Effects of n-3 polyunsaturated fatty acids on cardiac ion channels

Frontiers in Physiology

Volumn 3 JUL, Issue , 2012, Pages

  Moreno, Cristina ^a   Macías, Alvaro ^a   Prieto, Angela ^a   de la Cruz, Alicia ^a   González, Teresa ^a   Valenzuela, Carmen ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

Arrhythmias; Atrial fibrillation; Heart failure; N 3 pufas

Indexed keywords

EID: 84866456886     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00245     Document Type: Review

References (66)

1. Bannenberg, G., and Serhan, C. N. (2010). Specialized pro-resolving lipid mediators in the inflammatory response: an update. Biochim. Biophys. Acta 1801, 1260-1273.
2. Basiouni, S., Stockel, K., Fuhrmann, H., and Schumann, J. (2012). Polyunsaturated fatty acid supplements modulate mast cell membrane microdomain composition. Cell. Immunol. 275, 42-46.
3. Behrens, S., Li, C., and Franz, M. R. (1997). Effects of myocardial ischemia on ventricular fibrillation inducibility and defibrillation efficacy. J. Am. Coll. Cardiol. 29, 817-824.
4. Billman, G. E., Kang, J. X., and Leaf, A. (1997). Prevention of ischemia-induced cardiac sudden deathby n-3 polyunsaturated fatty acids in dogs. Lipids 32, 1161-1168.
5. Billman, G. E., Kang, J. X., and Leaf, A. (1999). Prevention of sudden cardiac death by dietary pure omega-3 polyunsaturated fatty acids in dogs. Circulation 99, 2452-2457.
6. Brouwer, I. A., Raitt, M. H., Dullemeijer, C., Kraemer, D. F., Zock, P. L., Morris, C., Katan, M. B., Connor, W. E., Camm, J. A., Schouten, E. G., and McAnulty, J. (2009). Effect of fish oil on ventricular tachyarrhythmia in three studies in patients with implantable cardioverter defibrillators. Eur. Heart J. 30, 820-826.
7. Burr, M. L., Ashfield-Watt, P. A., Dunstan, F. D., Fehily, A. M., Breay, P., Ashton, T., Zotos, P. C., Haboubi, N. A., and Elwood, P. C. (2003). Lack of benefit of dietary advice to men with angina: results of a controlled trial. Eur. J. Clin. Nutr. 57, 193-200.
8. Burr, M. L., Fehily, A., Gilbert, J. F., Rogers, S., Holliday, R. M., Sweetnam, P. M., Elwood, P. C., and Deadman, N. M. (1989). Effects of changes in fat, fish, and fibre intakes on death and myocardial reinfarction: diet and reinfarction trial (DART). Lancet 2, 757-761.
9. Burtis, C. A., Ashwood, E. R., and Tietz, N. W. (1999). Textbook of Clinical Chemistry. Philadelphia: W.B. Saunders.
10. Calo, L., Bianconi, L., Colivicchi, F., Lamberti, F., Loricchio, M. L., De Ruvo, E., Meo, A., Pandozi, C., Staibano, M., and Santini,M. (2005). N-3 fatty acids for the prevention of atrial fibrillation after coronary artery bypass surgery: a randomized, controlled trial. J. Am. Coll. Cardiol. 45, 1723-1728.
11. Coronel, R., Wilms-Schopman, F. J., Den Ruijter, H. M., Belterman, C. N., Schumacher, C. A., Opthof, T., Hovenier, R., Lemmens, A. G., Terpstra, A. H., Katan, M. B., and Zock, P. (2007). Dietary n-3 fatty acids promote arrhythmias during acute regional myocardial ischemia in isolated pig hearts. Cardiovasc. Res. 73, 386-394.
12. De Caterina, R., Madonna, R., Zucchi, R., and La Rovere, M. T. (2003). Antiarrhythmic effects of omega-3 fatty acids: from epidemiology to bedside. Am. Heart J. 146, 420-430.
