Inositol-1,4,5-trisphosphate induced Ca2+ release and excitation-contraction coupling in atrial myocytes from normal and failing hearts

Journal of Physiology

Volumn 593, Issue 6, 2015, Pages 1459-1477

  Hohendanner, Felix ^a   Walther, Stefanie ^a   Maxwell, Joshua T ^a   Kettlewell, Sarah ^b   Awad, Sawsan ^a   Smith, Godfrey L ^b   Lonchyna, Vassyl A ^c   Blatter, Lothar A ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; CALCIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARRHYTHMOGENESIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; EXCITATION CONTRACTION COUPLING; HEART ATRIUM ARRHYTHMIA; HEART ATRIUM CONTRACTILITY; HEART LEFT VENTRICLE FAILURE; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE POTENTIAL; HEART OUTPUT; HEART VENTRICLE FILLING; INOTROPISM; MALE; NEW ZEALAND WHITE (RABBIT); NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SARCOPLASMIC RETICULUM; SODIUM CALCIUM EXCHANGE; ANIMAL; CYTOLOGY; HEART ATRIUM; HEART FAILURE; METABOLISM; PHYSIOLOGY; RABBIT;

ANIMALS; CALCIUM; CALCIUM SIGNALING; EXCITATION CONTRACTION COUPLING; HEART ATRIA; HEART FAILURE; INOSITOL 1,4,5-TRISPHOSPHATE; MALE; MYOCYTES, CARDIAC; RABBITS;

EID: 84924527564     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.283226     Document Type: Article

References (79)

