12. Christou P., Capell T., Kohli A., Gatehouse J.A., Gatehouse A.M. Recent developments and future prospects in insect pest control in transgenic crops. Trends Plant Sci. 2006, 11:302-308.
13. Costechareyre D., Balmand S., Condemine G., Rahbe Y. Dickeya dadantii, a plant pathogenic bacterium producing Cyt-like entomotoxins, causes septicemia in the pea aphid Acyrthosiphon pisum. PLoS One 2012, 7:e30702.
14. Dahlman D.L., Rana R.L., Schepers E.J., Schepers T., DiLuna F.A., Webb B.A. A teratocyte gene from a parasitic wasp that is associated with inhibition of insect growth and development inhibits host protein synthesis. Insect Mol. Biol. 2003, 12:527-534.
15. DeBin J.A., Maggio J.E., Strichartz G.R. Purification and characterization of chlorotoxin, a chloride channel ligand from the venom of the scorpion. Am. J. Physiol. 1993, 264:C361-C369.
16. Devonshire A.L. Resistance of aphids to insecticides. Aphids, Their Biology, Natural Enemies and Control 1989, 123-139. Elsevier, Amsterdam. A.K. Minks, P. Harrewijn (Eds.).
17. Diaz-Montano J., Reese J.C., Schapaugh W.T., Campbell L.R. Characterization of antibiosis and antixenosis to the soybean aphid (Hemiptera: Aphididae) in several soybean genotypes. J. Econ. Entomol. 2006, 99:1884-1889.
18. Down R.E., Fitches E.C., Wiles D.P., Corti P., Bell H.A., Gatehouse J.A., Edwards J.P. Insecticidal spider venom toxin fused to snowdrop lectin is toxic to the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae) and the rice brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Pest Manag. Sci. 2006, 62:77-85.
19. Eitan M., Fowler E., Herrmann R., Duval A., Pelhate M., Zlotkin E. A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action. Biochem 1990, 29:5941-5947.
20. Emden H.v., Harrington R. Aphids as Crop Pests 2007, 717. CABI Publishing, London.
21. Febvay G., Delobel B., Rahbe Y. Influence of the amino-acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera, Aphididae). Can. J. Zool. 1988, 66:2449-2453.
22. Fitches E., Audsley N., Gatehouse J.A., Edwards J.P. Fusion proteins containing neuropeptides as novel insect control agents: snowdrop lectin delivers fused allatostatin to insect haemolymph following oral ingestion. Insect Biochem. Mol. Biol. 2002, 32:1653-1661.
23. Fitches E.C., Bell H.A., Powell M.E., Back E., Sargiotti C., Weaver R.J., Gatehouse J.A. Insecticidal activity of scorpion toxin (ButaIT) and snowdrop lectin (GNA) containing fusion proteins towards pest species of different orders. Pest Manag. Sci. 2010, 66:74-83.
24. Fitches E.C., Pyati P., King G.F., Gatehouse J.A. Fusion to snowdrop lectin magnifies the oral activity of insecticidal ω-Hexatoxin-Hv1a peptide by enabling its delivery to the central nervous system. PLoS One 2012, 7:e39389.
25. Fletcher J.I., Smith R., O'Donoghue S.I., Nilges M., Connor M., Howden M.E., Christie M.J., King G.F. The structure of a novel insecticidal neurotoxin, ω-atracotoxin-HV1, from the venom of an Australian funnel web spider. Nat. Struct. Biol. 1997, 4:559-566.
26. Froy O., Zilberberg N., Chejanovsky N., Anglister J., Loret E. Scorpion neurotoxins: structure/function relationships and application in agriculture. Pest Manag. Sci. 2000, 56:472-474.
27. Garcia J., Nakai J., Imoto K., Beam K.G. Role of S4 segments and the leucine heptad motif in the activation of an L-type calcium channel. Biophys. J. 1997, 72:2515-2523.
28. Garcia M.L., Knaus H.G., Munujos P., Slaughter R.S., Kaczorowski G.J. Charybdotoxin and its effects on potassium channels. Am. J. Physiol. 1995, 269:C1-C10.
29. Gatehouse J.A. Biotechnological prospects for engineering insect-resistant plants. Plant Physiol. 2008, 146:881-887.
30. Gentz M.C., Murdoch G., King G.F. Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biol. Control 2010, 52(3):208-215.
31. Gordon D., Karbat I., Ilan N., Cohen L., Kahn R., Gilles N., Dong K., Stuhmer W., Tytgat J., Gurevitz M. The differential preference of scorpion α-toxins for insect or mammalian sodium channels: implications for improved insect control. Toxicon 2007, 49:452-472.
32. Gordon D., MartinEauclaire M.F., Cestele S., Kopeyan C., Carlier E., BenKhalifa R., Pelhate M., Rochat H. Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J. Biol. Chem. 1996, 271:8034-8045.
33. Grenier A.M., Duport G., Pages S., Condemine G., Rahbe Y. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl. Environ. Microbiol. 2006, 72:1956-1965.
