Antagonism of lidocaine inhibition by open-channel blockers that generate resurgent Na current

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4976-4987

  Bant, Jason S ^a   Aman, Teresa K ^a   Raman, Indira M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIDOCAINE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG ANTAGONISM; HIPPOCAMPAL CA3 REGION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; SODIUM CURRENT; SPIKE; VOLTAGE CLAMP;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICAL PROCESSES; CA1 REGION, HIPPOCAMPAL; CNIDARIAN VENOMS; ELECTRIC STIMULATION; FEMALE; ION CHANNEL GATING; LIDOCAINE; MALE; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; PEPTIDES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; TETRODOTOXIN; VOLTAGE-GATED SODIUM CHANNEL BETA-4 SUBUNIT; VOLTAGE-GATED SODIUM CHANNEL BLOCKERS;

EID: 84874825477     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3026-12.2013     Document Type: Article

References (58)

1. Afshari FS, Ptak K, Khaliq ZM, Grieco TM, Slater NT, McCrimmon DR, Raman IM (2004) Resurgent Na currents in four classes of neurons of the cerebellum. J Neurophysiol 92:2831-2843. CrossRef Medline
2. Ahern CA, Eastwood AL, Dougherty DA, Horn R (2008) Electrostatic contributions of aromatic residues in the local anesthetic receptor of voltagegated sodium channels. Circ Res 102:86-94. CrossRef Medline
3. Aman TK, Raman IM (2007) Subunit dependence of Na channel slow inactivation and open channel block in cerebellar neurons. Biophys J 92: 1938-1951. CrossRef Medline
4. Aman TK, Raman IM (2010) Inwardly permeating Na ions generate the voltage dependence of resurgent Na current in cerebellar Purkinje neurons. J Neurosci 30:5629-5634. CrossRef Medline
5. Bant JS, Raman IM (2010) Control of transient, resurgent, and persistent current by open-channel block by Na channel β4 in cultured cerebellar granule neurons. Proc Natl Acad Sci U S A 107:12357-12362. CrossRef Medline
6. Bean BP, Cohen CJ, Tsien RW (1983) Lidocaine block of cardiac sodium channels. J Gen Physiol 81:613-642. CrossRef Medline
7. Brand S, Seeger T, Alzheimer C (2000) Enhancement of persistent Na+ current by sea anemone toxin (ATX II) exerts dual action on hippocampal excitability. Eur J Neurosci 12:2387-2396. CrossRef Medline
8. Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829-4843. Medline
9. Cahalan MD (1978) Local anesthetic block of sodium channels in normal and pronase-treated squid giant axons. Biophys J 2:285-311. CrossRef Medline
10. Cahalan MD, Almers W (1979) Interactions between quaternary lidocaine, the sodium channel gates, and tetrodotoxin. Biophys J 27:39-55. CrossRef Medline
11. Castelli L, Nigro MJ, Magistretti J (2007a) Analysis of resurgent sodium current expression in rat parahippocampal cortices and hippocampal formation. Brain Res 1163:44-55. CrossRef Medline
12. + current in pyramidal neurones of rat perirhinal cortex: axonal location of channels and contribution to depolarizing drive during repetitive firing. J Physiol 582:1179-1193. CrossRef Medline
13. Castillo C, Piernavieja C, Recio-Pinto E (1996) Anemone toxin II unmasks two conductance states in neuronal sodium channels. Brain Res 733:231-242. CrossRef Medline
14. Catterall WA (2002) Molecular mechanisms of gating and drug block of sodium channels. Novartis Found Symp 241:206-218. Medline
15. Chahine M, Chen LQ, Barchi RL, Kallen RG, Horn R (1992) Lidocaine block of human heart sodium channels expressed in Xenopus oocytes. J Mol Cell Cardiol 24:1231-1236. CrossRef Medline
