Therapeutic potential of cone snail venom peptides (conopeptides)

Current Topics in Medicinal Chemistry

Volumn 12, Issue 14, 2012, Pages 1546-1552

  Vetter, Irina ^a   Lewis, Richard J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Conopeptides; GPCR; Ion channels

Indexed keywords

ALPHA CONOTOXIN MII; AMPA RECEPTOR; CHI CONOPEPTIDE DERIVATIVE; CONANTOKIN G; CONOPEPTIDE DERIVATIVE; CONOPRESSIN; CONOTOXIN; CONTULAKIN DERIVATIVE; DELTA CONOTOXIN; G PROTEIN COUPLED RECEPTOR; IKOT IKOT CONOPEPTIDE DERIVATIVE; ION CHANNEL; MEMBRANE PROTEIN; MU CONOTOXIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTENSIN RECEPTOR; NICOTINIC RECEPTOR; OMEGA CONOTOXIN CVID; OMEGA CONOTOXIN MVIIA; ORGANIC ANION TRANSPORTER; RHO CONOTOXIN; SEROTONIN RECEPTOR; SIGMA CONOTOXIN; SNAIL VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; XEN 2174;

ANALGESIA; ARTICLE; DRUG ACTIVITY; DRUG EFFICACY; DRUG INDICATION; DRUG RECEPTOR BINDING; DRUG STRUCTURE; EPILEPSY; HEART ARRHYTHMIA; HUMAN; IRRITABLE COLON; MOLECULAR WEIGHT; NONHUMAN; PAIN; PROSTATE HYPERTROPHY; PROTEIN TARGETING; SNAIL; VOMITING;

ANIMALS; CONOTOXINS; CONUS SNAIL; HUMANS; MEMBRANE PROTEINS; PAIN; PEPTIDES;

EID: 84866941648     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802612802652457     Document Type: Article

References (64)