34. Herzig V., Wood D.L., Newell F., Chaumeil P.A., Kaas Q., Binford G.J., Nicholson G.M., Gorse D., King G.F. ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures. Nucleic Acids Res. 2011, 39:D653-D657.
35. Hesler L.S., Dashiell K.E., Lundgren J.G. Characterization of resistance to Aphis glycines in soybean accessions. Euphytica 2007, 154:91-99.
36. Hill C.B., Li Y., Hartman G.L. Resistance to the soybean aphid in soybean germplasm. Crop Sci. 2004, 44:98-106.
37. Huys I., Waelkens E., Tytgat J. Structure-function study of a chlorotoxin-chimer and its activity on Kv1.3 channels. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2004, 803:67-73.
38. Inceoglu A.B., Kamita S.G., Hammock B.D. Genetically modified baculoviruses: a historical overview and future outlook. Adv. Virus. Res. 2006, 68:323-360.
39. Jeffers L.A., Michael Roe R. The movement of proteins across the insect and tick digestive system. J. Insect Physiol. 2008, 54:319-332.
40. Jungo F., Bougueleret L., Xenarios I., Poux S. The UniProtKB/Swiss-Prot Tox-Prot program: a central hub of integrated venom protein data. Toxicon 2012, 60:551-557.
41. Kamita S.G., Kang K.-D., Hammock B.D., Inceoglu A.B. Genetically modified baculoviruses for pest insect control. Comprehensive Molecular Insect Science 2005, 271-322. Elsevier, Oxford, UK. L.I. Gilbert, K. Iatrou, S.S. Gill (Eds.).
42. Kanost M.R., Jiang H., Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 2004, 198:97-105.
43. Karbat I., Frolow F., Froy O., Gilles N., Cohen L., Turkov M., Gordon D., Gurevitz M. Molecular basis of the high insecticidal potency of scorpion α-toxins. J. Biol. Chem. 2004, 279:31679-31686.
44. Khan S.A., Zafar Y., Briddon R.W., Malik K.A., Mukhtar Z. Spider venom toxin protects plants from insect attack. Transgenic Res. 2006, 15:349-357.
45. Kim C.S., Schaible G.D., Garrett L., Lubowski R.N., Lee D.J. Economic impacts of the U.S. soybean aphid infestation: a multi-regional competitive dynamic analysis. Agric. Resour. Econ. Rev. 2008, 37:227-242.
46. King G.F. Modulation of insect Ca(v) channels by peptidic spider toxins. Toxicon 2007, 49:513-530.
47. King G.F., Escoubas P., Nicholson G.M. Peptide toxins that selectively target insect Na(V) and Ca(V) channels. Channels (Austin) 2008, 2:100-116.
48. King G.F., Gentz M.C., Escoubas P., Nicholson G.M. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 2008, 52:264-276.
49. Lampe R.A., Defeo P.A., Davison M.D., Young J., Herman J.L., Spreen R.C., Horn M.B., Mangano T.J., Keith R.A. Isolation and pharmacological characterization of ω-grammotoxin SIA, a novel peptide inhibitor of neuronal voltage-sensitive calcium channel responses. Molec. Pharmacol. 1993, 44:451-460.
50. Lee D., Adams M.E. Sodium channels in central neurons of the tobacco budworm, Heliothis virescens: basic properties and modification by scorpion toxins. J. Insect Physiol. 2000, 46:499-508.
51. Lee D., Park Y., Brown T.M., Adams M.E. Altered properties of neuronal sodium channels associated with genetic resistance to pyrethroids. Molec. Pharmacol. 1999, 55:584-593.
52. LeOra-Software POLO-PC, a User's Guide to Probit and Logit Analysis 1987, LeOra Software, Berkeley, California.
53. Li H., Chougule N.P., Bonning B.C. Interaction of the Bacillus thuringiensis delta endotoxins Cry1Ac and Cry3Aa with the gut of thepea aphid, Acyrthosiphon pisum (Harris). J. Invertebr. Pathol. 2011, 107:69-78.
54. Li Y., Hill C.B., Carlson S.R., Diers B.W., Hartman G.L. Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Mol. Breed. 2007, 19:25-34.
55. + channels. J. Biol. Chem. 2003, 278:31095-31104.
56. Maiti I.B., Oey N., Dahlman D.L., Webb B.A. Antibiosis-type resistance in transgenic plants expressing a teratocyte secretory peptide (TSP) gene from a hymenopteran endoparasite (Microplitis croceipes). Plant Biotech. J. 2003, 1:209-219.
57. Miles P.W. Specific responses and damage caused by Aphidoidea. Aphids. Their Biology, Natural Enemies and Control 1989, 23-47. Elsevier, Amsterdam. A.K. Minks, P. Harrewijn (Eds.).
58. Miller, W.A., Bonning, B.C., 2007. Plant Resistance to Insect Pests Mediated by Viral Proteins. U.S. Patent 7,312,080.