13. Den Ruijter, H. M., Berecki, G., Verkerk, A. O., Bakker, D., Baartscheer, A., Schumacher, C. A., Belterman, C. N., de, J. N., Fiolet, J. W., Brouwer, I. A., and Coronel, R. (2008). Acute administration of fish oil inhibits triggered activity in isolated myocytes from rabbits and patients with heart failure. Circulation 117, 536-544.
14. Den Ruijter, H. M., Verkerk, A. O., Berecki, G., Bakker, D., van Ginneken,A. C., and Coronel, R. (2006). Dietary fish oil reduces the occurrence of early afterdepolarizations in pig ventricular myocytes.J. Mol. Cell. Cardiol. 41, 914-917.
15. Den Ruijter, H. M., Verkerk, A. O., and Coronel, R. (2010). Incorporated fish oil fatty acids prevent action potential shortening induced by circulating fish oil fatty acids. Front. Physiol. 1:149. doi:10.3389/fphys.2010.00149
16. Den Ruijter, H. M., Verkerk, A. O., Schumacher, C. A., Houten, S. M., Belterman, C. N., Baartscheer, A., Brouwer, I. A., van, B. M., de, R. B., and Coronel, R. (2012). A diet rich in unsaturated Fatty acids prevents progression toward heart failure in a rabbit model of pressure and volume overload. Circ. Heart Fail. 5, 376-384.
17. Doolan, G. K., Panchal, R. G., Fonnes, E. L., Clarke, A. L., Williams, D. A., and Petrou,S. (2002). Fatty acid augmentation of the cardiac slowly activating delayed rectifier current (IKs) is conferred by hminK. FASEB J. 16, 1662-1664.
18. Dujardin, K. S., Dumotier, B., David, M., Guizy, M., Valenzuela, C., and Hondeghem, L. M. (2008). Ultrafast sodium channel block by dietaryfish oil prevents dofetilide-induced ventricular arrhythmias inrabbit hearts. Am. J. Physiol. Heart Circ. Physiol. 295, H1414-H1421.
19. Echt, D. S., Liebson, P. R., Mitchell, L. B., Peters, R. W., Obias-Manno, D., Barker, A. H., Arnsberg, D., Baker, A., Friedman, L., Greene, H. L., Huther, M. L., and Richardson, D. W. (1991). Mortality and morbidity in patients receiving encainide, flecainide and placebo. N. Engl. J. Med. 324, 781-788.
20. Fedida, D., Wible, B., Wang, Z., Fermini, B., Faust, F., Nattel, S., and Brown, A. M. (1993). Identity of a novel delayed rectifier current from human heartwithaclonedK+ channel current. Circ. Res. 73, 210-216.
21. Fuster, V., Ryden, L. E., Cannom, D. S., Crijns, H. J., Curtis, A. B., Ellenbogen, K. A., Halperin, J. L., Kay, G. N., Le Huezey, J. Y., Lowe, J. E., Olsson, S. B., Prystowsky, E. N., Tamargo, J. L., and Wann, L. S. (2011). 2011 ACCF/AHA/HRS focused updates incorporated into the ACC/AHA/ESC 2006 Guidelines for the management of patients with atrial fibrillation: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines developed in partnership with the European Society of Cardiology and in collaboration with the European Heart Rhythm Association and the Heart Rhythm Society. J. Am. Coll. Cardiol. 57, e101-e198.
22. Gaborit, N., Varro, A., Le, B. S., Szuts, V., Escande, D., Nattel, S., and Demolombe,S. (2010). Gender-related differences in ion-channel and transporter subunit expression in non-diseased human hearts. J. Mol. Cell. Cardiol. 49, 639-646.
23. GISSI-Prevenzione Investigators. (1999). Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico. Lancet 354, 447-455.
24. Guizy, M., Arias, C., David, M., Gonzalez, T., and Valenzuela, C. (2005). ω-3 and ω-6 polyunsaturated fatty acids block HERG channels. Am. J. Physiol. Cell Physiol. 289, C1251- C1260.
25. Guizy, M., David, M., Arias, C., Zhang, L., Cofan, M., Ruiz-Gutierrez, V., Ros, E., Lillo, M. P., Martens, J. R., and Valenzuela, C. (2008). Modulation of the atrial specific Kv1.5 channel by the n-3 polyun-saturated fatty acid, alpha-linolenic acid. J. Mol. Cell. Cardiol. 44, 323-335.
