A Novel Inhibitor of α9α10 Nicotinic Acetylcholine Receptors from Conus vexillum Delineates a New Conotoxin Superfamily

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Luo, Sulan ^a   Christensen, Sean ^b   Zhangsun, Dongting ^a   Wu, Yong ^a   Hu, Yuanyan ^a   Zhu, Xiaopeng ^a   Chhabra, Sandeep ^c   Norton, Raymond S ^c   McIntosh, J Michael ^b  

^a HAINAN UNIVERSITY   (China)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA A CONOTOXIN OIVB; ALPHA B CONOTOXIN VXXXIVA; ALPHA C CONOTOXIN PRXA; ALPHA CONOTOXIN AULB; ALPHA D CONOTOXIN VXXIIA; ALPHA S CONOTOXIN RVIIIA; ALPHA9ALPHA10 NICOTINIC ACETYLCHOLINE RECEPTOR; CONOTOXIN; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; PSI CONOTOXIN PIIIE; TOXIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL TISSUE; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; CONTROLLED STUDY; CONUS VEXILLUM; DNA SEQUENCE; DRUG MECHANISM; DRUG STRUCTURE; IC 50; MOLECULAR CLONING; MOLLUSC; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; SEQUENCE ANALYSIS;

ACETYLCHOLINE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CIRCULAR DICHROISM; CONOTOXINS; CONUS SNAIL; DNA, COMPLEMENTARY; EVOKED POTENTIALS; MOLECULAR SEQUENCE DATA; NICOTINIC ANTAGONISTS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; PEPTIDES; PROTEIN FOLDING; RECEPTORS, NICOTINIC;

EID: 84873868949     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054648     Document Type: Article

References (68)

1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW, (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89: 73-120.
2. Espiritu DJ, Watkins M, Dia-Monje V, Cartier GE, Cruz LJ, et al. (2001) Venomous cone snails: molecular phylogeny and the generation of toxin diversity. Toxicon 39: 1899-1916.
3. Norton RS, Olivera BM, (2006) Conotoxins down under. Toxicon 48: 780-798.
4. Daly NL, Craik DJ, (2009) Structural studies of conotoxins. IUBMB Life 61: 144-150.
5. Olivera BM, (2006) Conus peptides: biodiversity-based discovery and exogenomics. J Biol Chem 281: 31173-31177.
6. Armishaw CJ, Alewood PF, (2005) Conotoxins as research tools and drug leads. Curr Protein Pept Sci 6: 221-240.
7. Kaas Q, Yu R, Jin AH, Dutertre S, Craik DJ, (2012) ConoServer: updated content, knowledge, and discovery tools in the conopeptide database. Nucleic Acids Res 40: D325-330.
8. Ye M, Khoo KK, Xu S, Zhou M, Boonyalai N, et al. (2012) A helical conotoxin from Conus imperialis has a novel cysteine framework and defines a new superfamily. J Biol Chem 287: 14973-14983.
9. Plazas PV, Katz E, Gomez-Casati ME, Bouzat C, Elgoyhen AB, (2005) Stoichiometry of the alpha9alpha10 nicotinic cholinergic receptor. J Neurosci 25: 10905-10912.
10. McIntosh JM, Absalom N, Chebib M, Elgoyhen AB, Vincler M, (2009) Alpha9 nicotinic acetylcholine receptors and the treatment of pain. Biochem Pharmacol 78: 693-702.
11. Quan Y, Luo S, Lin Q, Zhangsun D, Zhang B, (2005) Conotoxin RNA isolation and its cDNA synthesis. Chin J Mar Drugs 24: 1-5.
12. Duckert P, Brunak S, Blom N, (2004) Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 17: 107-112.
13. Dowell C, Olivera BM, Garrett JE, Staheli ST, Watkins M, et al. (2003) Alpha-conotoxin PIA is selective for alpha6 subunit-containing nicotinic acetylcholine receptors. J Neurosci 23: 8445-8452.
14. Cartier GE, Yoshikami D, Gray WR, Luo S, Olivera BM, et al. (1996) A new alpha-conotoxin which targets alpha3beta2 nicotinic acetylcholine receptors. J Biol Chem 271: 7522-7528.