59. Moran Y., Gordon D., Gurevitz M. Sea anemone toxins affecting voltage-gated sodium channels - molecular and evolutionary features. Toxicon 2009, 54:1089-1101.
60. Mukherjee A.K., Sollod B.L., Wikel S.K., King G.F. Orally active acaricidal peptide toxins from spider venom. Toxicon 2006, 47:182-187.
61. Nicholson G.M. Insect-selective spider toxins targeting voltage-gated sodium channels. Toxicon 2007, 49:490-512.
62. Perez C., Fernandez L.E., Sun J., Folch J.L., Gill S.S., Soberon M., Bravo A. Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18303-18308.
63. Pham Trung N., Fitches E., Gatehouse J.A. A fusion protein containing a lepidopteran-specific toxin from the South Indian red scorpion (Mesobuthus tamulus) and snowdrop lectin shows oral toxicity to target insects. BMC Biotechnol. 2006, 6:18.
64. Porcar M., Grenier A.M., Federici B., Rahbe Y. Effects of Bacillus thuringiensis delta-endotoxins on the pea aphid, Acyrthosiphon pisum. Appl. Environ. Microbiol. 2009, 75:4897-4900.
65. Possani L.D., Merino E., Corona M., Bolivar F., Becerril B. Peptides and genes coding for scorpion toxins that affect ion-channels. Biochimie 2000, 82:861-868.
66. Pray C.E., Huang J., Hu R., Rozelle S. Five years of Bt cotton in China - the benefits continue. Plant J. 2002, 31:423-430.
67. 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.
68. Ragsdale D.W., Landis D.A., Brodeur J., Heimpel G.E., Desneux N. Ecology and management of the soybean aphid in North America. Annu. Rev. Entomol. 2011, 56:375-399.
69. Russell R.M., Robertson J.L., Savin N.E. POLO: a new computer program for probit analysis. Bull. Entomol. Soc. Am. 1977, 23:209-213.
70. Saez N.J., Senff S., Jensen J.E., Er S.Y., Herzig V., Rash L.D., King G.F. Spider-venom peptides as therapeutics. Toxins 2010, 2:2851-2871.
71. Sanahuja G., Banakar R., Twyman R.M., Capell T., Christou P. Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotech. J. 2011, 9:283-300.
72. Soberon M., Fernandez L.E., Perez C., Gill S.S., Bravo A. Mode of action of mosquitocidal Bacillus thuringiensis toxins. Toxicon 2007, 49:597-600.
73. St Leger R.J., Wang C. Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl. Microbiol. Biotechnol. 2010, 85:901-907.
74. Sylvester E.S. Viruses transmitted by aphids. Aphids. Their Biology, Natural Enemies and Control 1989, 65-88. Elsevier, Amsterdam. A.K. Minks, P. Harrewijn (Eds.).
75. 2+ channel. J. Molec. Biol. 2002, 321:517-526.
76. Tedford H.W., Fletcher J.I., King G.F. Functional significance of the β-hairpin in the insecticidal neurotoxin ω-atracotoxin-Hv1a. J. Biol. Chem. 2001, 276:26568-26576.
77. Tedford H.W., Sollod B.L., Maggio F., King G.F. Australian funnel-web spiders: master insecticide chemists. Toxicon 2004, 43:601-618.
78. Toenniessen G.H., O'Toole J.C., DeVries J. Advances in plant biotechnology and its adoption in developing countries. Curr. Opin. Plant Biol. 2003, 6:191-198.
79. Tomalski M.D., Bruce W.A., Travis J., Blum M.S. Preliminary characterization of toxins from the straw itch mite, Pyemotes tritici,which induce paralysis in the larvae of a moth. Toxicon 1988, 26:127-132.
80. Ullrich N., Gillespie G.Y., Sontheimer H. Human astrocytoma cells express a unique chloride current. Neuroreport 1995, 7:343-347.
81. Valdivia H.H., Possani L.D. Peptide toxins as probes of ryanodine receptor structure and function. Trends Cardiovasc. Med. 1998, 8:111-118.
82. Wang C., Leger R.J.S. Expressing a scorpion neurotoxin makes a fungus hyperinfectious to insects. Nat. Biotechnol. 2007, 25:1455-1456.
83. Wang X., Smith R., Fletcher J.I., Wilson H., Wood C.J., Howden M.E., King G.F. Structure-function studies of ω-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur. J. Biochem. 1999, 264:488-494.
84. Wang X.H., Connor M., Wilson D., Wilson H.I., Nicholson G.M., Smith R., Shaw D., Mackay J.P., Alewood P.F., Christie M.J., King G.F. Discovery and structure of a potent and highly specific blocker of insect calcium channels. J. Biol. Chem. 2001, 276:40306-40312.
85. 2+ currents in central insect neurons: electrophysiological and pharmacological properties. J. Neurophysiol. 1997, 77:186-199.
86. 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.
87. Yamamoto C., Sawada S., Ohno-Shosaku T. Suppression of hippocampal synaptic transmission by the spider toxin ω-agatoxin-IV-A. Brain Res. 1994, 634:349-352.