16. Cummins TR, Dib-Hajj SD, Herzog RI, Waxman SG (2005) Nav1.6 channels generate resurgent sodium currents in spinal sensory neurons. FEBS Lett 579:2166-2170. CrossRef Medline
17. Ding S, Wei W, Zhou FM (2011) Molecular and functional differences in voltage-activated sodium currents between GABA projection neurons and dopamine neurons in the substantia nigra. J Neurophysiol 106:3019-3034. CrossRef Medline
18. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120. CrossRef Medline
19. el-Sherif N, Fozzard HA, Hanck DA (1992) Dose-dependent modulation of the cardiac sodium channel by sea anemone toxin ATXII. Circ Res 70: 285-301. CrossRef Medline
20. Enomoto A, Han JM, Hsiao CF, Wu N, Chandler SH (2006) Participation of sodium currents in burst generation and control of membrane excitability in mesencephalic trigeminal neurons. J Neurosci 26:3412-3422. CrossRef Medline
21. Gittis AH, du Lac S (2008) Similar properties of transient, persistent, and resurgent Na currents in GABAergic and non-GABAergic vestibular nucleus neurons. J Neurophysiol 99:2060-2065. CrossRef Medline
22. V1.6-null Purkinje neurons by slowing sodium channel inactivation with β-pompilidotoxin. J Neurosci 24:35-42. CrossRef Medline
23. Grieco TM, Malhotra JD, Chen C, Isom LL, Raman IM (2005) Openchannel block by the cytoplasmic tail of sodium channel β4 as a mechanism for resurgent sodium current. Neuron 45:233-244. CrossRef Medline
24. Hanck DA, Sheets MF (2007) Site-3 toxins and cardiac sodium channels. Toxicon 49:181-193. CrossRef Medline
25. Hille B (1977) Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 69:497-515. CrossRef Medline
26. Jarecki BW, Piekarz AD, Jackson JO 2nd, Cummins TR (2010) Human voltage-gated sodium channel mutations that cause inherited neuronal and muscle channelopathies increase resurgent sodium currents. J Clin Invest 120:369-378. CrossRef Medline
27. Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-4912. Medline
28. Kim JH, Kushmerick C, von Gersdorff H (2010) Presynaptic resurgent Na currents sculpt the action potential waveform and increase firing reliability at a CNS nerve terminal. J Neurosci 30:15479-15490. CrossRef Medline
29. Leão RN, Naves MM, Leão KE, Walmsley B (2006) Altered sodium currents in auditory neurons of congenitally deaf mice. Eur J Neurosci 24:1137-1146. CrossRef Medline
30. Lee AM, Simon RA, Aman TK, Raman IM (2006) Effect of Na channel β4 cytoplasmic tail on resurgent current and firing in CA3 hippocampal cells. Program No. 130.3. 2006 Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience.
31. Lewis AH, Raman IM (2011) Cross-species conservation of open-channel block by Na channel β4 peptides reveals structural features required for resurgent Na current. J Neurosci 31:11527-11536. CrossRef Medline
32. Mantegazza M, Franceschetti S, Avanzini G. (1998) Anemone toxin (ATX II)-induced increase in persistent sodium current: effects on the firing properties of rat neocortical pyramidal neurones. J Physiol 507:105-116. CrossRef Medline
33. Meeks JP, Mennerick S (2007) Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97:3460-3472. CrossRef Medline
34. Mercer JN, Chan CS, Tkatch T, Held J, Surmeier DJ (2007) Nav1.6 sodium channels are critical to pacemaking and fast spiking in globus pallidus neurons. J Neurosci 27:13552-13566. CrossRef Medline
35. Miyawaki T, Tsubokawa H, Yokota H, Oguro K, Konno K, Masuzawa T, Kawai N (2002) Differential effects of novel wasp toxin on rat hippocampal interneurons. Neurosci Lett 328:25-28. CrossRef Medline
36. Muroi Y, Chanda B (2009) Local anesthetics disrupt energetic coupling between the voltage-sensing segments of a sodium channel. J Gen Physiol 133:1-15. CrossRef Medline
