A novel mechanism of inhibition of high-voltage activated calcium channels by α-conotoxins contributes to relief of nerve injury-induced neuropathic pain

Pain

Volumn 152, Issue 2, 2011, Pages 259-266

  Klimis, Harry ^a   Adams, D J ^b,c   Callaghan, B ^b,c   Nevin, S ^b   Alewood, P F ^b   Vaughan, C W ^a   Mozar, C A ^a   Christie, M J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c RMIT UNIVERSITY   (Australia)

Author keywords

Conotoxin; GABA B receptor; Mechanical allodynia; N type Ca 2+ channel; Neuropathic pain; Nicotinic acetylcholine receptor; Sensory neuron

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; 5,5 DIMETHYL 2 MORPHOLINEACETIC ACID; ALPHA CONOTOXIN AUIB; ALPHA CONOTOXIN MII; ALPHA CONOTOXIN VC1 1; BACLOFEN; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CALCIUM CHANNEL; CALCIUM CHANNEL N TYPE; CONOTOXIN; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC PAIN; DRUG MECHANISM; DRUG POTENCY; MALE; MEMBRANE CURRENT; MOTOR PERFORMANCE; NERVE INJURY; NERVE LIGATION; NEUROPATHIC PAIN; NEUROTRANSMISSION; NONHUMAN; OOCYTE; PAIN; PRIORITY JOURNAL; RAT; SPINAL GANGLION; XENOPUS LAEVIS;

ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, N-TYPE; CELLS, CULTURED; CONOTOXINS; DISEASE MODELS, ANIMAL; FEMALE; MALE; PAIN; PERIPHERAL NERVOUS SYSTEM DISEASES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SCIATIC NEUROPATHY; SENSORY RECEPTOR CELLS;

EID: 78651488405     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2010.09.007     Document Type: Article

References (45)

