Free fatty acid effects on the atrial myocardium: Membrane ionic currents are remodeled by the disruption of T-tubular architecture

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  O'Connell, Ryan P ^a   Musa, Hassan ^a   Gomez, Mario San Martin ^a   Avula, Uma Mahesh ^a   Herron, Todd J ^a   Kalifa, Jerome ^a   Anumonwo, Justus M B ^a   Talkachova, Alena ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CAV1.2 PROTEIN; FATTY ACID; OLEIC ACID; PALMITIC ACID; STEARIC ACID; UNCLASSIFIED DRUG;

ACTION POTENTIAL DURATION; ANIMAL CELL; ARTICLE; CELL MEMBRANE CONDUCTANCE; CONTROLLED STUDY; HEART ATRIUM MUSCLE; HEART MUSCLE CELL; MEMBRANE CURRENT; MEMBRANE STEADY POTENTIAL; NONHUMAN; POTASSIUM CURRENT; SHEEP; TRANSVERSE TUBULAR SYSTEM; ANIMAL; CARDIAC MUSCLE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ELECTROPHYSIOLOGY; HEART ATRIUM; IMMUNOBLOTTING; ION TRANSPORT; MALE; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALS; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTROPHYSIOLOGY; FATTY ACIDS, NONESTERIFIED; HEART ATRIA; IMMUNOBLOTTING; ION TRANSPORT; MALE; MYOCARDIUM; SHEEP;

EID: 84943179997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133052     Document Type: Article

References (53)