1. Lewis, R.J.; Garcia, M.L. Therapeutic potential of venom peptides. Nat. Rev. Drug Discov., 2003, 2, 790-802.
2. Lewis, R.J.; Dutertre, S.; Vetter, I.; Christie, M.J. Conus venom peptide pharmacology. Pharmacol. Rev., 2012, 64, 259-98.
3. Catterall, W.A.; Perez-Reyes, E.; Snutch, T.P.; Striessnig, J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev., 2005, 57, 411-25.
4. Lewis, R.J.; Nielsen, K.J.; Craik, D.J.; Loughnan, M.L.; Adams, D.A.; Sharpe, I.A.; Luchian, T.; Adams, D.J.; Bond, T.; Thomas, L.; Jones, A.; Matheson, J.L.; Drinkwater, R.; Andrews, P.R.; Alewood, P.F. Novel ω-conotoxins from Conus catus discriminate among neuronal calcium channel subtypes. J. Biol. Chem., 2000, 275, 35335-44.
5. Malmberg, A.B.; Yaksh, T.L. Effect of continuous intrathecal infusion of omega-conopeptides, N-type calcium-channel blockers, on behavior and antinociception in the formalin and hot-plate tests in rats. Pain, 1995, 60, 83-90.
6. Smith, M.T.; Cabot, P.J.; Ross, F.B.; Robertson, A.D.; Lewis, R.J. The novel N-type calcium channel blocker, AM336, produces potent dose-dependent antinociception after intrathecal dosing in rats and inhibits substance P release in rat spinal cord slices. Pain, 2002, 96, 119-27.
7. Nielsen, K.J.; Schroeder, T.; Lewis, R. Structure-activity relationships of ω-conotoxins at N-type voltage-sensitive calcium channels. J. Mol. Recognit., 2000, 13, 55-70.
8. Schroeder, C.I.; Smythe, M.L.; Lewis, R.J. Development of small molecules that mimic the binding of ω-conotoxins at the N-type voltage-gated calcium channel. Mol. Divers., 2004, 8, 127-34.
9. Scott, D.A.; Wright, C.E.; Angus, J.A. Actions of intrathecal ω-conotoxins CVID, GVIA, MVIIA, and morphine in acute and neuropathic pain in the rat. Eur. J. Pharmacol., 2002, 451, 279-86.
10. Berecki, G.; Motin, L.; Haythornthwaite, A.; Vink, S.; Bansal, P.; Drinkwater, R.; Wang, C.I.; Moretta, M.; Lewis, R.J.; Alewood, P.F.; Christie, M.J.; Adams, D.J. Analgesic ω-conotoxins CVIE and CVIF selectively and voltage-dependently block recombinant and native N-type calcium channels. Mol. Pharmacol., 2010, 77, 139-48.
11. Catterall, W.A.; Goldin, A.L.; Waxman, S.G. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev., 2005, 57, 397-409.
12. Wood, J.N.; Boorman, J. Voltage-gated sodium channel blockers; target validation and therapeutic potential. Curr. Top. Med. Chem., 2005, 5, 529-37.
13. Wingerd, J.S.; Vetter, I.; Lewis, R.J., Voltage Gated Sodium Channels as Therapeutic Targets., in Therapeutic Targets: Modulation, Inhibition, and Activation, E. Luis M. Botana and Mabel Loza, Editor. 2011, John Wiley & Sons: New Jersey.
14. v1.8 sensory neuron specific sodium channels and chronic pain behavior without motor deficits. Proc Natl Acad Sci USA, 2006, 103, 17030-5.
15. Vetter, I.; Dekan, Z.; Knapp, O.; Adams, D.J.; Alewood, P.F.; Lewis, R.J. Isolation, characterization and total regioselective synthesis of the novel μO-conotoxin MfVIA from Conus magnificus that targets voltage-gated sodium channels. Biochem. Pharmacol., 2012,
16. Leipold, E.; Hansel, A.; Olivera, B.M.; Terlau, H.; Heinemann, S.H. Molecular interaction of δ-conotoxins with voltage-gated sodium channels. FEBS Lett., 2005, 579, 3881-3884.
17. Nicke, A.; Wonnacott, S.; Lewis, R.J. α-Conotoxins as tools for the elucidation of structure and function of neuronal nicotinic acetylcholine receptor subtypes. Eur. J. Biochem., 2004, 271, 2305-2319.
