Unique scorpion toxin with a putative ancestral fold provides insight into evolution of the inhibitor cystine knot motif

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 26, 2011, Pages 10478-10483

  Smith, Jennifer J ^a   Hill, Justine M ^a   Little, Michelle J ^b   Nicholson, Graham M ^b   King, Glenn F ^a   Alewood, Paul F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Molecular evolution; NMR; Protein structure

Indexed keywords

INSECTICIDE; PESTICIDE; PROTEIN INHIBITOR; SCORPION VENOM;

AMINO ACID SEQUENCE; ARTICLE; CYSTINE KNOT MOTIF; DISULFIDE BOND; DNA SEQUENCE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; INHIBITOR CYSTINE KNOT; INSECTICIDAL ACTIVITY; LIOCHELES WAIGIENSIS; MOLECULAR EVOLUTION; NONHUMAN; PEPTIDOMICS; POISONOUS SCORPION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN ISOLATION; PROTEIN MOTIF; PROTEIN STRUCTURE; TOXIN ANALYSIS; TOXIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; CYSTINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROTOXINS; PROTEIN CONFORMATION; PROTEIN FOLDING; SCORPION VENOMS; SCORPIONS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ARANEAE; GASTROPODA; HEXAPODA; LIOCHELES WAIGIENSIS; SCORPIONES;

EID: 79960586218     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1103501108     Document Type: Article

References (50)