1. Khawaja O, Bartz TM, Ix JH, et al. Plasma free fatty acids and risk of atrial fibrillation (from the Cardiovascular Health Study). The American journal of cardiology. Jul 15 2012; 110(2):212-216.
2. Djousse L, Benkeser D, Arnold A, et al. Plasma free fatty acids and risk of heart failure: the Cardiovascular Health Study. Circulation. Heart failure. Sep 1 2013; 6(5):964-969.
3. Rennison JH, Van Wagoner DR. Impact of dietary fatty acids on cardiac arrhythmogenesis. Circulation. Arrhythmia and electrophysiology. Aug 2009; 2(4):460-469.
4. Al Chekakie MO, Welles CC, Metoyer R, et al. Pericardial Fat Is Independently Associated With Human Atrial Fibrillation. Journal of the American College of Cardiology. August 31, 2010 2010; 56(10):784-788.
5. Gong D, Yang R, Munir KM, Horenstein RB, Shuldiner AR. New progress in adipocytokine research. Current Opinion in Endocrinology, Diabetes and Obesity. 2003; 10(2):115-121.
6. Maan A, Mansour M, Ruskin JN, Heist EK. Role of Epicardial Fat in Atrial Fibrillation Pathophysiology and Clincial Implications. The Journal of Innovations in Cardiac Rhythm Management. 2013 2013; 4:1077-1082.
7. Hendrickson SC, St Louis JD, Lowe JE, Abdel-aleem S. Free fatty acid metabolism during myocardial ischemia and reperfusion. Molecular and cellular biochemistry. Jan 1997; 166(1-2):85-94.
8. Pantanowitz L. Fat infiltration in the heart. Heart. Mar 2001; 85(3):253.
9. Graner M, Siren R, Nyman K, et al. Cardiac steatosis associates with visceral obesity in nondiabetic obese men. J Clin Endocrinol Metab. Mar 2013; 98(3):1189-1197.
10. Ricci E, Smallwood S, Chouabe C, et al. Electrophysiological characterization of left ventricular myocytes from obese Sprague-Dawley rat. Obesity. May 2006; 14(5):778-786.
11. Lin YK, Chen YC, Chen JH, Chen SA, Chen YJ. Adipocytes modulate the electrophysiology of atrial myocytes: implications in obesity-induced atrial fibrillation. Basic Res Cardiol. Sep 2012; 107(5):293.
12. Abed HS, Samuel CS, Lau DH, et al. Obesity results in progressive atrial structural and electrical remodeling: implications for atrial fibrillation. Heart rhythm: the official journal of the Heart Rhythm Society. Jan 2013; 10(1):90-100.
13. Barber MC, Ward RJ, Richards SE, et al. Ovine adipose tissue monounsaturated fat content is correlated to depot-specific expression of the stearoyl-CoA desaturase gene. J Anim Sci. Jan 2000; 78(1):62-68.
14. Dublin S, French B, Glazer NL, et al. Risk of new-onset atrial fibrillation in relation to body mass index. Archives of internal medicine. Nov 27 2006; 166(21):2322-2328.
15. Veiga-Lopez A, Moeller J, Patel D, et al. Developmental programming: impact of prenatal testosterone excess on insulin sensitivity, adiposity, and free fatty acid profile in postpubertal female sheep. Endocrinology. May 2013; 154(5):1731-1742.
16. Kim JY, Park JY, Kim OY, et al. Metabolic profiling of plasma in overweight/obese and lean men using ultra performance liquid chromatography and Q-TOF mass spectrometry (UPLC-Q-TOF MS). J Proteome Res. Sep 3 2010; 9(9):4368-4375.
17. Leaf A. The electrophysiological basis for the antiarrhythmic actions of polyunsaturated fatty acids. European Heart Journal Supplements. 2001; 3(suppl D):D98.
18. Musa H, Kaur K, O'Connell R, et al. Inhibition of platelet-derived growth factor-AB signaling prevents electromechanical remodeling of adult atrial myocytes that contact myofibroblasts. Heart rhythm: the official journal of the Heart Rhythm Society. Mar 14 2013.
19. Dhamoon AS, Pandit SV, Sarmast F, et al. Unique Kir2.x properties determine regional and species differences in the cardiac inward rectifier K+ current. Circulation research. May 28 2004; 94(10):1332-1339.
20. Vaidyanathan R, O'Connell RP, Deo M, et al. The ionic bases of the action potential in isolated mouse cardiac Purkinje cell. Heart rhythm: the official journal of the Heart Rhythm Society. Jan 2013; 10(1):80-87.
21. Dhamoon AS, Pandit SV, Sarmast F, et al. Unique Kir2.x Properties Determine Regional and Species Differences in the Cardiac Inward Rectifier K+ Current. Circulation research. May 28, 2004 2004; 94(10):1332-1339.
22. Martins RP, Kaur K, Hwang E, et al. Dominant frequency increase rate predicts transition from paroxysmal to long-term persistent atrial fibrillation. Circulation. Apr 8 2014; 129(14):1472-1482.
23. Anumonwo JM, Delmar M, Jalife J. Electrophysiology of single heart cells from the rabbit tricuspid valve. The Journal of physiology. Jun 1990; 425:145-167.
24. Isenberg G, Klockner U. Calcium tolerant ventricular myocytes prepared by preincubation in a "KB medium". Pflugers Archiv: European journal of physiology. Oct 1982; 395(1):6-18.
25. Vaidyanathan R, Taffet SM, Vikstrom KL, Anumonwo JM. Regulation of cardiac inward rectifier potassium current (IK1) by synapse associated protein-97. The Journal of biological chemistry. Jun 8 2010.
26. Marshall C, Hitman GA, Cassell PG, Turner MD. Effect of glucolipotoxicity and rosiglitazone upon insulin secretion. Biochemical and biophysical research communications. May 11 2007; 356(3):756-762.