15. Hwang TL, Shaka AJ, (1995) Water suppression that works-excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J Magn Reson 112: 275-279.
16. Sreerama N, Woody RW, (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287: 252-260.
17. Zhangsun D, Luo S, Wu Y, Zhu X, Hu Y, et al. (2006) Novel O-superfamily conotoxins identified by cDNA cloning from three vermivorous Conus species. Chem Biol Drug Des 68: 256-265.
18. Kaas Q, Westermann JC, Halai R, Wang CK, Craik DJ, (2008) ConoServer, a database for conopeptide sequences and structures. Bioinformatics 24: 445-446.
19. Corzo G, Escoubas P, Villegas E, Barnham KJ, He W, et al. (2001) Characterization of unique amphipathic antimicrobial peptides from venom of the scorpion Pandinus imperator. Biochem J 359: 35-45.
20. Santos AD, McIntosh JM, Hillyard DR, Cruz LJ, Olivera BM, (2004) The A-superfamily of conotoxins: structural and functional divergence. J Biol Chem 279: 17596-17606.
21. Han TS, Teichert RW, Olivera BM, Bulaj G, (2008) Conus venoms- a rich source of peptide-based therapeutics. Curr Pharm Des 14: 2462-2479.
22. Hidaka Y, Ohno M, Hemmasi B, Hill O, Forssmann WG, et al. (1998) In vitro disulfide-coupled folding of guanylyl cyclase-activating peptide and its precursor protein. Biochemistry 37: 8498-8507.
23. Woodward SR, Cruz LJ, Olivera BM, Hillyard DR, (1990) Constant and hypervariable regions in conotoxin propeptides. EMBO J 9: 1015-1020.
24. Price-Carter M, Gray WR, Goldenberg DP, (1996) Folding of omega-conotoxins. 1. Efficient disulfide-coupled folding of mature sequences in vitro. Biochemistry 35: 15537-15546.
25. Buczek O, Olivera BM, Bulaj G, (2004) Propeptide does not act as an intramolecular chaperone but facilitates protein disulfide isomerase-assisted folding of a conotoxin precursor. Biochemistry 43: 1093-1101.
26. Conticello SG, Kowalsman ND, Jacobsen C, Yudkovsky G, Sato K, et al. (2003) The prodomain of a secreted hydrophobic mini-protein facilitates its export from the endoplasmic reticulum by hitchhiking on sorting receptors. J Biol Chem 278: 26311-26314.
27. Vincler M, Wittenauer S, Parker R, Ellison M, Olivera BM, et al. (2006) Molecular mechanism for analgesia involving specific antagonism of alpha9alpha10 nicotinic acetylcholine receptors. Proc Natl Acad Sci U S A 103: 17880-17884.
28. Clark RJ, Fischer H, Nevin ST, Adams DJ, Craik DJ, (2006) The synthesis, structural characterization, and receptor specificity of the alpha-conotoxin Vc1.1. J Biol Chem 281: 23254-23263.
29. Callaghan B, Haythornthwaite A, Berecki G, Clark RJ, Craik DJ, et al. (2008) Analgesic alpha-conotoxins Vc1.1 and Rg1A inhibit N-type calcium channels in rat sensory neurons via GABAB receptor activation. J Neurosci 28: 10943-10951.
30. Favreau P, Benoit E, Hocking HG, Carlier L, D' Hoedt D, et al. (2012) A novel μ-conopeptide, CnIIIC, exerts potent and preferential inhibition of Nav1.2/1.4 channels and blocks neuronal nicotinic acetylcholine receptors. Br J Pharmacol 166: 1654-68.
31. Imperial JS, Bansal PS, Alewood PF, Daly NL, Craik DJ, et al. (2006) A novel conotoxin inhibitor of Kv1.6 channel and nAChR subtypes defines a new superfamily of conotoxins. Biochemistry 45: 8331-8340.
32. Franchini LF, Elgoyhen AB, (2006) Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Mol Phylogenet Evol 41: 622-635.
33. Satkunanathan N, Livett B, Gayler K, Sandall D, Down J, et al. (2005) Alpha-conotoxin Vc1.1 alleviates neuropathic pain and accelerates functional recovery of injured neurones. Brain Res 1059: 149-158.
