The differential effects of two sodium channel modulators on the conductive properties of C-fibers in pig skin in vivo

Anesthesia and Analgesia

Volumn 115, Issue 3, 2012, Pages 560-571

  Obreja, Otilia ^a   Hirth, Michael ^a   Turnquist, Brian ^b   Rukwied, Roman ^a   Ringkamp, Matthias ^c   Schmelz, Martin ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b BETHEL UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HARKOSERIDE; LIDOCAINE; SODIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; ELECTROSTIMULATION; IN VIVO STUDY; LATENT PERIOD; MECHANORECEPTOR; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SAPHENOUS NERVE; SPIKE; SWINE; SYNTHETIC FIBER;

ACETAMIDES; ANALGESICS; ANIMALS; ELECTRIC STIMULATION; FEMALE; LIDOCAINE; MALE; NERVE FIBERS, UNMYELINATED; NEURAL CONDUCTION; NOCICEPTORS; REACTION TIME; SKIN; SODIUM CHANNELS; SWINE;

EID: 84865696010     PISSN: 00032999     EISSN: None     Source Type: Journal    
DOI: 10.1213/ANE.0b013e3182542843     Document Type: Article

References (68)

1. Wolff RF, Bala MM, Westwood M, Kessels AG, Kleijnen J. 5% lidocaine-medicated plaster vs other relevant interventions and placebo for post-herpetic neuralgia (PHN): a systematic review. Acta Neurol Scand 2011;123:295-309
2. Rauck RL, Shaibani A, Biton V, Simpson J, Koch B. Lacosamide in painful diabetic peripheral neuropathy: a phase 2 doubleblind placebo-controlled study. Clin J Pain 2007;23:150-8
3. Hille B. Ion Channels of Excitable Membranes. 3rd ed. Sunderland, MA: Sinauer Associates, Inc., 2001
4. Errington AC, Stoehr T, Heers C, Lees G. The investigational anticonvulsant lacosamide selectively enhances slow inactivation of voltage-gated sodium channels. Mol Pharmacol 2007;73:157-69
5. Wang Y, Khanna R. Voltage-gated calcium channels are not affected by the novel anti-epileptic drug lacosamide. Transl Neurosci 2011;2:13-22
6. Hildebrand ME, Smith PL, Bladen C, Eduljee C, Xie JY, Chen L, Fee-Maki M, Doering CJ, Mezeyova J, Zhu Y, Belardetti F, Pajouhesh H, Parker D, Arneric SP, Parmar M, Porreca F, Tringham E, Zamponi GW, Snutch TP. A novel slowinactivation-specific ion channel modulator attenuates neuropathic pain. Pain 2011;152:833-43
7. Cheng X, Dib-Hajj SD, Tyrrell L, Te Morsche RH, Drenth JP, Waxman SG. Deletion mutation of sodium channel NaV1.7 in inherited erythromelalgia: enhanced slow inactivation modulates dorsal root ganglion neuron hyperexcitability. Brain 2011;134:1972-86
8. De Col R, Messlinger K, Carr RW. Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol 2008;586:1089-103
9. Snape A, Pittaway JF, Baker MD. Excitability parameters and sensitivity to anemone toxin ATX-II in rat small diameter primary sensory neurones discriminated by Griffonia simplicifolia isolectin IB4. J Physiol 2010;588:125-37
10. Weidner C, Schmelz M, Schmidt R, Hansson B, Handwerker HO, Torebjö rk HE. Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin. J Neurosci 1999;19:10184-90
11. Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 1999;515(Pt 3):799-811
12. Thalhammer JG, Raymond SA, Popitz-Bergez FA, Strichartz GR. Modality-dependent modulation of conduction by impulse activity in functionally characterized single cutaneous afferents in the rat. Somatosens Mot Res 1994;11:243-57
13. Shim B, Ringkamp M, Lambrinos GL, Hartke TV, Griffin JW, Meyer RA. Activity-dependent slowing of conduction velocity in uninjured L4 C fibers increases after an L5 spinal nerve injury in the rat. Pain 2007;128:40-51
14. Obreja O, Ringkamp M, Namer B, Forsch E, Klusch A, Rukwied R, Petersen M, Schmelz M. Patterns of activity-dependent conduction velocity changes differentiate classes of unmyelinated mechano-insensitive afferents including cold nociceptors, in pig and in human. Pain 2010;148:59-69
15. Lang PM, Moalem-Taylor G, Tracey DJ, Bostock H, Grafe P. Activity-dependent modulation of axonal excitability in unmyelinated peripheral rat nerve fibers by the 5-HT(3) serotonin receptor. J Neurophysiol 2006;96:2963-71
16. Obreja O, Kluschina O, Mayer A, Hirth M, Schley M, Schmelz M, Rukwied R. NGF enhances electrically induced pain, but not axon reflex sweating. Pain 2011;152:1856-63
17. Raymond SA. Effects of nerve impulses on threshold of frog sciatic nerve fibres. J Physiol 1979;290:273-303
18. Sittl R, Carr RW, Grafe P. Sustained increase in the excitability of myelinated peripheral axons to depolarizing current is mediated by Nav1.6. Neurosci Lett 2011;492:129-33
19. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 1996;379:257-62
20. Sangameswaran L, Fish LM, Koch BD, Rabert DK, Delgado SG, Ilnicka M, Jakeman LB, Novakovic S, Wong K, Sze P, Tzoumaka E, Stewart GR, Herman RC, Chan H, Eglen RM, Hunter JC. A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 1997;272:14805-9
21. Chevrier P, Vijayaragavan K, Chahine M. Differential modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by the local anesthetic lidocaine. Br J Pharmacol 2004;142: 576-84
22. Leffler A, Reiprich A, Mohapatra DP, Nau C. Use-dependent block by lidocaine but not amitriptyline is more pronounced in tetrodotoxin (TTX)-resistant Nav1.8 than in TTX-sensitive Na+ channels. J Pharmacol Exp Ther 2007;320:354-64
23. Blair NT, Bean BP. Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 2003;23:10338-50
24. Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol 2003;89:2441-8
25. Koppert W, Ostermeier N, Sittl R, Weidner C, Schmelz M. Low-dose lidocaine reduces secondary hyperalgesia by a central mode of action. Pain 2000;85:217-24
26. Namer B, Barta B, Orstavik K, Schmidt R, Carr R, Schmelz M, Handwerker HO. Microneurographic assessment of C-fibre function in aged healthy subjects. J Physiol 2009;587:419-28
27. Serra J, Bostock H, Sola R, Aleu J, García E, Cokic B, Navarro X, Quiles C. Microneurographic identification of spontaneous activity in C-nociceptors in neuropathic pain states in humans and rats. Pain 2012;153:42-55
28. Orstavik K, Jorum E. Microneurographic findings of relevance to pain in patients with erythromelalgia and patients with diabetic neuropathy. Neurosci Lett 2010;470:180-4
29. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983;16:109-10
30. Torebjö rk HE, Hallin RG. Responses in human A and C fibres to repeated electrical intradermal stimulation. J Neurol Neurosurg Psychiatry 1974;37:653-64
31. Schmelz M, Forster C, Schmidt R, Ringkamp M, Handwerker HO, Torebjö rk HE. Delayed responses to electrical stimuli reflect C-fiber responsiveness in human microneurography. Exp Brain Res 1995;104:331-6
32. Meyer RA, Campbell JN. A novel electrophysiological technique for locating cutaneous nociceptive and chemospecific receptors. Brain Res 1988;441:81-6
33. Obreja O, Ringkamp M, Turnquist BP, Hirth M, Forsch E, Rukwied R, Petersen M, Schmelz M. Nerve growth factor selectively decreases activity-dependent conduction slowing in mechano-insensitive C-nociceptors. Pain 2011;152:2138-46
34. Campero M, Serra J, Bostock H, Ochoa JL. Partial reversal of conduction slowing during repetitive stimulation of single sympathetic efferents in human skin. Acta Physiol Scand 2004;182:305-11
35. Ringkamp M, Johanek LM, Borzan J, Hartke TV, Wu G, Pogatzki-Zahn EM, Campbell JN, Shim B, Schepers RJ, Meyer RA. Conduction properties distinguish unmyelinated sympathetic efferent fibers and unmyelinated primary afferent fibers in the monkey. PLoS ONE 2010;5:e9076
36. Gokin AP, Philip B, Strichartz GR. Preferential block of small myelinated sensory and motor fibers by lidocaine: in vivo electrophysiology in the rat sciatic nerve. Anesthesiology 2001;95:1441-54
37. Kirillova I, Teliban A, Gorodetskaya N, Grossmann L, Bartsch F, Rausch VH, Struck M, Tode J, Baron R, Jänig W. Effect of local and intravenous lidocaine on ongoing activity in injured afferent nerve fibers. Pain 2011;152:1562-71
38. Torebjork HE, Hallin RG. Perceptual changes accompanying controlled preferential blocking of A and C fibre responses in intact human skin nerves. Exp Brain Res 1973;16:321-32
39. Burgess PR, Perl ER. Myelinated afferent fibres responding specifically to noxious stimulation of the skin. J Physiol 1967;190:541-62
40. Cummins TR, Howe JR, Waxman SG. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel. J Neurosci 1998; 18:9607-19
41. Djouhri L, Fang X, Okuse K, Wood JN, Berry CM, Lawson SN. The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol 2003;550:739-52
42. Sheets PL, Heers C, Stoehr T, Cummins TR. Differential block of sensory neuronal voltage-gated sodium channels by lacosamide [(2R)-2-(acetylamino)-N- benzyl-3-methoxypropanamide], lidocaine, and carbamazepine. J Pharmacol Exp Ther 2008;326: 89-99
43. Fang X, McMullan S, Lawson SN, Djouhri L. Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurones in the rat in vivo. J Physiol 2005;565:927-43
