Lidocaine block of neonatal Nav1.3 is differentially modulated by co-expression of β1 and β3 subunits

European Journal of Pharmacology

Volumn 467, Issue 1-3, 2003, Pages 23-30

  Lenkowski, Paul W ^a   Shah, Bhaval S ^b   Dinn, Andrew E ^a   Lee, Kevin ^b   Patel, Manoj K ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Lidocaine; Nav1.3 Na+ channel; Neonatal; Oocyte; Subunit

Indexed keywords

LIDOCAINE; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BETA CHAIN; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SODIUM CURRENT; XENOPUS LAEVIS;

EID: 0037466471     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-2999(03)01595-4     Document Type: Article

References (41)

1. Aronica E., Yankaya B., Troost D., van Vliet E.A., Lopes da Silva F.H., Gorter J.A. Induction of neonatal sodium channel II and III alpha-isoform mRNAs in neurons and microglia after status epilepticus in the rat hippocampus. Eur. J. Neurosci. 13:2001;1261-1266.
2. Bach F.W., Jensen T.S., Kastrup J., Stigsby B., Dejgard A. The effect of intravenous lidocaine on nociceptive processing in diabetic neuropathy. Pain. 40:1990;29-34.
3. Balser J.R., Nuss H.B., Romashko D.N., Marban E., Tomaselli G.F. Functional consequences of lidocaine binding to slow-inactivated sodium channels. J. Gen. Physiol. 107:1996;643-658.
4. Bean B.P., Cohen C.J., Tsien R.W. Lidocaine block of cardiac sodium channels. J. Gen. Physiol. 81:1983;613-642.
5. + channels. Modification of block by alterations in the alpha-subunit III-IV interdomain. Circ. Res. 77:1995;584-592.
6. Bottaro D., Shepro D., Peterson S., Hechtman H.B. Serotonin, norepinephrine, and histamine mediation of endothelial cell barrier function in vitro. J. Cell. Physiol. 128:1986;189-194.
7. Chen Z., Ong B.H., Kambouris N.G., Marban E., Tomaselli G.F., Balser J.R. Lidocaine induces a slow inactivated state in rat skeletal muscle sodium channels. J. Physiol. 524(Pt 1):2000;37-49.
8. Cummins T.R., Waxman S.G. Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J. Neurosci. 17:1997;3503-3514.
9. Dib-Hajj S.D., Fjell J., Cummins T.R., Zheng Z., Fried K., LaMotte R., Black J.A., Waxman S.G. Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain. Pain. 83:1999;591-600.
10. Gastaldi M., Bartolomei F., Massacrier A., Planells R., Robaglia-Schlupp A., Cau P. Increase in mRNAs encoding neonatal II and III sodium channel alpha-isoforms during kainate-induced seizures in adult rat hippocampus. Brain Res., Mol. Brain Res. 44:1997;179-190.
11. Gustafson T.A., Clevinger E.C., O'Neill T.J., Yarowsky P.J., Krueger B.K. Mutually exclusive exon splicing of type III brain sodium channel alpha subunit RNA generates developmentally regulated isoforms in rat brain. J. Biol. Chem. 268:1993;18648-18653.
12. Hanck D.A., Makielski J.C., Sheets M.F. Kinetic effects of quaternary lidocaine block of cardiac sodium channels: a gating current study. J. Gen. Physiol. 103:1994;19-43.
13. Hanck D.A., Makielski J.C., Sheets M.F. Lidocaine alters activation gating of cardiac Na channels. Pflugers Arch. 439:2000;814-821.
14. Hille B. Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J. Gen. Physiol. 69:1977;497-515.
15. Hondeghem L.M., Katzung B.G. Time- and voltage-dependent interactions of antiarrhythmic drugs with cardiac sodium channels. Biochim. Biophys. Acta. 472:1977;373-398.
16. Isom L.L., De Jongh K.S., Patton D.E., Reber B.F., Offord J., Charbonneau H., Walsh K., Goldin A.L., Catterall W.A. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science. 256:1992;839-842.
17. Isom L.L., Ragsdale D.S., De Jongh K.S., Westenbroek R.E., Reber B.F., Scheuer T., Catterall W.A. Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell. 83:1995;433-442.
18. Kambouris N.G., Hastings L.A., Stepanovic S., Marban E., Tomaselli G.F., Balser J.R. Mechanistic link between lidocaine block and inactivation probed by outer pore mutations in the rat micro1 skeletal muscle sodium channel. J. Physiol. 512(Pt 3):1998;693-705.