1. 2+ leak in heart failure. Circ Res 97, 1314-1322.
2. Alpert JS, Petersen P & Godtfredsen J (1988). Atrial fibrillation: natural history, complications, and management. Annu Rev Med 39, 41-52.
3. Barth E, Stammler G, Speiser B & Schaper J (1992). Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol 24, 669-681.
4. Bassani JW, Bassani RA & Bers DM (1994). Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol 476, 279-293.
5. Bers DM, Pogwizd SM & Schlotthauer K (2002). Upregulated Na/Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure. Basic Res Cardiol 97(Suppl. 1), I36-42.
6. Bonow RO, Frederick TM, Bacharach SL, Green MV, Goose PW, Maron BJ & Rosing DR (1983). Atrial systole and left ventricular filling in hypertrophic cardiomyopathy: effect of verapamil. Am J Cardiol 51, 1386-1391.
7. Bootman MD, Harzheim D, Smyrnias I, Conway SJ & Roderick HL (2007). Temporal changes in atrial EC-coupling during prolonged stimulation with endothelin-1. Cell Calcium 42, 489-501.
8. Bootman MD, Higazi DR, Coombes S & Roderick HL (2006). Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J Cell Sci 119, 3915-3925.
9. Bootman MD, Smyrnias I, Thul R, Coombes S & Roderick HL (2011). Atrial cardiomyocyte calcium signalling. Biochim Biophys Acta 1813, 922-934.
10. Cannell MB, Berlin JR & Lederer WJ (1987). Effect of membrane potential changes on the calcium transient in single rat cardiac muscle cells. Science 238, 1419-1423.
11. Cannell MB & Kong CH (2012). Local control in cardiac E-C coupling. J Mol Cell Cardiol 52, 298-303.
12. 3-I receptor mRNA expression in patients with atrial fibrillation. Chin Med J (Engl) 115, 664-667.
13. Chen-Izu Y, McCulle SL, Ward CW, Soeller C, Allen BM, Rabang C, Cannell MB, Balke CW & Izu LT (2006). Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J 91, 1-13.
14. Cheng CP, Suzuki M, Ohte N, Ohno M, Wang ZM & Little WC (1996). Altered ventricular and myocyte response to angiotensin II in pacing-induced heart failure. Circ Res 78, 880-892.
15. Cohn JN, Johnson G, Ziesche S, Cobb F, Francis G, Tristani F, Smith R, Dunkman WB, Loeb H, Wong M et al. (1991). A comparison of enalapril with hydralazine-isosorbide dinitrate in the treatment of chronic congestive heart failure. N Engl J Med 325, 303-310.
16. Coleman R, Silbermann M, Gershon D & Reznick AZ (1987). Giant mitochondria in the myocardium of aging and endurance-trained mice. Gerontology 33, 34-39.
17. 2+ release. Phys Rev E Stat Nonlin Soft Matter Phys 68, 021915.
18. Daoud EG, Weiss R, Bahu M, Knight BP, Bogun F, Goyal R, Harvey M, Strickberger SA, Man KC & Morady F (1996). Effect of an irregular ventricular rhythm on cardiac output. Am J Cardiol 78, 1433-1436.
19. Dedkova EN & Blatter LA (2012). Measuring mitochondrial function in intact cardiac myocytes. J Mol Cell Cardiol 52, 48-61.
20. Dedkova EN & Blatter LA (2013). Calcium signaling in cardiac mitochondria. J Mol Cell Cardiol 58, 125-133.
21. + pump rate in rat and rabbit ventricular myocytes. J Physiol 539, 133-143.
22. 2+ release termination by ryanodine receptor sensitization and in heart failure. J Physiol 587, 5197-5209.
23. 2+ wave generation. J Physiol 590, 6093-6108.
24. 2+ release modulates excitation-contraction coupling in rabbit ventricular myocytes. Am J Physiol Heart Circ Physiol 294, H596-H604.
25. Dominic EA, Ramezani A, Anker SD, Verma M, Mehta N & Rao M (2014). Mitochondrial cytopathies and cardiovascular disease. Heart 100, 611-618.
26. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
27. 2+ release channels. Physiol Rev 87, 593-658.
28. Go LO, Moschella MC, Watras J, Handa KK, Fyfe BS & Marks AR (1995). Differential regulation of two types of intracellular calcium release channels during end-stage heart failure. J Clin Invest 95, 888-894.
29. 2+ transients and arrhythmias associated with cardiac hypertrophy. Proc Natl Acad Sci USA 106, 11406-11411.
30. 2+] decay in ventricular cardiomyocytes in cardiac remodeling and human heart failure. Circ Res 113, 527-538.
