Membrane permeable local anesthetics modulate NaV1.5 mechanosensitivity

Channels

Volumn 6, Issue 4, 2012, Pages 308-316

  Beyder, Arthur ^a   Strege, Peter R ^a   Bernard, Cheryl ^a   Farrugia, Gianrico ^a  

^a MAYO CLINIC   (United States)

Author keywords

Benzocaine; Ion channel; Lidocaine; Mechanosensitive; Pressure; QX 314; Sodium channel; Stretch; Voltage gated

Indexed keywords

BENZOCAINE; LIDOCAINE; LIDOCAINE ETHOBROMIDE; SODIUM CHANNEL NAV1.5; DRUG DERIVATIVE; LOCAL ANESTHETIC AGENT; QX-314; SCN5A PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CELL ADHESION; CELL STRAIN HEK293; COMPETITIVE INHIBITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROPHOBICITY; HYPERPOLARIZATION; LOCAL ANESTHESIA; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; MOLECULAR INTERACTION; PRESSURE; PROTEIN EXPRESSION; WILD TYPE; AMINO ACID SUBSTITUTION; CELL MEMBRANE PERMEABILITY; DRUG EFFECT; ELECTROPHYSIOLOGY; GENETIC TRANSFECTION; GENETICS; HYDROSTATIC PRESSURE; METABOLISM; PATCH CLAMP;

AMINO ACID SUBSTITUTION; ANESTHETICS, LOCAL; BENZOCAINE; BINDING SITES; CELL MEMBRANE PERMEABILITY; ELECTROPHYSIOLOGICAL PHENOMENA; HEK293 CELLS; HUMANS; HYDROSTATIC PRESSURE; LIDOCAINE; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PATCH-CLAMP TECHNIQUES; TRANSFECTION;

EID: 84865286004     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.21202     Document Type: Article

References (50)

