2,175
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Capsaicin as an amphipathic modulator of NaV1.5 mechanosensitivity

ORCID Icon, , , , & ORCID Icon
Pages 9-26 | Received 01 Oct 2021, Accepted 03 Jan 2022, Published online: 12 Apr 2022

References

  • Makielski JC, Ye B, Valdivia CR, et al. A ubiquitous splice variant and a common polymorphism affect heterologous expression of recombinant human SCN5A heart sodium channels. Circ Res. 2003;93(9):821–828.
  • Hille B. Ionic channels in excitable membranes. Current problems and biophysical approaches. Biophys J. 1978;22(2):283–294.
  • Gellens ME, George AL Jr., Chen LQ, 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(2):554–558.
  • Farrugia G. Ionic conductances in gastrointestinal smooth muscles and interstitial cells of Cajal. Annu Rev Physiol. 1999;61(1):45–84.
  • Beyder A, Rae JL, Bernard C, et al. Mechanosensitivity of Nav1.5, a voltage-sensitive sodium channel. J Physiol. 2010;588(24):4969–4985.
  • Morris CE, Juranka PF. Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch. Biophys J. 2007;93(3):822–833.
  • Neshatian L, Strege PR, Rhee PL, et al. Ranolazine inhibits voltage-gated mechanosensitive sodium channels in human colon circular smooth muscle cells. Am J Physiol Gastrointest Liver Physiol. 2015;309(6):G506–512
  • Strege PR, Ou Y, Sha L, et al. Sodium current in human intestinal interstitial cells of Cajal. Am. J. Physiol. Gastrointest. Liver Physiol. 2003;285(6):G1111–1121
  • Strege PR, Mazzone A, Kraichely RE, et al. Species dependent expression of intestinal smooth muscle mechanosensitive sodium channels. Neurogastroenterol Motil. 2007;19(2):135–143.
  • Beyder A, Farrugia G. Ion channelopathies in functional GI disorders. Am J Physiol: Gastrointes Liver Physiol. 2016;311:G581–G586.
  • Kass RS. The channelopathies: novel insights into molecular and genetic mechanisms of human disease. J Clin Invest. 2005;115(8):1986–1989.
  • Marban E. Cardiac channelopathies. Nature. 2002;415(6868):213–218.
  • Beyder A, Gibbons SJ, Mazzone A, et al. Expression and function of the Scn5a-encoded voltage-gated sodium channel NaV1.5 in the rat jejunum. Neurogastroenterol Motil. 2016;28(1):64–73.
  • Banderali U, Juranka PF, Clark RB, et al. Impaired stretch modulation in potentially lethal cardiac sodium channel mutants. Channels (Austin). 2010;4(1):12–21.
  • Beyder A, Mazzone A, Strege PR, et al. Loss-of-function of the voltage-gated sodium channel NaV1.5 (channelopathies) in patients with irritable bowel syndrome. Gastroenterology. 2014;146(7):1659–1668.
  • Saito YA, Strege PR, Tester DJ, et al. Sodium channel mutation in irritable bowel syndrome: evidence for an ion channelopathy. Am. J. Physiol. Gastrointest. Liver Physiol. 2009;296(2):G211–218
  • Strege PR, Mercado-Perez A, Mazzone A, et al. SCN5A mutation G615E results in NaV1.5 voltage-gated sodium channels with normal voltage-dependent function yet loss of mechanosensitivity. Channels (Austin). 2019;13(1):287–298.
  • Strege PR, Mazzone A, Bernard CE, et al. Irritable bowel syndrome (IBS) patients have SCN5A channelopathies that lead to decreased NaV1.5 current and mechanosensitivity. Am J Physiol Gastrointest Liver Physiol. 2017;314(4):G494–G503.
  • Beyder A, Mazzone A, Strege PR, et al. Loss-of-function of the voltage-gated sodium channel NaV1.5 (channelopathies) in patients with irritable bowel syndrome. Gastroenterology. 2014;146(7):1659–1668.