27. Richieri GV, Kleinfeld AM. Unbound free fatty acid levels in human serum. Journal of lipid research. Feb 1995; 36(2):229-240.
28. Haim TE, Wang W, Flagg TP, et al. Palmitate attenuates myocardial contractility through augmentation of repolarizing Kv currents. Journal of molecular and cellular cardiology. Feb 2010; 48(2):395-405.
29. Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. The Journal of biological chemistry. May 4 2001; 276(18):14890-14895.
30. Lin YK, Chen YC, Kao YH, et al. A monounsaturated fatty acid (oleic acid) modulates electrical activity in atrial myocytes with calcium and sodium dysregulation. International journal of cardiology. Sep 2014; 176(1):191-198.
31. Kang JX, Xiao YF, Leaf A. Free, long-chain, polyunsaturated fatty acids reduce membrane electrical excitability in neonatal rat cardiac myocytes. Proceedings of the National Academy of Sciences of the United States of America. Apr 25 1995; 92(9):3997-4001.
32. Sun H, Kerfant BG, Zhao D, et al. Insulin-like growth factor-1 and PTEN deletion enhance cardiac L-type Ca2+ currents via increased PI3Kalpha/PKB signaling. Circulation research. Jun 9 2006; 98(11):1390-1397.
33. Xu H, Guo W, Nerbonne JM. Four kinetically distinct depolarization-activated K+ currents in adult mouse ventricular myocytes. The Journal of general physiology. May 1999; 113(5):661-678.
34. Moench I, Meekhof KE, Cheng LF, Lopatin AN. Resolution of hyposmotic stress in isolated mouse ventricular myocytes causes sealing of t-tubules. Exp Physiol. Jul 2013; 98(7):1164-1177.
35. Patel SP, Campbell DL. Transient outward potassium current, 'Ito', phenotypes in the mammalian left ventricle: underlying molecular, cellular and biophysical mechanisms. The Journal of physiology. Nov 15 2005; 569(Pt 1):7-39.
36. Grandi E, Pandit SV, Voigt N, et al. Human atrial action potential and Ca2+ model: sinus rhythm and chronic atrial fibrillation. Circulation research. Oct 14 2011; 109(9):1055-1066.
37. Musa H, Kaur K, O'Connell R, et al. Inhibition of platelet-derived growth factor-AB signaling prevents electromechanical remodeling of adult atrial myocytes that contact myofibroblasts. Heart rhythm: the official journal of the Heart Rhythm Society. Jul 2013; 10(7):1044-1051.
38. van Oort RJ, Garbino A, Wang W, et al. Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation. Mar 8 2011; 123(9):979-988.
39. Catterall WA. Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol. 2000; 16:521-555.
40. Campbell DL, Stamler JS, Strauss HC. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. The Journal of general physiology. Oct 1996; 108(4):277-293.
41. Lenaerts I, Bito V, Heinzel FR, et al. Ultrastructural and functional remodeling of the coupling between Ca2+ influx and sarcoplasmic reticulum Ca2+ release in right atrial myocytes from experimental persistent atrial fibrillation. Circulation research. Oct 23 2009; 105(9):876-885.
42. Louch WE, Sejersted OM, Swift F. There goes the neighborhood: pathological alterations in T-tubule morphology and consequences for cardiomyocyte Ca2+ handling. J Biomed Biotechnol. 2010; 2010:503906.
43. Sacks HS, Fain JN. Human epicardial adipose tissue: a review. Am Heart J. Jun 2007; 153(6):907-917.
44. Doolan GK, Panchal RG, Fonnes EL, Clarke AL, Williams DA, Petrou S. Fatty acid augmentation of the cardiac slowly activating delayed rectifier current (IKs) is conferred by hmin K. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. Oct 2002; 16(12):1662-1664.
45. Hong TT, Smyth JW, Gao D, et al. BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol. Feb 2010; 8(2):e1000312.
46. Emken EA. Metabolism of dietary stearic acid relative to other fatty acids in human subjects. The American journal of clinical nutrition. Dec 1994; 60(6 Suppl):1023S-1028S.
47. Dibb KM, Clarke JD, Horn MA, et al. Characterization of an extensive transverse tubular network in sheep atrial myocytes and its depletion in heart failure. Circulation. Heart failure. Sep 2009; 2(5):482-489.
48. Frisk M, Koivumaki JT, Norseng PA, Maleckar MM, Sejersted OM, Louch WE. Variable t-tubule organization and Ca2+ homeostasis across the atria. American journal of physiology. Heart and circulatory physiology. Aug 15 2014; 307(4):H609-620.
49. Lyon AR, MacLeod KT, Zhang Y, et al. Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proceedings of the National Academy of Sciences of the United States of America. Apr 21 2009; 106(16):6854-6859.
50. Cheng LF, Wang F, Lopatin AN. Metabolic stress in isolated mouse ventricular myocytes leads to remodeling of t tubules. American journal of physiology. Heart and circulatory physiology. Nov 2011; 301(5):H1984-1995.
51. Lemieux H, Bulteau AL, Friguet B, Tardif JC, Blier PU. Dietary fatty acids and oxidative stress in the heart mitochondria. Mitochondrion. Jan 2011; 11(1):97-103.
52. Suzuki T. Ultrastructural changes of heart muscle in cyanide poisoning. The Tohoku journal of experimental medicine. Jul 1968; 95(3):271-287.
53. Riquelme CA, Magida JA, Harrison BC, et al. Fatty acids identified in the Burmese python promote beneficial cardiac growth. Science. Oct 28 2011; 334(6055):528-531.