1. Gellens ME, George AL Jr., Chen LQ, Chahine M, Horn R, Barchi RL, et al. Primary structure and functional expression of the human cardiac tetrodotoxin-insensitive voltage-dependent sodium channel. Proc Natl Acad Sci U S A 1992; 89:554-8; PMID:1309946; http://dx.doi.org/10.1073/pnas.89.2.554.
2. Ou Y, Gibbons SJ, Miller SM, Strege PR, Rich A, Distad MA, et al. SCN5A is expressed in human jejunal circular smooth muscle cells. Neurogastroenterol Motil 2002; 14:477-86; PMID:12358675; http://dx.doi.org/10.1046/j.1365-2982. 2002.00348.x.
3. Bennett PB, Yazawa K, Makita N, George AL Jr. Molecular mechanism for an inherited cardiac arrhythmia. Nature 1995; 376:683-5; PMID:7651517; http://dx.doi.org/10.1038/376683a0.
4. Farrugia G. Ionic conductances in gastrointestinal smooth muscles and interstitial cells of Cajal. Annu Rev Physiol 1999; 61:45-84; PMID:10099682; http://dx.doi.org/10.1146/annurev.physiol.61.1.45.
5. Strege PR, Mazzone A, Kraichely RE, Sha L, Holm AN, Ou Y, et al. Species dependent expression of intestinal smooth muscle mechanosensitive sodium channels. Neurogastroenterol Motil 2007; 19:135-43; PMID:17244168; http://dx.doi.org/10.1111/j.1365-2982.2006.00844.x.
6. Strege PR, Ou Y, Sha L, Rich A, Gibbons SJ, Szurszewski JH, et al. Sodium current in human intestinal interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 2003; 285:G1111-21; PMID:12893628.
7. Locke GR 3rd, Ackerman MJ, Zinsmeister AR, Thapa P, Farrugia G. Gastrointestinal symptoms in families of patients with an SCN5A-encoded cardiac channelopathy: evidence of an intestinal channelopathy. Am J Gastroenterol 2006; 101:1299-304; PMID:16771953; http://dx.doi.org/10.1111/j.1572-0241.2006.00507. x.
8. Saito YA, Strege PR, Tester DJ, Locke GR 3rd, Talley NJ, Bernard CE, et al. Sodium channel mutation in irritable bowel syndrome: evidence for an ion channelopathy. Am J Physiol Gastrointest Liver Physiol 2009; 296:G211-8; PMID:19056759; http://dx.doi.org/10.1152/ajpgi.90571.2008.
9. Morris CE, Juranka PF. Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch. Biophys J 2007; 93:822-33; PMID:17496023; http://dx.doi.org/10.1529/biophysj.106.101246.
10. Beyder A, Rae JL, Bernard C, Strege PR, Sachs F, Farrugia G. Mechanosensitivity of Nav1.5, a voltage-sensitive sodium channel. J Physiol 2010; 588:4969-85; PMID:21041530; http://dx.doi.org/10.1113/jphysiol.2010. 199034.
11. Banderali U, Juranka PF, Clark RB, Giles WR, Morris CE. Impaired stretch modulation in potentially lethal cardiac sodium channel mutants. Channels (Austin) 2010; 4:12-21; PMID:20090423; http://dx.doi.org/10.4161/chan.4.1.10260.
12. Ou Y, Strege P, Miller SM, Makielski J, Ackerman M, Gibbons SJ, et al. Syntrophin gamma 2 regulates SCN5A gating by a PDZ domain-mediated interaction. J Biol Chem 2003; 278:1915-23; PMID:12429735; http://dx.doi.org/10.1074/jbc. M209938200.
13. Strege PR, Holm AN, Rich A, Miller SM, Ou Y, Sarr MG, et al. Cytoskeletal modulation of sodium current in human jejunal circular smooth muscle cells. Am J Physiol Cell Physiol 2003; 284:C60-6; PMID:12475760.
14. Shcherbatko A, Ono F, Mandel G, Brehm P. Voltage-dependent sodium channel function is regulated through membrane mechanics. Biophys J 1999; 77:1945-59; PMID:10512815; http://dx.doi.org/10.1016/S0006-3495(99)77036-0.
15. Wang JA, Lin W, Morris T, Banderali U, Juranka PF, Morris CE. Membrane trauma and Na+ leak from Nav1.6 channels. Am J Physiol Cell Physiol 2009; 297:C823-34; PMID:19657055; http://dx.doi.org/10.1152/ajpcell.00505.2008.
16. Tabarean IV, Juranka P, Morris CE. Membrane stretch affects gating modes of a skeletal muscle sodium channel. Biophys J 1999; 77:758-74; PMID:10423424; http://dx.doi.org/10.1016/S0006-3495(99)76930-4.
