Atrial cardiomyocyte calcium signalling

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 5, 2011, Pages 922-934

  Bootman, Martin D ^a   Smyrnias, Ioannis ^a   Thul, Rüdiger ^b   Coombes, Stephen ^b   Roderick, H Llewelyn ^a,c  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Arrhythmia; Atrial; Calcium; Cardiac; Excitation contraction coupling; Inositol; Inotropy; Ryanodine; Signalling; T tubules

Indexed keywords

CALCIUM ION; ENDOTHELIN 1; ISOPRENALINE; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SODIUM CALCIUM EXCHANGE PROTEIN; TROPONIN C;

BLOOD PUMP; CALCIUM BINDING; CALCIUM SIGNALING; EXERCISE; HEART ATRIUM; HEART ATRIUM FIBRILLATION; HEART ATRIUM PACEMAKER; HEART BEAT; HEART CONTRACTION; HEART CYCLE; HEART DEPOLARIZATION; HEART EJECTION FRACTION; HEART EXCITATION; HEART FUNCTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE FIBER MEMBRANE; HEART RHYTHM; HEART VENTRICLE FILLING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; TRANSVERSE TUBULAR SYSTEM;

ANIMALS; CALCIUM SIGNALING; EXCITATION CONTRACTION COUPLING; HEART ATRIA; HEART FAILURE; HEART VENTRICLES; HUMANS; MYOCYTES, CARDIAC;

EID: 79955644787     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.01.030     Document Type: Review

References (123)