26. Hondeghem, L. M., Carlsson, L., and Duker, G. (2001). Instability and tri-angulation of the action potential predict serious proarrhythmia, but action potential duration prolongation is antiarrhythmic. Circulation. 103, 2004-2013.
27. Honoré, E., Barhanin, J., Attali, B., Lesage, F., and Lazdunski,M. (1994). External blockade of the major cardiac delayed-rectifier K+ channel (Kv1.5) by polyunsaturated fatty acids. Proc. Natl. Acad. Sci. U.S.A. 91, 1937-1941.
28. Jude, S., Bedut, S., Roger, S., Pinault, M., Champeroux, P., White, E., and Le Guennec, J. Y. (2003). Peroxidation of docosahexaenoic acid is responsible for its effects on I TO and I SS in rat ventricular myocytes. Br. J. Pharmacol. 139, 816-822.
29. Kang, J. X., Xiao, Y. F., and Leaf, A. (1995). Free, long-chain, polyunsaturated fatty acids reduce membrane electrical excitability in neonatal rat cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A. 92, 3997-4001.
30. Koshida, S., Kurata, Y., Notsu, T., Hirota, Y., Kuang, T. Y., Li, P., Bahrudin, U., Harada, S., Miake, J., Yamamoto, Y., Hoshikawa, Y., Igawa, O., Higaki, K., Soma, M.,Yoshida, A., Ninomiya, H., Shiota, G., Shirayoshi, Y., and Hisatome, I. (2009). Stabilizing effects of eicosapentaenoic acid on Kv1.5 channel protein expressed in mammalian cells. Eur. J. Pharmacol. 604, 93-102.
31. Kromhout, D., Giltay, E. J., and Geleijnse, J. M. (2010). n-3 fatty acids and cardiovascular events after myocardial infarction. N. Engl. J. Med. 363, 2015-2026.
32. Leaf, A., Kang, J. X., Xiao, Y. F., and Billman, G. E. (2003). Clinical prevention of sudden cardiac death by n-3 polyunsaturated fatty acids and mechanism of prevention of arrhythmias by n-3 fish oils. Circulation 107, 2646-2652.
33. Leaf,A.,and Xiao,Y.F. (2001). Themodulation of ionic currents in excitable tissues by n-3 polyunsaturated fatty acids. J. Membr. Biol. 184, 263-271.
34. Leifert, W. R., Jahangiri, A., Saint, D. A., and McMurchie, E. J. (2000). Effects of dietary n-3 fatty acids on contractility, Na+ and K+ currents in a rat cardiomyocyte model of arrhythmia. J. Nutr. Biochem. 11, 382-392.
35. Leifert, W. R., McMurchie, E. J., and Saint, D. A. (1999). Inhibition of cardiac sodium currents in adult rat myocytes by n-3 polyunsaturated fatty acids. J. Physiol. (Lond.) 520(Pt 3), 671-679.
36. Li, G. R., Feng, J., Yue, L., Carrier, M., and Nattel, S. (1996). Evidence for two components of delayed rectifier K+ currentinhuman ventricular myocytes. Circ. Res. 78, 689-696.
37. Li, G. R., Sun, H. Y., Zhang, X. H., Cheng, L. C., Chiu, S. W., Tse, H. F., and Lau, C. P. (2009). Omega-3 polyunsaturated fatty acids inhibit transient outward and ultra-rapid delayed rectifier K+currents and Na+current in human atrial myocytes. Cardiovasc. Res. 81, 286-293.
38. Li, Y. S., Wu, P., Zhou, X. Y., Chen, J. G., Cai, L., Wang, F., Xu, L. M., Zhang, X. L., Chen, Y., Liu, S. J., Huang,Y. P., and Ye, D.Y. (2008). Formylpeptide receptor like 1: a potent mediator of the Ca2+ release-activated Ca2+ current ICRAC. Arch. Biochem. Biophys. 478, 110-118.