31. Huser J, Lipsius SL & Blatter LA (1996). Calcium gradients during excitation-contraction coupling in cat atrial myocytes. J Physiol 494, 641-651.
32. Johnstone D, Limacher M, Rousseau M, Liang CS, Ekelund L, Herman M, Stewart D, Guillotte M, Bjerken G, Gaasch W et al. (1992). Clinical characteristics of patients in studies of left ventricular dysfunction (SOLVD). Am J Cardiol 70, 894-900.
33. 3-mediated signaling in embryonic stem cell-derived cardiomyocytes. PLoS One 9, e83715.
34. Kettlewell S, Burton FL, Smith GL & Workman AJ (2013). Chronic myocardial infarction promotes atrial action potential alternans, afterdepolarizations, and fibrillation. Cardiovasc Res 99, 215-224.
35. 2+ indicator targeted to mitochondria. J Mol Cell Cardiol 46, 891-901.
36. 2+ release during excitation-contraction coupling in atrial myocytes. Biophys J 81, 2590-2605.
37. Kockskamper J, Zima AV, Roderick HL, Pieske B, Blatter LA & Bootman MD (2008). Emerging roles of inositol 1, 4, 5-trisphosphate signaling in cardiac myocytes. J Mol Cell Cardiol 45, 128-147.
38. Li Q, O'Neill SC, Tao T, Li Y, Eisner D & Zhang H (2012). Mechanisms by which cytoplasmic calcium wave propagation and alternans are generated in cardiac atrial myocytes lacking T-tubules-insights from a simulation study. Biophys J 102, 1471-1482.
39. 3)-receptor type 2-deficient mice. Circ Res 96, 1274-1281.
40. Linderer T, Chatterjee K, Parmley WW, Sievers RE, Glantz SA & Tyberg JV (1983). Influence of atrial systole on the Frank-Starling relation and the end-diastolic pressure-diameter relation of the left ventricle. Circulation 67, 1045-1053.
41. 3 receptors that may modulate excitation-contraction coupling in the heart. Curr Biol 10, 939-942.
42. Mackenzie L, Roderick HL, Berridge MJ, Conway SJ & Bootman MD (2004). The spatial pattern of atrial cardiomyocyte calcium signalling modulates contraction. J Cell Sci 117, 6327-6337.
43. Majerus PW, Kisseleva MV & Norris FA (1999). The role of phosphatases in inositol signaling reactions. J Biol Chem 274, 10669-10672.
44. 2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J Biol Chem 273, 10223-10231.
45. Maxwell JT & Blatter LA (2012). Facilitation of cytosolic calcium wave propagation by local calcium uptake into the sarcoplasmic reticulum in cardiac myocytes. J Physiol 590, 6037-6045.
46. Maxwell JT, Domeier TL & Blatter LA (2012). Dantrolene prevents arrhythmogenic Ca release in heart failure. Am J Physiol Heart Circ Physiol 302, H953-H963.
47. 2+ handling in normal and hypertrophied rat myocardium. J Mol Cell Cardiol 30, 2507-2518.
48. 2+ concentration in living single rat cardiac myocytes. Am J Physiol Heart Circ Physiol 261, H1123-H1134.
49. Nattel S (2002). New ideas about atrial fibrillation 50 years on. Nature 415, 219-226.
50. Nicod P, Hillis LD, Winniford MD & Firth BG (1986). Importance of the "atrial kick" in determining the effective mitral valve orifice area in mitral stenosis. Am J Cardiol 57, 403-407.
51. 2+ uptake: tortoise or hare? J Mol Cell Cardiol 46, 767-774.
52. Peppiatt CM, Collins TJ, Mackenzie L, Conway SJ, Holmes AB, Bootman MD, Berridge MJ, Seo JT & Roderick HL (2003). 2-Aminoethoxydiphenyl borate (2-APB) antagonises inositol 1, 4, 5-trisphosphate-induced calcium release, inhibits calcium pumps and has a use-dependent and slowly reversible action on store-operated calcium entry channels. Cell Calcium 34, 97-108.
53. Picht E, Zima AV, Blatter LA & Bers DM (2007). SparkMaster: automated calcium spark analysis with ImageJ. Am J Physiol Cell Physiol 293, C1073-C1081.
54. Pogwizd SM (1995). Nonreentrant mechanisms underlying spontaneous ventricular arrhythmias in a model of nonischemic heart failure in rabbits. Circulation 92, 1034-1048.
55. 2+ exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 85, 1009-1019.
56. Pogwizd SM, Schlotthauer K, Li L, Yuan W & Bers DM (2001). Arrhythmogenesis and contractile dysfunction in heart failure: Roles of sodium-calcium exchange, inward rectifier potassium current, and residual β-adrenergic responsiveness. Circ Res 88, 1159-1167.