1. Lo H.M., Lin F.Y., Lin J.L., Hsu K.L., Chiang F.T., Tseng C.D., Tseng Y.Z. Impaired cardiac performance relating to delayed left atrial activation after atrial compartment operation for chronic atrial fibrillation. Pacing Clin. Electrophysiol. 1999, 22:379-381.
2. Dobrev D. Atrial Ca2+ signaling in atrial fibrillation as an antiarrhythmic drug target. Naunyn Schmiedebergs Arch. Pharmacol. 2010, 381:195-206.
3. Alpert J.S., Petersen P., Godtfredsen J. Atrial fibrillation: natural history, complications, and management. Annu. Rev. Med. 1988, 39:41-52.
4. Dobrev D., Nattel S. Calcium handling abnormalities in atrial fibrillation as a target for innovative therapeutics. J. Cardiovasc. Pharmacol. 2008, 52:293-299.
5. Yeh Y.H., Wakili R., Qi X.Y., Chartier D., Boknik P., Kaab S., Ravens U., Coutu P., Dobrev D., Nattel S. Calcium-handling abnormalities underlying atrial arrhythmogenesis and contractile dysfunction in dogs with congestive heart failure. Circ. Arrhythm. Electrophysiol. 2008, 1:93-102.
6. Hove-Madsen L., Llach A., Bayes-Genis A., Roura S., Rodriguez Font E., Aris A., Cinca J. Atrial fibrillation is associated with increased spontaneous calcium release from the sarcoplasmic reticulum in human atrial myocytes. Circulation 2004, 110:1358-1363.
7. Wakili R., Yeh Y.H., Qi X.Y., Greiser M., Chartier D., Nishida K., Maguy A., Villeneuve L.R., Boknik P., Voigt N., Krysiak J., Kaab S., Ravens U., Linke W.A., Stienen G.J., Shi Y., Tardif J.C., Schotten U., Dobrev D., Nattel S. Multiple potential molecular contributors to atrial hypocontractility caused by atrial tachycardia remodeling in dogs. Circ. Arrhythm. Electrophysiol. 2010.
8. Greiser M., Lederer W.J., Schotten U. Alterations of atrial Ca2+ handling as cause and consequence of atrial fibrillation. Cardiovasc. Res. 2010.
9. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
10. Ayettey A.S., Navaratnam V. The T-tubule system in the specialized and general myocardium of the rat. J. Anat. 1978, 127:125-140.
11. Fill M., Copello J.A. Ryanodine receptor calcium release channels. Physiol. Rev. 2002, 82:893-922.
12. Meissner G. Molecular regulation of cardiac ryanodine receptor ion channel. Cell Calcium 2004, 35:621-628.
13. Roderick H.L., Berridge M.J., Bootman M.D. Calcium-induced calcium release. Curr. Biol. 2003, 13:R425.
14. Peskoff A., Langer G.A. Calcium concentration and movement in the ventricular cardiac cell during an excitation-contraction cycle. Biophys. J. 1998, 74:153-174.
15. Jones P.P., Bazzazi H., Kargacin G.J., Colyer J. Inhibition of cAMP-dependent protein kinase under conditions occurring in the cardiac dyad during a Ca2+ transient. Biophys. J. 2006, 91:433-443.
16. Cheng H., Lederer W.J., Cannell M.B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993, 262:740-744.
17. Cannell M.B., Cheng H., Lederer W.J. The control of calcium release in heart muscle. Science 1995, 268:1045-1049.
18. Soeller C., Cannell M.B. Estimation of the sarcoplasmic reticulum Ca2+ release flux underlying Ca2+ sparks. Biophys. J. 2002, 82:2396-2414.
19. Parker I., Wier W.G. Variability in frequency and characteristics of Ca2+ sparks at different release sites in rat ventricular myocytes. J. Physiol. 1997, 505(Pt 2):337-344.
20. Shen J.X., Wang S., Song L.S., Han T., Cheng H. Polymorphism of Ca2+ sparks evoked from in-focus Ca2+ release units in cardiac myocytes. Biophys. J. 2004, 86:182-190.
21. Inoue M., Bridge J.H. Ca2+ sparks in rabbit ventricular myocytes evoked by action potentials: involvement of clusters of L-type Ca2+ channels. Circ. Res. 2003, 92:532-538.
22. Eisner D.A., Sipido K.R. Sodium calcium exchange in the heart: necessity or luxury?. Circ. Res. 2004, 95:549-551.
23. Cartwright E.J., Oceandy D., Neyses L. Physiological implications of the interaction between the plasma membrane calcium pump and nNOS. Pflugers Arch. 2009, 457:665-671.
24. Guatimosim S., Dilly K., Santana L.F., Saleet Jafri M., Sobie E.A., Lederer W.J. Local Ca(2+) signaling and EC coupling in heart: Ca(2+) sparks and the regulation of the [Ca(2+)](i) transient. J. Mol. Cell. Cardiol. 2002, 34:941-950.
25. Smyrnias I., Mair W., Harzheim D., Walker S.A., Roderick H.L., Bootman M.D. Comparison of the T-tubule system in adult rat ventricular and atrial myocytes, and its role in excitation-contraction coupling and inotropic stimulation. Cell Calcium 2010, 47:210-223.
26. Song L.S., Guatimosim S., Gomez-Viquez L., Sobie E.A., Ziman A., Hartmann H., Lederer W.J. Calcium biology of the transverse tubules in heart. Ann. NY Acad. Sci. 2005, 1047:99-111.
27. Bootman M.D., Higazi D.R., Coombes S., Roderick H.L. Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J. Cell Sci. 2006, 119:3915-3925.
28. Brette F., Orchard C. T-tubule function in mammalian cardiac myocytes. Circ. Res. 2003, 92:1182-1192.
29. Louch W.E., Sejersted O.M., Swift F. There goes the neighborhood: pathological alterations in T-tubule morphology and consequences for cardiomyocyte Ca2+ handling. J. Biomed. Biotechnol. 2010, 2010:503906.
30. Pasek M., Brette F., Nelson A., Pearce C., Qaiser A., Christe G., Orchard C.H. Quantification of t-tubule area and protein distribution in rat cardiac ventricular myocytes. Prog. Biophys. Mol. Biol. 2008, 96:244-257.
31. Mackenzie L., Roderick H.L., Berridge M.J., Conway S.J., Bootman M.D. The spatial pattern of atrial cardiomyocyte calcium signalling modulates contraction. J. Cell Sci. 2004, 117:6327-6337.
32. Chen-Izu Y., McCulle S.L., Ward C.W., Soeller C., Allen B.M., Rabang C., Cannell M.B., Balke C.W., Izu L.T. Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys. J. 2006, 91:1-13.