1. M. Abe, T. Kurihara, W. Han, K. Shinomiya, and T. Tanabe Changes in expression of voltage-dependent ion channel subunits in dorsal root ganglia of rats with radicular injury and pain Spine 27 2002 1517 1524
2. D. Alonso, Z. Khalil, N. Satkunanathan, and B.G. Livett Drugs from the sea: conotoxins as drug leads for neuropathic pain and other neurological conditions Mini Rev Med Chem 3 2003 785 787
3. 2+ channels to treat pain: T-type versus N-type Trends Pharmacol Sci 25 2004 465 470
4. B receptors Physiol Rev 84 2004 835 867
5. F.M. Blyth, L.M. March, A.J. Brnabic, L.R. Jorm, M. Williamson, and M.J. Cousins Chronic pain in Australia: a prevalence study Pain 89 2001 127 134
6. B receptor antagonist J Pharmacol Exp Ther 274 1995 1393 1398
7. B. Callaghan, and D.J. Adams Analgesic α-conotoxins Vc1.1 and RgIA inhibit N-type calcium channels in sensory neurons of α9 nicotinic receptor knockout mice Channels 4 2010 1 4
8. B receptor activation J Neurosci 28 2008 10943 10951
9. G.E. Cartier, D. Yoshikami, W.R. Gray, S. Luo, B.M. Olivera, and J.M. McIntosh A new α-conotoxin which targets α3β2 nicotinic acetylcholine receptors J Biol Chem 271 1996 7522 7528
10. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 53 1994 55 63
11. 2+ channels in the rat spinal cord following chronic constrictive nerve injury Exp Brain Res 147 2002 456 463
12. R.J. Clark, H. Fischer, S.T. Nevin, D.J. Adams, and D.J. Craik The synthesis, structural characterisation and receptor specificity of the α-conotoxin Vc1.1 J Biol Chem 281 2006 23254 23263
13. M.J. Cousins, F. Brennan, and D.B. Carr Pain relief: a universal human right Pain 112 2004 1 4
14. J.L. Dutton, P.S. Bansal, R.C. Hogg, D.J. Adams, P.F. Alewood, and D.J. Craik A new level of conotoxin diversity, a non-native disulfide bond connectivity in α-conotoxin AuIB reduces structural definition but increases biological activity J Biol Chem 277 2002 48849 48857
15. J.L. Dutton, and D.J. Craik α-Conotoxins: nicotinic acetylcholine receptor antagonists as pharmacological tools and potential drug leads Curr Med Chem 8 2001 327 344
16. E. Eisenberg, E.D. McNicol, and D.B. Carr Efficacy and safety of opioid agonists in the treatment of neuropathic pain of nonmalignant origin: systematic review and meta-analysis of randomized controlled trials JAMA 293 2005 3043 3052
17. D. Everhart, G.E. Cartier, A. Malhotra, A.V. Gomes, J.M. McIntosh, and C.W. Luetje Determinants of potency on α-conotoxin MII, a peptide antagonist of neuronal nicotinic receptors Biochemistry 43 2004 2732 2737
18. K. Gayler, D. Sandall, D. Greening, D. Keays, M. Polidano, B. Livett, J. Down, N. Satkunanathan, and Z. Khalil Molecular prospecting for drugs from the sea. Isolating therapeutic peptides and proteins from cone snail venom IEEE Eng Med Biol 24 2005 79 84
19. S.C. Harvey, J.M. McIntosh, G.E. Cartier, F.N. Maddox, and C.W. Luetje Determinants of specificity for α-conotoxin MII on α3β2 neuronal nicotinic receptors Mol Pharmacol 51 1997 336 342
20. 2+ channels Neuroreport 12 2001 2423 2427
21. P.G. Jones, and J. Dunlop Targeting the cholinergic system as a therapeutic strategy for the treatment of pain Neuropharmacology 53 2007 197 206
22. A. Kolosov, C.S. Goodchild, and I. Cooke CNSB004 (Leconotide) causes antihyperalgesia without side effects when given intravenously: a comparison with ziconotide in a rat model of diabetic neuropathic pain 2009 Pain Med 11 2010 262 273
23. C. Kim, K. Jun, T. Lee, S.S. Kim, M.W. McEnery, H. Chin, H.L. Kim, J.M. Park, D.K. Kim, S.J. Jung, J. Kim, and H.S. Shin Altered nociceptive response in mice deficient in the alpha(1B) subunit of the voltage-dependent calcium channel Mol Cell Neurosci 18 2001 235 245
24. P.M. Lang, R. Burgstahler, R.V. Haberberger, W. Sippel, and P. Grafe A conus peptide blocks nicotinic receptors of unmyelinated axons in human nerves Neuroreport 16 2005 479 483
25. P.M. Lang, R. Burgstahler, W. Sippel, D. Irnich, B. Schlotter-Weigel, and P. Grafe Characterization of neuronal nicotinic acetylcholine receptors in the membrane of unmyelinated human C-fiber axons by in vitro studies J Neurophysiol 90 2003 3295 3303
26. B.G. Livett, K.R. Gayler, and Z. Khalil Drugs from the sea: conopeptides as potential therapeutics Curr Med Chem 11 2004 1715 1723
27. S. Luo, J.M. Kulak, G.E. Cartier, R.B. Jacobsen, D. Yoshikami, B.M. Olivera, and J.M. McIntosh α-Conotoxin AuIB selectively blocks α3β4 nicotinic acetylcholine receptors and nicotine-evoked norepinephrine release J Neurosci 18 1998 8571 8579
28. J.G. McGivern Targeting N-type and T-type calcium channels for the treatment of pain Drug Discov Today 11 2006 245 253
29. J.M. McIntosh, N. Absalom, M. Chebib, A.B. Elgoyhen, and M. Vincler Alpha9 nicotinic acetylcholine receptors and the treatment of pain Biochem Pharmacol 78 2009 693 702
30. J.M. McIntosh, A.D. Santos, and B.M. Olivera Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes Ann Rev Biochem 68 1999 59 88
31. S.T. Nevin, R.J. Clark, H. Klimis, M.J. Christie, D.J. Craik, and D.J. Adams Are α9α10 nicotinic acetylcholine receptors a pain target for α-conotoxins? Mol Pharmacol 72 2007 1406 1410
32. H.-L. Pan, Z.-Z. Wu, H.-Y. Zhou, S.-R. Chen, H.-M. Zhang, and D.-P. Li Modulation of pain transmission by G-protein-coupled receptors Pharmacol Ther 117 2008 141 161
33. S. Patel, S. Naeem, S. Kesingland, S. Froestl, M. Capogna, L. Urban, and A. Fox The effects of GABA(B) agonists and gabapentin on mechanical hyperalgesia in models of neuropathic and inflammatory pain in the rat Pain 90 2001 217 226
34. K.K. Rau, R.D. Johnson, and B.Y. Cooper Nicotinic ACh in subclassified capsaicin-sensitive and -insensitive nociceptors of the rat DRG J Neurophysiol 93 2005 1358 1371
35. 2+ channel EMBO J 20 2001 2349 2356
36. D.W. Sandall, N. Satkunanathan, D.A. Keays, M.A. Polidano, X. Liping, V. Pham, J.G. Down, Z. Khalil, B.G. Livett, and K.R. Gayler A novel α-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo Biochemistry 42 2003 6904 6911
37. N. Satkunanathan, B. Livett, K. Gayler, D. Sandall, J. Down, and Z. Khalil α-Conotoxin Vc1.1 alleviates neuropathic pain and accelerates functional recovery of injured neurones Brain Res 1059 2005 149 158
38. M. Schnolzer, P. Alewood, A. Jones, D. Alewood, and S.B. Kent In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, high yield assembly of difficult sequences Int J Pept Protein Res 40 1992 180 193
39. B(1) Neuron 31 2001 47 58
40. Z. Seltzer, R. Dubner, and Y. Shir A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury Pain 43 1990 205 218
41. H. Terlau, and B.M. Olivera Conus venoms: a rich source of novel ion channel-targeted peptides Physiol Rev 84 2004 41 68
42. M. Vincler, and J.M. McIntosh Targeting the α9α10 nicotinic acetylcholine receptor to treat severe pain Expert Opin Ther Targets 11 2007 891 897
43. M. Vincler, S. Wittenauer, R. Parker, M. Ellison, B.M. Olivera, and J.M. McIntosh Molecular mechanism for analgesia involving specific antagonism of α9α10 nicotinic acetylcholine receptors Proc Natl Acad Sci USA 103 2006 17880 17884
44. 2+ channel expression after preconditioning is responsible for prostaglandin E2-induced long-lasting allodynia Anesthesiology 99 2003 1364 1370
45. T. Young, S. Wittenauer, J.M. McIntosh, and M. Vincler Spinal α3β nicotinic acetylcholine receptors tonically inhibit the transmission of nociceptive stimuli Brain Res 1229 2008 118 124