37. Nagy K (1987) Subconductance states of single sodium channels modified by chloramine-T and sea anemone toxin in neuroblastoma cells. Eur Biophys J 15:129-132. CrossRef Medline
38. Nayak TK, Harinath S, Nama S, Somasundaram K, Sikdar SK (2009) Inhibition of human two-pore domain K+ channel TREK1 by local anesthetic lidocaine: negative cooperativity and half-of-sites saturation kinetics. Mol Pharmacol 76:903-917. CrossRef Medline
39. Oliveira JS, Redaelli E, Zaharenko AJ, Cassulini RR, Konno K, Pimenta DC, Freitas JC, Clare JJ, Wanke E (2004) Binding specificity of sea anemone toxins to Nav 1.1-1.6 sodium channels: unexpected contributions from differences in the IV/S3-S4 outer loop. J Biol Chem 279:33323-33335. CrossRef Medline
40. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353-358. CrossRef Medline
41. Putrenko I, Schwarz SK (2011) Lidocaine blocks the hyperpolarizationactivated mixed cation current, I(h), in rat thalamocortical neurons. Anesthesiology 115:822-835. CrossRef Medline
42. Ragsdale DS, McPhee JC, Scheuer T, Catterall WA (1994) Molecular determinants of state-dependent block of Na+ channels by local anesthetics. Science 265:1724-1728. CrossRef Medline
43. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526. Medline
44. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674. Medline
45. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80:729-737. CrossRef Medline
46. Raman IM, Trussell LO (1995) Concentration-jump analysis of voltagedependent conductances activated by glutamate and kainate in neurons of the avian cochlear nucleus. Biophys J 69:1868-1879. CrossRef Medline
47. Raman IM, Sprunger LK, Meisler MH, Bean BP (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19:881-891. CrossRef Medline
48. Sheets MF, Hanck DA (2003) Molecular action of lidocaine on the voltage sensors of sodium channels. J Gen Physiol 121:163-175. CrossRef Medline
49. Sheets MF, Hanck DA (2007) Outward stabilization of the S4 segments in domains III and IV enhances lidocaine block of sodium channels. J Physiol 582:317-334. CrossRef Medline
50. Sheets MF, Kyle JW, Kallen RG, Hanck DA (1999) The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys J 77:747-757. CrossRef Medline
51. Strichartz GR (1973) The inhibition of sodium currents in myelinated nerve by quaternary derivatives of lidocaine. J Gen Physiol 62:37-57. CrossRef Medline
52. Vβ4 peptide-mediated resurgent sodium currents. J Physiol 589:597-608. CrossRef Medline
53. Trellakis S, Benzenberg D, Urban BW, Friederich P (2006) Differential lidocaine sensitivity of human voltage-gated potassium channels relevant to the auditory system. Otol Neurotol 27:117-123. CrossRef Medline
54. Vedantham V, Cannon SC (1999) The position of the fast-inactivation gate during lidocaine block of voltage-gated Na+ channels. J Gen Physiol 113:7-16. CrossRef Medline
55. Wang GK, Brodwick MS, Eaton DC, Strichartz GR (1987) Inhibition of sodium currents by local anesthetics in chloramine-T-treated squid axons: the role of channel activation. J Gen Physiol 89:645-667. CrossRef Medline
56. Wang GK, Edrich T, Wang SY (2006) Time-dependent block and resurgent tail currents induced by mouse β4(154-167) peptide in cardiac Na channels. J Gen Physiol 127:277-289. CrossRef Medline
57. Wright SN, Wang SY, Kallen RG, Wang GK (1997) Differences in steadystate inactivation between Na channel isoforms affect local anesthetic binding affinity. Biophys J 73:779-788. CrossRef Medline
58. Zhou W, Goldin AL (2004) Use-dependent potentiation of the Nav1.6 sodium channel. Biophys J 87:3862-3872. CrossRef Medline