39. Lowe, J. S., Stroud, D. M., Yang, T., Hall, L., Atack, T. C., and Roden, D. M. (2012). Increased late sodium current contributes to long QT-related arrhythmia susceptibility in female mice. Cardiovasc. Res. doi: 10.1093/cvr/cvs160. [Epub ahead of print].
40. Marchioli, R., Barzi, F., Bomba, E., Chieffo, C., Di, G. D., Di, M. R., Franzosi, M. G., Geraci, E., Levantesi, G., Maggioni, A. P., Mantini, L., Marfisi, R. M., Mastrogiuseppe, G., Mininni, N., Nicolosi, G. L., Santini, M., Schweiger, C., Tavazzi, L., Tognoni, G., Tucci, C., Valagussa, F., and GISSI-Prevenzione Investigators. (2002). Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Soprav-vivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation 105, 1897-1903.
41. Mariscalco, G., Sarzi, B. S., Banach, M., Borsani, P., Bruno, V. D., Napoleone, M., Vitale, C., Piffaretti, G., Pedretti, R. F., and Sala, A. (2010). Preoperative n-3 polyunsatured fatty acids are associated with a decrease in the incidence of early atrial fibrillation following cardiac surgery. Angiology 61, 643-650.
42. Mays,D. J., Foose,J. M., Philipson,L. H., and Tamkun, M. M. (1995). Localizationof the Kv1.5 K+ channel protein in explanted cardiac tissue. J. Clin. Invest. 96, 282-292.
43. Membersof the Sicilian Gambit. (2001). New approaches to antiarrhythmic therapy, part I: emerging therapeutic applications of the cell biology of cardiac arrhythmias. Circulation. 104, 2865-2873.
44. Nau, C., Wang, S. Y., Strichartz, G. R., and Wang, G. K. (2000). Block of human heart hH1 sodium channels by the enantiomers of bupivacaine. Anesthesiology. 93, 1022-1033.
45. Raitt, M. H., Connor, W. E., Morris, C., Kron, J., Halperin, B., Chugh, S. S., McClelland, J., Cook, J., MacMurdy, K., Swenson, R., Connor, S. L., Gerhard, G., Kraemer, D. F., Oseran, D., Marchant, C., Calhoun, D., Shnider, R., and McAnulty, J. (2005). Fish oil supplementation and risk of ventricular tachycardia and ventricular fibrillation in patients with implantable defibrillators: a randomized controlled trial. JAMA 293, 2884-2891.
46. Rauch, B., Schiele, R., Schneider, S., Diller, F., Victor, N., Gohlke, H., Gottwik, M., Steinbeck, G., Del, C. U., Sack, R., Worth, H., Katus, H., Spitzer, W., Sabin, G., Senges, J., and OMEGA Study Group. (2010). OMEGA, a randomized, placebo-controlled trial to test the effect of highly purified omega-3 fatty acids on top of modern guideline-adjusted therapy after myocardial infarction. Circulation 122, 2152-2159.
47. Ravens, U., and Cerbai, E. (2008). Role of potassium currents in cardiac arrhythmias. Europace 10, 1133-1137.
48. Rosen, M. R., Schwartz, P. J., and for Task Force of the Working Group on Arrhythmias of the European Society of Cardiology. (1991). The Sicilian Gambit. A new approach to the classification of antiarrhythmic drugs based on their actions on arrhythmogenic mechanism. Circulation 84, 1831-1851.
49. Sanguinetti, M. C., Jiang, C., Curran, M. E., and Keating, M. T. (1995). A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell 81, 299-307.
50. Sanguinetti, M. C., and Jurkiewicz, N. K. (1991). Delayed rectifier outward K+ current is composed of two currents in guinea pig atrial cells. Am. J. Physiol. 260, H393-H399.
51. Serhan, C. N., Yacoubian, S., and Yang, R. (2008). Anti-inflammatory and proresolving lipid mediators. Annu. Rev. Pathol. 3, 279-312.
52. Sinclair,H. M. (1953). The diet of Canadian Indian Eskimos. Proc. Nutr. Soc. 12, 69-82.
53. Sinclair, H. M. (1956). Deficiency of essential fatty acids and atherosclerosis, etcetera. Lancet 270, 381-383.
54. Snyders,D. J., Tamkun,M. M., and Bennett, P. B. (1993). A rapidly activating and slowly inactivating potassium channel cloned from human heart. Functional analysis after stable mammalian cell culture expression. J. Gen. Physiol. 101, 513-543.