  • Bagal SK, Brown AD, Cox PJ, et al. Ion channels as therapeutic targets: a drug discovery perspective. J Med Chem. 2013;56(3):593–624.
  • Beyder A, Strege PR, Bernard C, et al. Membrane permeable local anesthetics modulate Na(V)1.5 mechanosensitivity. Channels (Austin). 2012;6(4):308–316.
  • Beyder A, Strege PR, Reyes S, et al. Ranolazine Decreases Mechanosensitivity of the Voltage-Gated Sodium Ion Channel NaV1.5. Circulation. 2012;125(22):2698–2706.
  • Sukharev S, Sachs F. Molecular force transduction by ion channels: diversity and unifying principles. J Cell Sci. 2012;125(Pt 13):3075–3083.
  • Kraichely RE, Farrugia G. Mechanosensitive ion channels in interstitial cells of Cajal and smooth muscle of the gastrointestinal tract. Neurogastroenterol Motil. 2007;19(4):245–252.
  • Strege PR, Holm AN, Rich A, et al. Cytoskeletal modulation of sodium current in human jejunal circular smooth muscle cells. Am J Physiol Cell Physiol. 2003;284(1):C60–66.
  • Beyder A, Strege PR, Reyes S, et al. Ranolazine Decreases Mechanosensitivity of the Voltage-Gated Sodium Ion Channel Na(V)1.5. Circulation. 2012;125(22):2698–2706.
  • Antzelevitch C, Burashnikov A, Sicouri S, et al. Electrophysiologic basis for the antiarrhythmic actions of ranolazine. Heart Rhythm. 2011;8(8):1281–1290.
  • Rusinova R, Koeppe RE 2nd, Andersen OS. A general mechanism for drug promiscuity: studies with amiodarone and other antiarrhythmics. J Gen Physiol. 2015;146(6):463–475.
  • Kraichely RE, Strege PR, Sarr MG, et al. Lysophosphatidyl choline modulates mechanosensitive L-type Ca2+ current in circular smooth muscle cells from human jejunum. Am J Physiol Gastrointest Liver Physiol. 2009;296(4):G833–839.
  • Nash DT, Nash SD. Ranolazine for chronic stable angina. Lancet. 2008;372(9646):1335–1341.
  • Greene HL, Graham EL, Werner JA, et al. Toxic and therapeutic effects of amiodarone in the treatment of cardiac arrhythmias. J Am Coll Cardiol. 1983;2:1114–1128.
  • Abrahamsson H, Dotevall G. Effects of propranolol on colonic pressure in patients with irritable bowel syndrome. Scand J Gastroenterol. 1981;16(8):1021–1024.
  • Rusinova R, Herold KF, Sanford RL, et al. Thiazolidinedione insulin sensitizers alter lipid bilayer properties and voltage-dependent sodium channel function: implications for drug discovery. J Gen Physiol. 2011;138(2):249–270.
  • Ho YF, Chou HY, Chu JS, et al. Comedication with interacting drugs predisposes amiodarone users in cardiac and surgical intensive care units to acute liver injury: a retrospective analysis. Medicine (Baltimore). 2018;97(37):e12301.
  • Avdeef A, Box KJ, Comer JE, et al. pH-metric logP 10. Determination of liposomal membrane-water partition coefficients of ionizable drugs. Pharm Res. 1998;15(2):209–215.
  • PubChem. PubChem Compound Summary for CID 5590. Octoxinol NIH: National Library of Medicine; 2019.
  • LaHann TR, DeKrey LJ, Tarr BD. Capsaicin analgesia: predictions based on physico-chemical properties. Proc West Pharmacol Soc. 1989;32:201–204.
  • Wang DW, Mistry AM, Kahlig KM, et al. Propranolol blocks cardiac and neuronal voltage-gated sodium channels. Front Pharmacol. 2010;1:144.