18. Sandall, D.W.; Satkunanathan, N.; Keays, D.A.; Polidano, M.A.; Liping, X.; Pham, V.; Down, J.G.; Khalil, Z.; Livett, B.G.; Gayler, K.R. A novel α-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo. Biochemistry, 2003, 42, 6904-6911.
19. B receptor activation. J. Neurosci., 2008, 28, 10943-10951.
20. Satkunanathan, N.; Livett, B.; Gayler, K.; Sandall, D.; Down, J.; Khalil, Z. α-Conotoxin Vc1.1 alleviates neuropathic pain and accelerates functional recovery of injured neurones. Brain Res., 2005, 1059, 149-158.
21. Luo, S.; Akondi, K.B.; Zhangsun, D.; Wu, Y.; Zhu, X.; Hu, Y.; Christensen, S.; Dowell, C.; Daly, N.L.; Craik, D.J.; Wang, C.I.; Lewis, R.J.; Alewood, P.F.; Michael McIntosh, J. Atypical α-conotoxin LtIA from Conus litteratus targets a novel microsite of the α3β2 nicotinic receptor. J. Biol. Chem., 2010, 285, 12355-12366.
22. Grishin, A.A.; Wang, C.I.; Muttenthaler, M.; Alewood, P.F.; Lewis, R.J.; Adams, D.J. Alpha-conotoxin AuIB isomers exhibit distinct inhibitory mechanisms and differential sensitivity to stoichiometry of α3β4 nicotinic acetylcholine receptors. J. Biol. Chem., 2010, 285, 22254-22263.
23. Dekan, Z.; Vetter, I.; Daly, N.L.; Craik, D.J.; Lewis, R.J.; Alewood, P.F. α-Conotoxin ImI incorporating stable cystathionine bridges maintains full potency and identical three-dimensional structure. J. Am. Chem. Soc., 2011, 133, 15866-15869.
24. Sharpe, I.A.; Gehrmann, J.; Loughnan, M.L.; Thomas, L.; Adams, D.A.; Atkins, A.; Palant, E.; Craik, D.J.; Adams, D.J.; Alewood, P.F.; Lewis, R.J. Two new classes of conopeptides inhibit the α1-adrenoceptor and noradrenaline transporter. Nat. Neurosci., 2001, 4, 902-7.
25. Nielsen, C.K.; Lewis, R.J.; Alewood, D.; Drinkwater, R.; Palant, E.; Patterson, M.; Yaksh, T.L.; McCumber, D.; Smith, M.T. Antiallodynic efficacy of the χ-conopeptide, Xen2174, in rats with neuropathic pain. Pain, 2005, 118, 112-24.
26. Brust, A.; Palant, E.; Croker, D.E.; Colless, B.; Drinkwater, R.; Patterson, B.; Schroeder, C.I.; Wilson, D.; Nielsen, C.K.; Smith, M.T.; Alewood, D.; Alewood, P.F.; Lewis, R.J. χ-Conopeptide pharmacophore development: toward a novel class of norepinephrine transporter inhibitor (Xen2174) for pain. J. Med. Chem., 2009, 52, 6991-7002.
27. Lewis, R.J. Discovery and development of the χ-conopeptide class of analgesic peptides. Toxicon, 2012, 59, 524-528.
28. Paczkowski, F.A.; Sharpe, I.A.; Dutertre, S.; Lewis, R.J. χ-Conotoxin and tricyclic antidepressant interactions at the norepinephrine transporter define a new transporter model. J. Biol. Chem., 2007, 282, 17837-17844.
29. Malmberg, A.B.; Gilbert, H.; McCabe, R.T.; Basbaum, A.I. Powerful antinociceptive effects of the cone snail venom-derived subtype-selective NMDA receptor antagonists conantokins G and T. Pain, 2003, 101, 109-116.
30. Jimenez, E.C.; Donevan, S.; Walker, C.; Zhou, L.M.; Nielsen, J.; Cruz, L.J.; Armstrong, H.; White, H.S.; Olivera, B.M. Conantokin-L, a new NMDA receptor antagonist: determinants for anticonvulsant potency. Epilepsy Res., 2002, 51, 73-80.
31. Craig, A.G.; Norberg, T.; Griffin, D.; Hoeger, C.; Akhtar, M.; Schmidt, K.; Low, W.; Dykert, J.; Richelson, E.; Navarro, V.; Mazella, J.; Watkins, M.; Hillyard, D.; Imperial, J.; Cruz, L.J.; Olivera, B.M. Contulakin-G, an O-glycosylated invertebrate neurotensin. J. Biol. Chem., 1999, 274, 13752-13759.