34. Klimis H, Adams DJ, Callaghan B, Nevin S, Alewood PF, et al. (2011) A novel mechanism of inhibition of high-voltage activated calcium channels by alpha-conotoxins contributes to relief of nerve injury-induced neuropathic pain. Pain 152: 259-266.
35. Holtman JR, Dwoskin LP, Dowell C, Wala EP, Zhang Z, et al. (2011) The novel small molecule alpha9alpha10 nicotinic acetylcholine receptor antagonist ZZ-204G is analgesic. Eur J Pharmacol 670: 500-508.
36. Zheng G, Zhang Z, Dowell C, Wala E, Dwoskin LP, et al. (2011) Discovery of non-peptide, small molecule antagonists of alpha9alpha10 nicotinic acetylcholine receptors as novel analgesics for the treatment of neuropathic and tonic inflammatory pain. Bioorg Med Chem Lett 21: 2476-2479.
37. Chernyavsky AI, Arredondo J, Vetter DE, Grando SA, (2007) Central role of alpha9 acetylcholine receptor in coordinating keratinocyte adhesion and motility at the initiation of epithelialization. Exp Cell Res 313: 3542-3555.
38. Lee CH, Huang CS, Chen CS, Tu SH, Wang YJ, et al. (2010) Overexpression and activation of the alpha9-nicotinic receptor during tumorigenesis in human breast epithelial cells. J Natl Cancer Inst 102: 1322-1335.
39. Chen CS, Lee CH, Hsieh CD, Ho CT, Pan MH, et al. (2011) Nicotine-induced human breast cancer cell proliferation attenuated by garcinol through down-regulation of the nicotinic receptor and cyclin D3 proteins. Breast Cancer Res Treat 125: 73-87.
40. Chikova A, Grando SA, (2011) Naturally occurring variants of human Alpha9 nicotinic receptor differentially affect bronchial cell proliferation and transformation. PLoS One 6: e27978.
41. Dutton JL, Bansal PS, Hogg RC, Adams DJ, Alewood PF, et al. (2002) A new level of conotoxin diversity, a non-native disulfide bond connectivity in alpha-conotoxin AuIB reduces structural definition but increases biological activity. J Biol Chem 277: 48849-48857.
42. Tietze AA, Tietze D, Ohlenschlager O, Leipold E, Ullrich F, et al. (2012) Structurally diverse mu-conotoxin PIIIA isomers block sodium channel NaV 1.4. Angew Chem Int Ed Engl 51: 4058-4061.
43. Dyson HJ, (2011) Expanding the proteome: disordered and alternatively folded proteins. Q Rev Biophys 44: 467-518.
44. Wright PE, Dyson HJ, (2009) Linking folding and binding. Curr Opin Struct Biol 19: 31-38.
45. Nemecz A, Taylor P, (2011) Creating an alpha7 nicotinic acetylcholine recognition domain from the acetylcholine-binding protein: crystallographic and ligand selectivity analyses. J Biol Chem 286: 42555-42565.
46. Luo S, Zhangsun D, Feng J, Wu Y, Zhu X, et al. (2007) Diversity of the O-superfamily conotoxins from Conus miles. J Pept Sci 13: 44-53.
47. Luo S, Akondi KB, Zhangsun D, Wu Y, Zhu X, et al. (2010) Atypical alpha-conotoxin LtIA from Conus litteratus targets a novel microsite of the alpha3beta2 nicotinic receptor. J Biol Chem 285: 12355-12366.
48. Pi C, Liu J, Peng C, Liu Y, Jiang X, et al. (2006) Diversity and evolution of conotoxins based on gene expression profiling of Conus litteratus. Genomics 88: 809-819.
49. Loughnan ML, Nicke A, Lawrence N, Lewis RJ, (2009) Novel alpha D-conopeptides and their precursors identified by cDNA cloning define the D-conotoxin superfamily. Biochemistry 48: 3717-3729.
50. Mebs D, Kordis D, Kendel Y, Kauferstein S, (2011) The evolution of alphaD-conopeptides targeting neuronal nicotinic acetylcholine receptors. Acta Chim Slov 58: 730-734.