17. Lundbaek JA, Birn P, Hansen AJ, Søgaard R, Nielsen C, Girshman J, et al. Regulation of sodium channel function by bilayer elasticity: the importance of hydrophobic coupling. Effects of Micelle-forming amphiphiles and cholesterol. J Gen Physiol 2004; 123:599-621; PMID:15111647; http://dx.doi.org/10.1085/jgp.200308996.
18. Lundbaek JA, Koeppe RE 2 nd, Andersen OS. Amphiphile regulation of ion channel function by changes in the bilayer spring constant. Proc Natl Acad Sci U S A 2010; 107:15427-30; PMID:20713738; http://dx.doi.org/10.1073/pnas. 1007455107.
19. Fredj S, Sampson KJ, Liu H, Kass RS. Molecular basis of ranolazine block of LQT-3 mutant sodium channels: evidence for site of action. Br J Pharmacol 2006; 148:16-24; PMID:16520744; http://dx.doi.org/10.1038/sj.bjp.0706709.
20. Beyder A, Strege PR, Reyes S, Bernard CE, Terzic A, Makielski J, et al. Ranolazine decreases mechanosensitivity of the voltage-gated sodium ion channel NaV1.5: a novel mechanism of drug action. Circulation 2012; 125:2698-706; PMID:22565935; http://dx.doi.org/10.1161/CIRCULATIONAHA.112.094714.
21. Arnadóttir J, Chalfie M. Eukaryotic mechanosensitive channels. Annu Rev Biophys 2010; 39:111-37; PMID:20192782; http://dx.doi.org/10.1146/ annurev.biophys.37.032807.1258 36.
22. Suchyna TM, Besch SR, Sachs F. Dynamic regulation of mechanosensitive channels: capacitance used to monitor patch tension in real time. Phys Biol 2004; 1:1-18; PMID:16204817; http://dx.doi.org/10.1088/1478-3967/1/1/001.
23. Gu CX, Juranka PF, Morris CE. Stretch-activation and stretch-inactivation of Shaker-IR, a voltage-gated K+ channel. Biophys J 2001; 80:2678-93; PMID:11371444; http://dx.doi.org/10.1016/S0006-3495(01)76237-6.
24. Hille B. Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 1977; 69:497-515; PMID:300786; http://dx.doi.org/10.1085/jgp.69.4.497.
25. Nau C, Wang GK. Interactions of local anesthetics with voltage-gated Na+ channels. J Membr Biol 2004; 201:1-8; PMID:15635807; http://dx.doi.org/10.1007/ s00232-004-0702-y.
26. Sheets MF, Fozzard HA, Lipkind GM, Hanck DA. Sodium channel molecular conformations and antiarrhythmic drug affinity. Trends Cardiovasc Med 2010; 20:16-21; PMID:20685573; http://dx.doi.org/10.1016/j.tcm.2010.03.002.
27. Hanck DA, Nikitina E, McNulty MM, Fozzard HA, Lipkind GM, Sheets MF. Using lidocaine and benzocaine to link sodium channel molecular conformations to state-dependent antiarrhythmic drug affinity. Circ Res 2009; 105:492-9; PMID:19661462; http://dx.doi.org/10.1161/CIRCRESAHA.109.198572.
28. Pless SA, Galpin JD, Frankel A, Ahern CA. Molecular basis for class Ib anti-arrhythmic inhibition of cardiac sodium channels. Nat Commun 2011; 2:351; PMID:21673672; http://dx.doi.org/10.1038/ncomms1351.
29. Mike A, Lukacs P. The enigmatic drug binding site for sodium channel inhibitors. Curr Mol Pharmacol 2010; 3:129-44; PMID:20565383.
30. Carboni M, Zhang ZS, Neplioueva V, Starmer CF, Grant AO. Slow sodium channel inactivation and use-dependent block modulated by the same domain IV S6 residue. J Membr Biol 2005; 207:107-17; PMID:16477531; http://dx.doi.org/10. 1007/s00232-005-0805-0.
31. Qu Y, Rogers J, Tanada T, Scheuer T, Catterall WA. Molecular determinants of drug access to the receptor site for antiarrhythmic drugs in the cardiac Na+ channel. Proc Natl Acad Sci U S A 1995; 92:11839-43; PMID:8524860; http://dx.doi.org/10.1073/pnas.92.25.11839.
32. Morris CE, Juranka PF, Lin W, Morris TJ, Laitko U. Studying the mechanosensitivity of voltage-gated channels using oocyte patches. Methods Mol Biol 2006; 322:315-29; PMID:16739733; http://dx.doi.org/10.1007/978-1-59745-000- 3-22.