32. Allen, J.W.; Hofer, K.; McCumber, D.; Wagstaff, J.D.; Layer, R.T.; McCabe, R.T.; Yaksh, T.L. An assessment of the antinociceptive efficacy of intrathecal and epidural contulakin-G in rats and dogs. Anesth. Analg., 2007, 104, 1505-1513, table of contents.
33. Machu, T.K. Therapeutics of 5-HT3 receptor antagonists: current uses and future directions. Pharmacol. Ther., 2011, 130, 338-347.
34. Karnovsky, A.M.; Gotow, L.F.; McKinley, D.D.; Piechan, J.L.; Ruble, C.L.; Mills, C.J.; Schellin, K.A.; Slightom, J.L.; Fitzgerald, L.R.; Benjamin, C.W.; Roberds, S.L. A cluster of novel serotonin receptor 3-like genes on human chromosome 3. Gene, 2003, 319, 137-148.
35. Niesler, B.; Frank, B.; Kapeller, J.; Rappold, G.A. Cloning, physical mapping and expression analysis of the human 5-HT3 serotonin receptor-like genes HTR3C, HTR3D and HTR3E. Gene, 2003, 310, 101-111.
36. England, L.J.; Imperial, J.; Jacobsen, R.; Craig, A.G.; Gulyas, J.; Akhtar, M.; Rivier, J.; Julius, D.; Olivera, B.M. Inactivation of a serotonin-gated ion channel by a polypeptide toxin from marine snails. Science, 1998, 281, 575-578.
37. Mellor, I.R. The AMPA receptor as a therapeutic target: current perspectives and emerging possibilities. Future Med. Chem., 2010, 2, 877-891.
38. Armstrong, N.; Jasti, J.; Beich-Frandsen, M.; Gouaux, E. Measurement of conformational changes accompanying desensitization in an ionotropic glutamate receptor. Cell, 2006, 127, 85-97.
39. Walker, C.S.; Jensen, S.; Ellison, M.; Matta, J.A.; Lee, W.Y.; Imperial, J.S.; Duclos, N.; Brockie, P.J.; Madsen, D.M.; Isaac, J.T.; Olivera, B.; Maricq, A.V. A novel Conus snail polypeptide causes excitotoxicity by blocking desensitization of AMPA receptors. Curr. Biol., 2009, 19, 900-908.
40. Lynch, G. AMPA receptor modulators as cognitive enhancers. Curr. Opin. Pharmacol., 2004, 4, 4-11.
41. Koch, W.J.; Rockman, H.A.; Samama, P.; Hamilton, R.A.; Bond, R.A.; Milano, C.A.; Lefkowitz, R.J. Cardiac function in mice overexpressing the β-adrenergic receptor kinase or a β ARK inhibitor. Science, 1995, 268, 1350-1353.
42. Bylund, D.B.; Eikenberg, D.C.; Hieble, J.P.; Langer, S.Z.; Lefkowitz, R.J.; Minneman, K.P.; Molinoff, P.B.; Ruffolo, R.R., Jr.; Trendelenburg, U. International Union of Pharmacology nomenclature of adrenoceptors. Pharmacol. Rev., 1994, 46, 121-136.
43. Graham, R.M.; Perez, D.M.; Hwa, J.; Piascik, M.T. α1-Adrenergic receptor subtypes. Molecular structure, function, and signaling. Circ. Res., 1996, 78, 737-749.
44. Sharpe, I.A.; Thomas, L.; Loughnan, M.; Motin, L.; Palant, E.; Croker, D.E.; Alewood, D.; Chen, S.; Graham, R.M.; Alewood, P.F.; Adams, D.J.; Lewis, R.J. Allosteric α1-adrenoreceptor antagonism by the conopeptide ρ-TIA. J. Biol. Chem., 2003, 278, 34451-34457.
45. Chen, Z.; Rogge, G.; Hague, C.; Alewood, D.; Colless, B.; Lewis, R.J.; Minneman, K.P. Subtype-selective noncompetitive or competitive inhibition of human α1-adrenergic receptors by ρ-TIA. J. Biol. Chem., 2004, 279, 35326-35333.
46. Docherty, J.R. Subtypes of functional α1-adrenoceptor. Cell Mol. Life Sci., 2010, 67, 405-417.
47. Zuscik, M.J.; Sands, S.; Ross, S.A.; Waugh, D.J.; Gaivin, R.J.; Morilak, D.; Perez, D.M. Overexpression of the α1B-adrenergic receptor causes apoptotic neurodegeneration: multiple system atrophy. Nat. Med., 2000, 6, 1388-1394.