1. Dunlop JA, Selden PA (2009) Calibrating the chelicerate clock: A paleontological reply to Jeyaprakash and Hoy. Exp Appl Acarol 48:183-197.
2. Rodriguez de la Vega RC, Schwartz EF, Possani LD (2010) Mining on scorpion venom biodiversity. Toxicon 56:1155-1161.
3. Mamelak AN, Jacoby DB (2007) Targeted delivery of antitumoral therapy to glioma and other malignancies with synthetic chlorotoxin (TM-601). Expert Opin Drug Deliv 4:175-186. (Pubitemid 46389915)
4. Zlotkin E, Fishman Y, Elazar M (2000) AaIT: From neurotoxin to insecticide. Biochimie 82:869-881.
5. He QY, et al. (2008) ATDB: A uni-database platform for animal toxins. Nucleic Acids Res 36:D293-D297.
6. +-channels. Toxicon 43:865-875.
7. Chagot B, et al. (2005) An unusual fold for potassium channel blockers: NMR structure of three toxins from the scorpion Opisthacanthus madagascariensis. Biochem J 388:263-271. (Pubitemid 40732954)
8. Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS (1994) A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci 3:1833-1839. (Pubitemid 24356606)
9. King GF, Tedford HW, Maggio F (2002) Structure and function of insecticidal neurotoxins from Australian funnel-web spiders. J Toxicol-Toxin Rev 21:359-389. (Pubitemid 35425080)
10. Craik DJ, Daly NL, Waine C (2001) The cystine knot motif in toxins and implications for drug design. Toxicon 39:43-60.
11. Fry BG, et al. (2009) The toxicogenomic multiverse: Convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10:483-511.
12. Zhu S, Li W, Jiang D, Zeng X (2000) Evidence for the existence of insect defensin-like peptide in scorpion venom. IUBMB Life 50:57-61.
13. Wang X, et al. (2000) Discovery and characterization of a family of insecticidal neurotoxins with a rare vicinal disulfide bridge. Nat Struct Biol 7:505-513. (Pubitemid 30414474)
14. King GF, Gentz MC, Escoubas P, Nicholson GM(2008) A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 52:264-276.
15. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795. (Pubitemid 38829638)
16. Tedford HW, Sollod BL, Maggio F, King GF (2004) Australian funnel-web spiders: Master insecticide chemists. Toxicon 43:601-618. (Pubitemid 38520199)
17. Holm L, Rosenstrom P (2010) Dali server: Conservation mapping in 3D. Nucl Acids Res 38:W545-W549.
18. Sollod BL, et al. (2005)Were arachnids the first to use combinatorial peptide libraries? Peptides 26:131-139.
19. Fletcher JI, et al. (1997) The structure of a novel insecticidal neurotoxin, ω-atracotoxin- HV1, from the venom of an Australian funnel web spider. Nat Struct Biol 4:559-566.
20. Heitz A, Le-Nguyen D, Chiche L (1999) Min-21 and min-23, the smallest peptides that fold like a cystine-stabilized beta-sheet motif: design, solution structure, and thermal stability. Biochemistry 38:10615-10625.
21. Le-Nguyen D, Heitz A, Chiche L, El Hajji M, Castro B (1993) Characterization and 2D NMR study of the stable [9-21, 15-27] 2 disulfide intermediate in the folding of the 3 disulfide trypsin inhibitor EETI II. Protein Sci 2:165-174.
22. Prendini L (2000) Phylogeny and classification of the superfamily Scorpionoidea Latreille 1802 (Chelicerata, Scorpiones): An exemplar approach. Cladistics 16:1-78.
23. Prendini L, Wheeler WC (2005) Scorpion higher phylogeny and classification, taxonomic anarchy, and standards for peer review in online publishing. Cladistics 21:446-494.
24. Fet V, Soleglad ME (2005) Contributions to scorpion systematics. I. On recent changes in high-level taxonomy. Euscorpius 31:1-13.
25. Volschenk ES, Mattoni CI, Prendini L (2008) Comparative anatomy of the mesosomal organs of scorpions (Chelicerata, Scorpiones), with implications for the phylogeny of the order. Zool J Linn Soc 154:651-675.
26. Matsushita N, Miyashita M, Sakai A, Nakagawa Y, Miyagawa H (2007) Purification and characterization of a novel short-chain insecticidal toxin with two disulfide bridges from the venom of the scorpion Liocheles australasiae. Toxicon 50:861-867. (Pubitemid 47445691)
27. Silva EC, et al. (2009) Cloning and characterization of cDNA sequences encoding for new venom peptides of the Brazilian scorpion Opisthacanthus cayaporum. Toxicon 54:252-261.
28. Lazarovici P, Yanai P, Pelhate M, Zlotkin E (1982) Insect toxic component from the venom of a chactoid scorpion, Scorpio maurus palmatus (Scorpionidae). J Biol Chem 257:8397-8404. (Pubitemid 13231338)
29. Yuan W, et al. (2010) Cloning and functional characterization of a new antimicrobial peptide gene StCT1 from the venom of the scorpion Scorpiops tibetanus. Peptides 31:22-26.
30. Zeng XC, et al. (2000) Cloning and characterization of a cDNA sequence encoding the precursor of a chlorotoxin-like peptide from the Chinese scorpion Buthus martensii Karsch. Toxicon 38:1009-1014.
31. + channel-blocking peptides from the Chinese scorpion Buthus martensii Karsch. FEBS Lett 457:509-514.
32. 2+ release in developing skeletal muscle containing ryanodine receptor type 3. Biophys J 82:1319-1328.
33. 2+ release channel/ryanodine receptors. FEBS Lett 469:179-185.
34. 2+ channels. Biochem J 404:89-96.
35. Mosbah A, et al. (2000) A new fold in the scorpion toxin family, associated with an activity on a ryanodine-sensitive calcium channel. Proteins 40:436-442. (Pubitemid 30624451)
36. Boisseau S, et al. (2006) Cell penetration properties of maurocalcine, a natural venom peptide active on the intracellular ryanodine receptor. Biochim Biophys Acta 1758:308-319. (Pubitemid 43732520)
37. Mabrouk K, et al. (2007) Critical amino acid residues of maurocalcine involved in pharmacology, lipid interaction and cell penetration. Biochim Biophys Acta 1768:2528-2540. (Pubitemid 47542314)
38. Lee CW, et al. (2004) Molecular basis of the high-affinity activation of type 1 ryanodine receptors by imperatoxin A. Biochem J 377:385-394. (Pubitemid 38142194)
39. Schnolzer M, Alewood P, Jones A, Alewood D, Kent SB (1992) In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, high yield assembly of difficult sequences. Int J Pept Protein Res 40:180-193.
40. Eitan M, et al. (1990) A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: Purification, primary structure, and mode of action. Biochemistry 29:5941-5947. (Pubitemid 20201396)
41. Wang X, et al. (1999) Structure-function studies of omega-atracotoxin, a potent antagonist of insect voltage-gated calcium channels. Eur J Biochem 264:488-494. (Pubitemid 29424454)
42. Tedford HW, Fletcher JI, King GF (2001) Functional significance of the beta hairpin in the insecticidal neurotoxin ω-atracotoxin-Hv1a. J Biol Chem 276:26568-26576.
43. Gunning SJ, et al. (2008) The Janus-faced atracotoxins are specific blockers of invertebrate K(Ca) channels. FEBS J 275:4045-4059.
44. Bartels C, Xia TH, Billeter M, Güntert P, Wüthrich K (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J Biomol NMR 6:1-10.
45. Güntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278:353-378.
46. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319:209-227. (Pubitemid 34729497)
47. Wüthrich K (1986) NMR of Proteins and Nucleic Acids (John Wiley, New York).
48. Fletcher JI, Chapman BE, Mackay JP, Howden MEH, King GF (1997) The structure of versutoxin (δ-atracotoxin-Hv1) provides insights into the binding of site 3 neurotoxins to the voltage-gated sodium channel. Structure 5:1525-1535. (Pubitemid 27521807)
49. Davis IW, et al. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35:W375-W383.
50. Robson SA, King GF (2006) Domain architecture and structure of the bacterial cell division protein DivIB. Proc Natl Acad Sci USA 103:6700-6705.