19. Kastrup J., Petersen P., Dejgard A., Angelo H.R., Hilsted J. Intravenous lidocaine infusion - a new treatment of chronic painful diabetic neuropathy? Pain. 28:1987;69-75.
20. Kim C.H., Oh Y., Chung J.M., Chung K. The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Brain Res., Mol. Brain Res. 95:2001;153-161.
21. Koppert W., Ostermeier N., Sittl R., Weidner C., Schmelz M. Low-dose lidocaine reduces secondary hyperalgesia by a central mode of action. Pain. 85:2000;217-224.
22. Makielski J.C., Limberis J.T., Chang S.Y., Fan Z., Kyle J.W. Coexpression of beta 1 with cardiac sodium channel alpha subunits in oocytes decreases lidocaine block. Mol. Pharmacol. 49:1996;30-39.
23. Makielski J.C., Limberis J., Fan Z., Kyle J.W. Intrinsic lidocaine affinity for Na channels expressed in Xenopus oocytes depends on alpha (hH1 vs. rSkM1) and beta 1 subunits. Cardiovasc. Res. 42:1999;503-509.
24. + channels. J. Neurosci. 16:1996;7117-7127.
25. Mao J., Chen L.L. Systemic lidocaine for neuropathic pain relief. Pain. 87:2000;7-17.
26. + channel function in the extracellular domain of the beta1 subunit. J. Biol. Chem. 273:1998;3954-3962.
27. Morgan K., Stevens E.B., Shah B., Cox P.J., Dixon A.K., Lee K., Pinnock R.D., Hughes J., Richardson P.J., Mizuguchi K., Jackson A.P. Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl. Acad. Sci. U. S. A. 97:2000;2308-2313.
28. Nuss H.B., Tomaselli G.F., Marban E. Cardiac sodium channels (hH1) are intrinsically more sensitive to block by lidocaine than are skeletal muscle (mu 1) channels. J. Gen. Physiol. 106:1995;1193-1209.
29. Nuss H.B., Kambouris N.G., Marban E., Tomaselli G.F., Balser J.R. Isoform-specific lidocaine block of sodium channels explained by differences in gating. Biophys. J. 78:2000;200-210.
30. Patton D.E., Isom L.L., Catterall W.A., Goldin A.L. The adult rat brain beta 1 subunit modifies activation and inactivation gating of multiple sodium channel alpha subunits. J. Biol. Chem. 269:1994;17649-17655.
31. Qu Y., Rogers J.C., Chen S.F., McCormick K.A., Scheuer T., Catterall W.A. Functional roles of the extracellular segments of the sodium channel alpha subunit in voltage-dependent gating and modulation by beta1 subunits. J. Biol. Chem. 274:1999;32647-32654.
32. + channels by local anesthetics. Science. 265:1994;1724-1728.
33. Roy M.L., Narahashi T. Differential properties of tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels in rat dorsal root ganglion neurons. J. Neurosci. 12:1992;2104-2111.
34. Shah B.S., Stevens E.B., Gonzalez M.I., Bramwell S., Pinnock R.D., Lee K., Dixon A.K. Beta3, a novel auxiliary subunit for the voltage-gated sodium channel, is expressed preferentially in sensory neurons and is upregulated in the chronic constriction injury model of neuropathic pain. Eur. J. Neurosci. 12:2000;3985-3990.
35. Shah B.S., Stevens E.B., Pinnock R.D., Dixon A.K., Lee K. Developmental expression of the novel voltage-gated sodium channel auxiliary subunit beta3, in rat CNS. J. Physiol. 534:2001;763-776.
36. Strichartz G.R., Zhou Z., Sinnott C., Khodorova A. Therapeutic concentrations of local anaesthetics unveil the potential role of sodium channels in neuropathic pain. Novartis Found. Symp. 241:2002;189-201.
37. Sunami A., Dudley S.C. Jr., Fozzard H.A. Sodium channel selectivity filter regulates antiarrhythmic drug binding. Proc. Natl. Acad. Sci. U. S. A. 94:1997;14126-14131.
38. Sunami A., Glaaser I.W., Fozzard H.A. A critical residue for isoform difference in tetrodotoxin affinity is a molecular determinant of the external access path for local anesthetics in the cardiac sodium channel. Proc. Natl. Acad. Sci. U. S. A. 97:2000;2326-2331.
39. + channels. J. Gen. Physiol. 113:1999;7-16.
40. Waxman S.G., Kocsis J.D., Black J.A. Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J. Neurophysiol. 72:1994;466-470.
41. Whitaker W.R., Faull R.L., Dragunow M., Mee E.W., Emson P.C., Clare J.J. Changes in the mRNAs encoding voltage-gated sodium channel types II and III in human epileptic hippocampus. Neuroscience. 106:2001;275-285.