48. Petersson, M. Cardiovascular effects of oxytocin. Prog. Brain Res., 2002, 139, 281-288.
49. Gimpl, G.; Fahrenholz, F. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev., 2001, 81, 629-683.
50. Birnbaumer, M. Vasopressin receptors. Trends Endocrinol. Metab., 2000, 11, 406-410.
51. Chini, B.; Mouillac, B.; Balestre, M.N.; Trumpp-Kallmeyer, S.; Hoflack, J.; Hibert, M.; Andriolo, M.; Pupier, S.; Jard, S.; Barberis, C. Two aromatic residues regulate the response of the human oxytocin receptor to the partial agonist arginine vasopressin. FEBS Lett., 1996, 397, 201-206.
52. Kimura, T.; Makino, Y.; Saji, F.; Takemura, M.; Inoue, T.; Kikuchi, T.; Kubota, Y.; Azuma, C.; Nobunaga, T.; Tokugawa, Y.; et al. Molecular characterization of a cloned human oxytocin receptor. Eur. J. Endocrinol., 1994, 131, 385-90.
53. Mitchell, B.F.; Fang, X.; Wong, S. Oxytocin: a paracrine hormone in the regulation of parturition? Rev. Reprod., 1998, 3, 113-122.
54. Cruz, L.J.; de Santos, V.; Zafaralla, G.C.; Ramilo, C.A.; Zeikus, R.; Gray, W.R.; Olivera, B.M. Invertebrate vasopressin/oxytocin homologs. Characterization of peptides from Conus geographus and Conus straitus venoms. J. Biol. Chem., 1987, 262, 15821-15824.
55. Moller, C.; Mari, F. A vasopressin/oxytocin-related conopeptide with γ-carboxyglutamate at position 8. Biochem. J., 2007, 404, 413-419.
56. Dutertre, S.; Croker, D.; Daly, N.L.; Andersson, A.; Muttenthaler, M.; Lumsden, N.G.; Craik, D.J.; Alewood, P.F.; Guillon, G.; Lewis, R.J. Conopressin-T from Conus tulipa reveals an antagonist switch in vasopressin-like peptides. J. Biol. Chem., 2008, 283, 7100-7108.
57. Ueberheide, B.M.; Fenyo, D.; Alewood, P.F.; Chait, B.T. Rapid sensitive analysis of cysteine rich peptide venom components. Proc. Natl. Acad. Sci. USA, 2009, 106, 6910-6915.
58. Vetter, I.; Davis, J.L.; Rash, L.D.; Anangi, R.; Mobli, M.; Alewood, P.F.; Lewis, R.J.; King, G.F. Venomics: a new paradigm for natural products-based drug discovery. Amino Acids, 2011, 40, 15-28.
59. Vetter, I.; Lewis, R.J. Characterization of endogenous calcium responses in neuronal cell lines. Biochem. Pharmacol., 2010, 79, 908-920.
60. v types endogenously expressed in human SH-SY5Y neuroblastoma cells. Biochem. Pharmacol., 2012, 83, 1562-1571.
61. Prashanth, J.R.; Lewis, R.J.; Dutertre, S. Towards an integrated venomics approach for accelerated conopeptide discovery. Toxicon, 2012, 470-477.
62. Dekan, Z.; Wang, C.I.; Andrews, R.K.; Lewis, R.J.; Alewood, P.F. Conotoxin engineering: Dual pharmacophoric noradrenaline transport inhibitor/integrin binding peptide with improved stability. Org. Biomol. Chem., 2012, 5791-5794.
63. Muttenthaler, M.; Andersson, A.; de Araujo, A.D.; Dekan, Z.; Lewis, R.J.; Alewood, P.F. Modulating oxytocin activity and plasma stability by disulfide bond engineering. J. Med. Chem., 2010, 53, 8585-8596.
64. Muttenthaler, M.; Nevin, S.T.; Grishin, A.A.; Ngo, S.T.; Choy, P.T.; Daly, N.L.; Hu, S.H.; Armishaw, C.J.; Wang, C.I.; Lewis, R.J.; Martin, J.L.; Noakes, P.G.; Craik, D.J.; Adams, D.J.; Alewood, P.F. Solving the α-conotoxin folding problem: efficient selenium-directed on-resin generation of more potent and stable nicotinic acetylcholine receptor antagonists. J. Am. Chem. Soc., 2010, 132, 3514-3522.