44. Kistner K, Zimmermann K, Ehnert C, Reeh PW, Leffler A. The tetrodotoxin-resistant Na+ channel Na (v)1.8 reduces the potency of local anesthetics in blocking C-fiber nociceptors. Pflugers Arch 2010;459:751-63
45. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH, Wood JN. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 1999;2:541-8
46. Weidner C, Schmidt R, Schmelz M, Hilliges M, Handwerker HO, Torebjö rk HE. Time course of post-excitatory effects separates afferent human C fibre classes. J Physiol 2000;527(Pt 1):185-91
47. Moalem-Taylor G, Lang PM, Tracey DJ, Grafe P. Post-spike excitability indicates changes in membrane potential of isolated C-fibers. Muscle Nerve 2007;36:172-82
48. Poyraz D, Brau ME, Wotka F, Puhlmann B, Scholz AM, Hempelmann G, Kox WJ, Spies CD. Lidocaine and octanol have different modes of action at tetrodotoxin-resistant Na(+) channels of peripheral nerves. Anesth Analg 2003;97:1317-24
49. Beydoun A, D'Souza J, Hebert D, Doty P. Lacosamide: pharmacology, mechanisms of action and pooled efficacy and safety data in partial-onset seizures. Expert Rev Neurother 2009;9:33-42
50. Sheets PL, Jarecki BW, Cummins TR. Lidocaine reduces the transition to slow-inactivation in Na(v) 1.7 voltage-gated sodium channels. Br J Pharmacol 2011;164:719-30
51. Endres W, Grafe P, Bostock H, ten Bruggencate G. Changes in extracellular pH during electrical stimulation of isolated rat vagus nerve. Neurosci Lett 1986;64:201-5
52. Wang Y, Brittain JM, Jarecki BW, Park KD, Wilson SM, Wang B, Hale R, Meroueh SO, Cummins TR, Khanna R. In silico docking and electrophysiological characterization of lacosamide binding sites on collapsin response mediator protein-2 identifies a pocket important in modulating sodium channel slow inactivation. J Biol Chem 2010;285:25296-307
53. Hille B. Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 1977; 69:497-515
54. Strichartz GR, Sanchez V, Arthur GR, Chafetz R, Martin D. Fundamental properties of local anesthetics: II. Measured octanol:buffer partition coefficients and pKa values of clinically used drugs. Anesth Analg 1990;71:158-70
55. Rang HP, Ritchie JM. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol 1968;196:183-221
56. Grafe P, Quasthoff S, Grosskreutz J, Alzheimer C. Function of the hyperpolarization-activated inward rectification in nonmyelinated peripheral rat and human axons. J Neurophysiol 1997;77:421-6
57. Lang PM, Fleckenstein J, Passmore GM, Brown DA, Grafe P. Retigabine reduces the excitability of unmyelinated peripheral human axons. Neuropharmacology 2008;54:1271-8
58. Boettger MK, Till S, Chen MX, Anand U, Otto WR, Plumpton C, Trezise DJ, Tate SN, Bountra C, Coward K, Birch R, Anand P. Calcium-activated potassium channel SK1-and IK1-like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors. Brain 2002;125:252-63
59. Blair NT, Bean BP. Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 2003;23:10338-50
60. Brau ME, Nau C, Hempelmann G, Vogel W. Local anesthetics potently block a potential insensitive potassium channel in myelinated nerve. J Gen Physiol 1995;105:485-505
61. Nayak TK, Harinath S, Nama S, Somasundaram K, Sikdar SK. Inhibition of human two-pore domain K+ channel TREK1 by local anesthetic lidocaine: negative cooperativity and half-of-sites saturation kinetics. Mol Pharmacol 2009; 76:903-17
62. Du G, Chen X, Todorovic MS, Shu S, Kapur J, Bayliss DA. TASK channel deletion reduces sensitivity to local anestheticinduced seizures. Anesthesiology 2011;115:1003-11
63. Meng QT, Xia ZY, Liu J, Bayliss DA, Chen X. Local anesthetic inhibits hyperpolarization-activated cationic currents. Mol Pharmacol 2011;79:866-73
64. Olschewski A, Brau ME, Olschewski H, Hempelmann G, Vogel W. ATP-dependent potassium channel in rat cardiomyocytes is blocked by lidocaine. Possible impact on the antiarrhythmic action of lidocaine. Circulation 1996;93:656-9
65. Olschewski A, Hempelmann G, Vogel W, Safronov BV. Blockade of Na+ and K+ currents by local anesthetics in the dorsal horn neurons of the spinal cord. Anesthesiology 1998;88:172-9
66. Guo XT, Castle NA, Chernoff DM, Strichartz GR. Comparative inhibition of voltage-gated cation channels by local anesthetics. Ann N Y Acad Sci 1991;625:181-99
67. Sugiyama K, Muteki T. Local anesthetics depress the calcium current of rat sensory neurons in culture. Anesthesiology 1994;80:1369-78
68. Errington AC, Coyne L, Stohr T, Selve N, Lees G. Seeking a mechanism of action for the novel anticonvulsant lacosamide. Neuropharmacology 2006;50:1016-29