55. Tamargo, J., Caballero, R., Gomez, R., Valenzuela, C., and Delpon, E. (2004). Pharmacology of cardiac potassium channels. Cardiovasc. Res. 62, 9-33.
56. Tanaka, K., Ishikawa, Y., Yokoyama, M., Origasa, H., Matsuzaki, M., Saito, Y., Matsuzawa, Y., Sasaki, J., Oikawa, S., Hishida, H., Itakura, H., Kita, T., Kitabatake,A., Nakaya,N., Sakata, T., Shimada, K., Shirato, K., and JELIS Investigators, Japan. (2008). Reduction in the recurrence of stroke by eicosapentaenoic acid for hyper-cholesterolemic patients: subanalysis of the JELIS trial. Stroke 39, 2052-2058.
57. Tavazzi, L., Maggioni, A. P., Marchioli, R., Barlera, S., Franzosi, M. G., Latini, R., Lucci, D., Nicolosi, G. L., Porcu, M., and Tognoni, G. (2008). Effect of n-3 polyunsaturated fatty acids in patients with chronic heart failure (the GISSI-HF trial): a randomised, double-blind, placebo-controlled trial. Lancet 372, 1223-1230.
58. Turk, H. F., and Chapkin, R. S. (2012). Membrane lipid raft organization is uniquely modified by n-3 polyun-saturated fatty acids. Prostaglandins Leukot. Essent. Fatty Acids.
59. Verkerk, A. O., van Ginneken, A. C., Berecki, G., Den Ruijter, H. M., Schumacher,C.A.,Veldkamp,M.W., Baartscheer, A., Casini, S., Opthof, T., Hovenier, R., Fiolet, J. W., Zock, P. L., and Coronel, R. (2006). Incorporated sarcolemmal fish oil fatty acids shorten pig ventricular action potentials. Cardiovasc. Res. 70, 509-520.
60. Wang, Z., Fermini, B., and Nattel, S. (1993). Delayed rectifier outward current and repolarization in human atrial myocytes. Circ. Res. 73, 276-285.
61. Xiao, Y. F., Gomez, A. M., Morgan, J. P., Lederer, W. J., and Leaf, A. (1997). Suppression of voltage-gated L-type Ca2+ currents by polyun-saturated fatty acids in adult and neonatal rat ventricular myocytes. Proc. Natl. Acad. Sci. U.S.A. 94, 4182-4187.
62. Xiao, Y. F., Kang, J. X., Morgan, J. P., and Leaf, A. (1995). Blocking effects of polyunsaturated fatty acids on Na+ channels of neonatal rat ventricular myocytes. Proc. Natl. Acad. Sci. U.S.A. 92, 11000-11004.
63. Xiao, Y. F., Ke, Q., Wang, S. Y., Auktor, K., Yang, Y., Wang, G. K., Morgan, J. P., and Leaf, A. (2001). Single point mutations affect fatty acid block of human myocardial sodium channel alpha subunit Na+ channels. Proc. Natl. Acad. Sci. U.S.A. 98, 3606-3611.
64. Xiao, Y. F., Morgan, J. P., and Leaf, A. (2002). Effects of polyunsaturated fatty acids on cardiac voltage-activated K(+) currents in adult ferret cardiomyocytes. ShengLiXue Bao 54, 271-281.
65. Xiao, Y. F., Wright, S. N., Wang, G. K., Morgan, J. P., and Leaf, A. (1998). Fatty acids suppress voltage-gated Na+ currentsinHEK293t cells transfected with the alpha-subunit of the human cardiac Na+ channel. Proc. Natl. Acad. Sci. U.S.A. 95, 2680-2685.
66. Xiao, Y. F., Wright, S. N., Wang, G. K., Morgan, J. P., and Leaf, A. (2000). Coexpression with beta(1)-subunit modifies the kinetics and fatty acid block of hH1(alpha) Na(+) channels. Am. J. Physiol. Heart Circ. Physiol. 279, H35-H46.