57. Rahimtoola SH, Ehsani A, Sinno MZ, Loeb HS, Rosen KM & Gunnar RM (1975). Left atrial transport function in myocardial infarction. Importance of its booster pump function. Am J Med 59, 686-694.
58. Raymond RJ, Lee AJ, Messineo FC, Manning WJ & Silverman DI (1998). Cardiac performance early after cardioversion from atrial fibrillation. Am Heart J 136, 435-442.
59. Remus TP, Zima AV, Bossuyt J, Bare DJ, Martin JL, Blatter LA, Bers DM & Mignery GA (2006). Biosensors to measure inositol 1, 4, 5-trisphosphate concentration in living cells with spatiotemporal resolution. J Biol Chem 281, 608-616.
60. 2+ signals by mitochondria in cat ventricular myocytes. Am J Physiol Cell Physiol 291, C840-C850.
61. 2+ leak in intact ventricular myocytes from rabbits in heart failure. Circ Res 93, 592-594.
62. Sheehan KA & Blatter LA (2003). Regulation of junctional and non-junctional sarcoplasmic reticulum calcium release in excitation-contraction coupling in cat atrial myocytes. J Physiol 546, 119-135.
63. 2+ spark activity and regulation in cat atrial myocytes. J Physiol 572, 799-809.
64. Shkryl VM, Maxwell JT & Blatter LA (2011). A novel method for spatially complex diffraction-limited photoactivation and photobleaching in living cells. J Physiol 590, 1093-1100.
65. Solaro RJ & Briggs FN (1974). Estimating the functional capabilities of sarcoplasmic reticulum in cardiac muscle. Calcium binding. Circ Res 34, 531-540.
66. Stern MD, Song LS, Cheng H, Sham JS, Yang HT, Boheler KR & Rios E (1999). Local control models of cardiac excitation-contraction coupling. A possible role for allosteric interactions between ryanodine receptors. J Gen Physiol 113, 469-489.
67. Thul R, Coombes S, Roderick HL & Bootman MD (2012). Subcellular calcium dynamics in a whole-cell model of an atrial myocyte. Proc Natl Acad Sci USA 109, 2150-2155.
68. 3-activated elementary calcium signals and are downregulated by prolonged hormonal stimulation to inhibit cellular calcium responses. J Cell Sci 114, 3979-3989.
69. Trafford AW, Clarke JD, Richards MA, Eisner DA & Dibb KM (2013). Calcium signalling microdomains and the t-tubular system in atrial mycoytes: potential roles in cardiac disease and arrhythmias. Cardiovasc Res 98, 192-203.
70. Tsang TS, Gersh BJ, Appleton CP, Tajik AJ, Barnes ME, Bailey KR, Oh JK, Leibson C, Montgomery SC & Seward JB (2002). Left ventricular diastolic dysfunction as a predictor of the first diagnosed nonvalvular atrial fibrillation in 840 elderly men and women. J Am Coll Cardiol 40, 1636-1644.
71. 3 regulates phospholipase Cβ1 expression in cardiomyocytes. J Mol Cell Cardiol 45, 679-684.
72. Wang TJ, Larson MG, Levy D, Vasan RS, Leip EP, Wolf PA, D'Agostino RB, Murabito JM, Kannel WB & Benjamin EJ (2003). Temporal relations of atrial fibrillation and congestive heart failure and their joint influence on mortality: the Framingham Heart Study. Circulation 107, 2920-2925.
73. Wendt-Gallitelli MF & Isenberg G (1989). X-ray microanalysis of single cardiac myocytes frozen under voltage-clamp conditions. Am J Physiol Heart Circ Physiol 256, H574-H583.
74. Wijffels MC, Kirchhof CJ, Dorland R, Power J & Allessie MA (1997). Electrical remodeling due to atrial fibrillation in chronically instrumented conscious goats: roles of neurohumoral changes, ischemia, atrial stretch, and high rate of electrical activation. Circulation 96, 3710-3720.
75. Yamda J, Ohkusa T, Nao T, Ueyama T, Yano M, Kobayashi S, Hamano K, Esato K & Matsuzaki M (2001). Up-regulation of inositol 1, 4, 5 trisphosphate receptor expression in atrial tissue in patients with chronic atrial fibrillation. J Am Coll Cardiol 37, 1111-1119.
76. 2+ signaling in a chronic dog model of atrial fibrillation. Cardiology 107, 269-276.
77. 2+ signalling in cat atrial excitation-contraction coupling and arrhythmias. J Physiol 555, 607-615.
78. 2+ leak in normal and failing rabbit ventricular myocytes. J Physiol 588, 4743-4757.
79. 2+ signaling during excitation-contraction coupling in atrial myocytes. Am J Physiol Heart Circ Physiol 304, H983-H993.