  • Yang XC, Sachs F. Block of stretch-activated ion channels in xenopus oocytes by gadolinium and calcium ions. Science. 1989;243(4894):1068–1071.
  • Lundbaek JA, Collingwood SA, Ingolfsson HI, et al. Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes. J R Soc Interface. 2010;7(44):373–395.
  • Lundbaek JA, Koeppe RE 2nd, Andersen OS. Amphiphile regulation of ion channel function by changes in the bilayer spring constant. Proc Natl Acad Sci U S A. 2010;107(35):15427–15430.
  • Lundbaek JA, Birn P, Tape SE, et al. Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. Mol Pharmacol. 2005;68(3):680–689.
  • Kapoor R, Peyear TA, Koeppe RE 2nd, et al. Antidepressants are modifiers of lipid bilayer properties. J Gen Physiol. 2019;151(3):342–356.
  • Yang C, Zhang X, Guo Y, et al. Mechanical dynamics in live cells and fluorescence-based force/tension sensors. Biochim Biophys Acta. 2015;1853(8):1889–1904.
  • Suchyna TM, Markin VS, Sachs F. Biophysics and structure of the patch and the gigaseal. Biophys J. 2009;97(3):738–747.
  • Morris CE. Voltage-gated channel mechanosensitivity: fact or friction? Front Physiol. 2011;2:25.
  • Sokabe M, Sachs F. The structure and dynamics of patch-clamped membranes: a study using differential interference contrast light microscopy. J Cell Biol. 1990;111(2):599–606.
  • Beyder A, Rae JL, Bernard C, et al. Mechanosensitivity of Nav1.5, a voltage-sensitive sodium channel. J Physiol. 2010;588(24):4969–4985.
  • Kamkin A, Kiseleva I. Mechanosensitivity of Cells from Various Tissues. In: Kamkin A, and Kiseleva I, editors. Mechanosensitivity in Cells and Tissues. Moscow: Academia;2005: 5-7695-2590-8. https://www.ncbi.nlm.nih.gov/books/NBK7493/.
  • Joshi V, Strege PR, Farrugia G, et al. Mechanotransduction in gastrointestinal smooth muscle cells: role of mechanosensitive ion channels. Am J Physiol Gastrointest Liver Physiol. 2021;320(5):G897–G906.
  • Abriel H. Cardiac Sodium Channel Na(v)1.5 Mechanosensitivity Is Inhibited by Ranolazine. Circulation. 2012;125(22):2681–2683.
  • Fozzard HA, Sheets MF, Hanck DA. The sodium channel as a target for local anesthetic drugs. Front Pharmacol. 2011;2:68.
  • Strichartz GR. The inhibition of sodium currents in myelinated nerve by quaternary derivatives of lidocaine. J Gen Physiol. 1973;62(1):37–57.
  • Tikhonov DB, Zhorov BS. Mechanism of sodium channel block by local anesthetics, antiarrhythmics, and anticonvulsants. J Gen Physiol. 2017;149(4):465–481.
  • Stefan MI, Le Novere N. Cooperative binding. PLoS Comput Biol. 2013;9(6):e1003106.
  • Rusinova R, He C, Andersen OS. Mechanisms underlying drug-mediated regulation of membrane protein function. Proc Natl Acad Sci U S A. 2021;118(46):e2113229118.
  • Sachs F. Mechanical Transduction and the Dark Energy of Biology. Biophys J. 2018;114(1):3–9.
  • Burashnikov A, Di Diego JM, Zygmunt AC, et al. Atrium-selective sodium channel block as a strategy for suppression of atrial fibrillation: differences in sodium channel inactivation between atria and ventricles and the role of ranolazine. Circulation. 2007;116(13):1449–1457.
  • Gawali VS, Lukacs P, Cervenka R, et al. Mechanism of Modification, by Lidocaine, of Fast and Slow Recovery from Inactivation of Voltage-Gated Na(+) Channels. Mol Pharmacol. 2015;88(5):866–879.