33. Li GR, Baumgarten CM. Modulation of cardiac Na(+) current by gadolinium, a blocker of stretch-induced arrhythmias. Am J Physiol Heart Circ Physiol 2001; 280:H272-9; PMID:11123242.
34. Ursell T, Agrawal A, Phillips R. Lipid bilayer mechanics in a pipette with glass-bilayer adhesion. Biophys J 2011; 101:1913-20; PMID:22004745; http://dx.doi.org/10.1016/j.bpj.2011.08.057.
35. Bae C, Markin V, Suchyna T, Sachs F. Modeling ion channels in the gigaseal. Biophys J 2011; 101:2645-51; PMID:22261052; http://dx.doi.org/10.1016/ j.bpj.2011.11.002.
36. Quan C, Mok WM, Wang GK. Use-dependent inhibition of Na+ currents by benzocaine homologs. Biophys J 1996; 70:194-201; PMID:8770198; http://dx.doi.org/10.1016/S0006-3495(96)79563-2.
37. Schmidt D, MacKinnon R. Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc Natl Acad Sci U S A 2008; 105:19276-81; PMID:19050073; http://dx.doi.org/ 10.1073/pnas.0810187105.
38. Kraichely RE, Strege PR, Sarr MG, Kendrick ML, Farrugia G. Lysophosphatidyl choline modulates mechanosensitive L-type Ca2+ current in circular smooth muscle cells from human jejunum. Am J Physiol Gastrointest Liver Physiol 2009; 296:G833-9; PMID:19179622; http://dx.doi.org/10.1152/ajpgi.90610. 2008.
39. Hendry BM, Elliott JR, Haydon DA. Further evidence that membrane thickness influences voltage-gated sodium channels. Biophys J 1985; 47:841-5; PMID:2410046; http://dx.doi.org/10.1016/S0006-3495(85)83988-6.
40. Jogini V, Roux B. Dynamics of the Kv1.2 voltage-gated K+ channel in a membrane environment. Biophys J 2007; 93:3070-82; PMID:17704179; http://dx.doi.org/10.1529/biophysj.107.112540.
41. Conti F, Fioravanti R, Segal JR, Stühmer W. Pressure dependence of the sodium currents of squid giant axon. J Membr Biol 1982; 69:23-34; PMID:7120361; http://dx.doi.org/10.1007/BF01871238.
42. Pinto LM, Yokaichiya DK, Fraceto LF, de Paula E. Interaction of benzocaine with model membranes. Biophys Chem 2000; 87:213-23; PMID:11099183; http://dx.doi.org/10.1016/S0301-4622(00)00196-4.
43. Högberg CJ, Maliniak A, Lyubartsev AP. Dynamical and structural properties of charged and uncharged lidocaine in a lipid bilayer. Biophys Chem 2007; 125:416-24; PMID:17112652; http://dx.doi.org/10.1016/j.bpc.2006.10.005.
44. Högberg CJ, Lyubartsev AP. Effect of local anesthetic lidocaine on electrostatic properties of a lipid bilayer. Biophys J 2008; 94:525-31; PMID:17720733; http://dx.doi.org/10.1529/biophysj.107.104208.
45. Zhang J, Hadlock T, Gent A, Strichartz GR. Tetracaine-membrane interactions: effects of lipid composition and phase on drug partitioning, location, and ionization. Biophys J 2007; 92:3988-4001; PMID:17351014; http://dx.doi.org/10.1529/biophysj.106.102434.
46. Xu Y, Ramu Y, Lu Z. Removal of phospho-head groups of membrane lipids immobilizes voltage sensors of K+ channels. Nature 2008; 451:826-9; PMID:18273018; http://dx.doi.org/10.1038/nature06618.
47. Payandeh J, Scheuer T, Zheng N, Catterall WA. The crystal structure of a voltage-gated sodium channel. Nature 2011; 475:353-8; PMID:21743477; http://dx.doi.org/10.1038/nature10238.
48. Fraceto LF, Oyama S Jr., Nakaie CR, Spisni A, de Paula E, Pertinhez TA. Interaction of local anesthetics with a peptide encompassing the IV/S4-S5 linker of the Na+ channel. Biophys Chem 2006; 123:29-39; PMID:16687202; http://dx.doi.org/10.1016/j.bpc.2006.03.010.
49. Morris CE. Voltage-gated channel mechanosensitivity: fact or friction? Front Physiol 2011; 2:25; PMID:21660289; http://dx.doi.org/10.3389/fphys.2011. 00025.
50. Besch SR, Suchyna T, Sachs F. High-speed pressure clamp. Pflugers Arch 2002; 445:161-6; PMID:12397401; http://dx.doi.org/10.1007/s00424-002-0903-0.