51. Buczek O, Jimenez EC, Yoshikami D, Imperial JS, Watkins M, et al. (2008) I(1)-superfamily conotoxins and prediction of single D-amino acid occurrence. Toxicon 51: 218-229.
52. Fan CX, Chen XK, Zhang C, Wang LX, Duan KL, et al. (2003) A novel conotoxin from Conus betulinus, kappa-BtX, unique in cysteine pattern and in function as a specific BK channel modulator. J Biol Chem 278: 12624-12633.
53. Yuan DD, Liu L, Shao XX, Peng C, Chi CW, et al. (2009) New conotoxins define the novel I3-superfamily. Peptides 30: 861-865.
54. Biggs JS, Watkins M, Puillandre N, Ownby JP, Lopez-Vera E, et al. (2010) Evolution of Conus peptide toxins: analysis of Conus californicus Reeve, 1844. Mol Phylogenet Evol 56: 1-12.
55. Lluisma AO, Lopez-Vera E, Bulaj G, Watkins M, Olivera BM, (2008) Characterization of a novel psi-conotoxin from Conus parius Reeve. Toxicon 51: 174-180.
56. Lu BS, Yu F, Zhao D, Huang PT, Huang CF, (1999) Conopeptides from Conus striatus and Conus textile by cDNA cloning. Peptides 20: 1139-1144.
57. Lirazan MB, Hooper D, Corpuz GP, Ramilo CA, Bandyopadhyay P, et al. (2000) The spasmodic peptide defines a new conotoxin superfamily. Biochemistry 39: 1583-1588.
58. England LJ, Imperial J, Jacobsen R, Craig AG, Gulyas J, et al. (1998) Inactivation of a serotonin-gated ion channel by a polypeptide toxin from marine snails. Science 281: 575-578.
59. Jakubowski JA, Keays DA, Kelley WP, Sandall DW, Bingham JP, et al. (2004) Determining sequences and post-translational modifications of novel conotoxins in Conus victoriae using cDNA sequencing and mass spectrometry. J Mass Spectrom 39: 548-557.
60. Peng C, Liu L, Shao X, Chi C, Wang C, (2008) Identification of a novel class of conotoxins defined as V-conotoxins with a unique cysteine pattern and signal peptide sequence. Peptides 29: 985-991.
61. Yuan DD, Liu L, Shao XX, Peng C, Chi CW, et al. (2008) Isolation and cloning of a conotoxin with a novel cysteine pattern from Conus caracteristicus. Peptides 29: 1521-1525.
62. Luo SQ, Kulak JM, Cartier GE, Jacobsen RB, Yoshikami D, et al. (1998) alpha-Conotoxin AuIB selectively blocks alpha 3 beta 4 nicotinic acetylcholine receptors and nicotine-evoked norepinephrine release. Journal of Neuroscience 18: 8571-8579.
63. Teichert RW, Rivier J, Torres J, Dykert J, Miller C, et al. (2005) A uniquely selective inhibitor of the mammalian fetal neuromuscular nicotinic acetylcholine receptor. J Neurosci 25: 732-736.
64. Jimenez EC, Olivera BM, Teichert RW, (2007) AlphaC-conotoxin PrXA: a new family of nicotinic acetylcholine receptor antagonists. Biochemistry 46: 8717-8724.
65. Loughnan M, Nicke A, Jones A, Schroeder CI, Nevin ST, et al. (2006) Identification of a novel class of nicotinic receptor antagonists: dimeric conotoxins VxXIIA, VxXIIB, and VxXIIC from Conus vexillum. J Biol Chem 281: 24745-24755.
66. Kauferstein S, Kendel Y, Nicke A, Coronas FI, Possani LD, et al. (2009) New conopeptides of the D-superfamily selectively inhibiting neuronal nicotinic acetylcholine receptors. Toxicon 54: 295-301.
67. Teichert RW, Jimenez EC, Olivera BM, (2005) Alpha S-conotoxin RVIIIA: a structurally unique conotoxin that broadly targets nicotinic acetylcholine receptors. Biochemistry 44: 7897-7902.
68. Shon KJ, Grilley M, Jacobsen R, Cartier GE, Hopkins C, et al. (1997) A noncompetitive peptide inhibitor of the nicotinic acetylcholine receptor from Conus purpurascens venom. Biochemistry 36: 9581-9587.