  • Sheets MF, Hanck DA. Outward stabilization of the S4 segments in domains III and IV enhances lidocaine block of sodium channels. J Physiol. 2007;582(1):317–334.
  • Peters CH, Sokolov S, Rajamani S, et al. Effects of the antianginal drug, ranolazine, on the brain sodium channel Na(V)1.2 and its modulation by extracellular protons. Br J Pharmacol. 2013;169(3):704–716.
  • Dimitrakopoulos P. Analysis of the variation in the determination of the shear modulus of the erythrocyte membrane: effects of the constitutive law and membrane modeling. Phys Rev E Stat Nonlin Soft Matter Phys. 2012;85(4):041917.
  • Bavi N, Nakayama Y, Bavi O, et al. Biophysical implications of lipid bilayer rheometry for mechanosensitive channels. Proc Natl Acad Sci U S A. 2014;111(38):13864–13869.
  • Haswell ES, Phillips R, Rees DC. Mechanosensitive channels: what can they do and how do they do it? Structure. 2011;19(10):1356–1369.
  • Perozo E, Cortes DM, Sompornpisut P, et al. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 2002;418(6901):942–948.
  • Martinac B, Adler J, Kung C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature. 1990;348(6298):261–263.
  • Kohl P, Sachs F, Franz MR. Cardiac mechano-electric feedback and arrhythmias: from pipette to patient. 1st ed. Philadelphia PA: W.B. Saunders; 2005.
  • Franz MR. Mechano-electrical feedback. Cardiovasc Res. 2000;45(2):263–266.
  • Gonlachanvit S, Mahayosnond A, Kullavanijaya P. Effects of chili on postprandial gastrointestinal symptoms in diarrhoea predominant irritable bowel syndrome: evidence for capsaicin-sensitive visceral nociception hypersensitivity. Neurogastroenterol Motil. 2009;21(1):23–32.
  • Nikolaev YA, Cox CD, Ridone P, et al. Mammalian TRP ion channels are insensitive to membrane stretch. J Cell Sci. 2019;132(23): jcs238360.
  • Mazzone A, Gibbons SJ, Eisenman ST, et al. Direct repression of anoctamin 1 (ANO1) gene transcription by Gli proteins. FASEB J. 2019;33(5):6632–6642.
  • Agarwal MK, Bhatia SJ, Desai SA, et al. Effect of red chillies on small bowel and colonic transit and rectal sensitivity in men with irritable bowel syndrome. Indian J. Gastroenterol. 2002;21(5):179–182.
  • Aniwan S, Gonlachanvit S. Effects of Chili Treatment on Gastrointestinal and Rectal Sensation in Diarrhea-predominant Irritable Bowel Syndrome: a Randomized, Double-blinded, Crossover Study. J Neurogastroenterol Motil. 2014;20(3):400–406.
  • Patcharatrakul T, Gonlachanvit S. Chili Peppers, Curcumins, and Prebiotics in Gastrointestinal Health and Disease. Curr Gastroenterol Rep. 2016;18(4):19.
  • Spencer NJ, Hu H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat Rev Gastroenterol Hepatol. 2020;17(6):338–351.
  • Beyder A, Farrugia G. Ion channelopathies in functional GI disorders. Am J Physiol Gastrointest Liver Physiol. 2016;311(4):G581–G586.
  • Locke GR 3rd, Ackerman MJ, Zinsmeister AR, et al. Gastrointestinal symptoms in families of patients with an SCN5A-encoded cardiac channelopathy: evidence of an intestinal channelopathy. Am J Gastroenterol. 2006;101(6):1299–1304.
  • Alper SL. Genetic Diseases of PIEZO1 and PIEZO2 Dysfunction. Curr Top Membr. 2017;79:97–134.
  • Zarychanski R, Schulz VP, Houston BL, et al. Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood. 2012;120(9):1908–1915.
  • Bae C, Gnanasambandam R, Nicolai C, et al. Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. Proc Natl Acad Sci U S A. 2013;110(12):E1162–1168.