33. Scriven D.R., Klimek A., Lee K.L., Moore E.D. The molecular architecture of calcium microdomains in rat cardiomyocytes. Ann. NY Acad. Sci. 2002, 976:488-499.
34. Brette F., Despa S., Bers D.M., Orchard C.H. Spatiotemporal characteristics of SR Ca(2+) uptake and release in detubulated rat ventricular myocytes. J. Mol. Cell. Cardiol. 2005, 39:804-812.
35. Tanaka H., Kawanishi T., Shigenobu K. Optical bioimaging: from living tissue to a single molecule: atrio-ventricular difference in myocardial excitation-contraction coupling-sequential versus simultaneous activation of SR Ca2+ release units. J. Pharmacol. Sci. 2003, 93:248-252.
36. Cleemann L., Wang W., Morad M. Two-dimensional confocal images of organization, density, and gating of focal Ca2+ release sites in rat cardiac myocytes. Proc. Natl Acad. Sci. USA 1998, 95:10984-10989.
37. Isenberg G., Etter E.F., Wendt-Gallitelli M.F., Schiefer A., Carrington W.A., Tuft R.A., Fay F.S. Intrasarcomere [Ca2+] gradients in ventricular myocytes revealed by high speed digital imaging microscopy. Proc. Natl Acad. Sci. USA 1996, 93:5413-5418.
38. Gotoh T. Quantitative studies on the ultrastructural differentiation and growth of mammalian cardiac muscle cells. The atria and ventricles of the cat. Acta Anat. (Basel) 1983, 115:168-177.
39. Tidball J.G., Cederdahl J.E., Bers D.M. Quantitative analysis of regional variability in the distribution of transverse tubules in rabbit myocardium. Cell Tissue Res. 1991, 264:293-298.
40. Yamasaki Y., Furuya Y., Araki K., Matsuura K., Kobayashi M., Ogata T. Ultra-high-resolution scanning electron microscopy of the sarcoplasmic reticulum of the rat atrial myocardial cells. Anat. Rec. 1997, 248:70-75.
41. Mackenzie L., Bootman M.D., Berridge M.J., Lipp P. Predetermined recruitment of calcium release sites underlies excitation-contraction coupling in rat atrial myocytes. J. Physiol. 2001, 530:417-429.
42. Carl S.L., Felix K., Caswell A.H., Brandt N.R., Ball W.J., Vaghy P.L., Meissner G., Ferguson D.G. Immunolocalization of sarcolemmal dihydropyridine receptor and sarcoplasmic reticular triadin and ryanodine receptor in rabbit ventricle and atrium. J. Cell Biol. 1995, 129:672-682.
43. Hatem S.N., Benardeau A., Rucker-Martin C., Marty I., de Chamisso P., Villaz M., Mercadier J.J. Different compartments of sarcoplasmic reticulum participate in the excitation-contraction coupling process in human atrial myocytes. Circ. Res. 1997, 80:345-353.
44. Kockskamper J., Sheehan K.A., Bare D.J., Lipsius S.L., Mignery G.A., Blatter L.A. Activation and propagation of Ca(2+) release during excitation-contraction coupling in atrial myocytes. Biophys. J. 2001, 81:2590-2605.
45. Woo S.H., Cleemann L., Morad M. Ca2+ current-gated focal and local Ca2+ release in rat atrial myocytes: evidence from rapid 2-D confocal imaging. J. Physiol. 2002, 543:439-453.
46. Berlin J.R. Spatiotemporal changes of Ca2+ during electrically evoked contractions in atrial and ventricular cells. Am. J. Physiol. 1995, 269:H1165-1170.
47. Lipp P., Pott L., Callewaert G., Carmeliet E. Simultaneous recording of Indo-1 fluorescence and Na+/Ca2+ exchange current reveals two components of Ca2(+)-release from sarcoplasmic reticulum of cardiac atrial myocytes. FEBS Lett. 1990, 275:181-184.
48. Sheehan K.A., Blatter L.A. Regulation of junctional and non-junctional sarcoplasmic reticulum calcium release in excitation-contraction coupling in cat atrial myocytes. J. Physiol. 2003, 546:119-135.
49. Huser J., Lipsius S.L., Blatter L.A. Calcium gradients during excitation-contraction coupling in cat atrial myocytes. J. Physiol. 1996, 494(Pt 3):641-651.
50. Bootman M., Niggli E., Berridge M., Lipp P. Imaging the hierarchical Ca2+ signalling system in HeLa cells. J. Physiol. 1997, 499(Pt 2):307-314.
51. Coombes S., Hinch R., Timofeeva Y. Receptors, sparks and waves in a fire-diffuse-fire framework for calcium release. Prog. Biophys. Mol. Biol. 2004, 85:197-216.
52. Keizer J., Smith G.D., Ponce-Dawson S., Pearson J.E. Saltatory propagation of Ca2+ waves by Ca2+ sparks. Biophys. J. 1998, 75:595-600.
53. Izu L.T., Means S.A., Shadid J.N., Chen-Izu Y., Balke C.W. Interplay of ryanodine receptor distribution and calcium dynamics. Biophys. J. 2006, 91:95-112.
54. Diaz M.E., Graham H.K., O'Neill Test C. article sample title placed here. Cell Calcium 2005, 38:391-396.
55. Landgraf G., Gellerich F.N., Wussling M.H. Inhibitors of SERCA and mitochondrial Ca-uniporter decrease velocity of calcium waves in rat cardiomyocytes. Mol. Cell. Biochem. 2004, 256-257:379-386.
56. Gunter T.E., Yule D.I., Gunter K.K., Eliseev R.A., Salter J.D. Calcium and mitochondria. FEBS Lett. 2004, 567:96-102.
57. Lipp P., Laine M., Tovey S.C., Burrell K.M., Berridge M.J., Li W., Bootman M.D. Functional InsP3 receptors that may modulate excitation-contraction coupling in the heart. Curr. Biol. 2000, 10:939-942.
58. Woo S.H., Cleemann L., Morad M. Spatiotemporal characteristics of junctional and nonjunctional focal Ca2+ release in rat atrial myocytes. Circ. Res. 2003, 92:e1-11.
59. Woo S.H., Soldatov N.M., Morad M. Modulation of Ca2+ signalling in rat atrial myocytes: possible role of the alpha1C carboxyl terminal. J. Physiol. 2003, 552:437-447.
60. van der Heyden M.A., Wijnhoven T.J., Opthof T. Molecular aspects of adrenergic modulation of cardiac L-type Ca2+ channels. Cardiovasc. Res. 2005, 65:28-39.
61. Frank K.F., Bolck B., Erdmann E., Schwinger R.H. Sarcoplasmic reticulum Ca2+-ATPase modulates cardiac contraction and relaxation. Cardiovasc. Res. 2003, 57:20-27.
62. Koizumi S., Lipp P., Berridge M.J., Bootman M.D. Regulation of ryanodine receptor opening by lumenal Ca(2+) underlies quantal Ca(2+) release in PC12 cells. J. Biol. Chem. 1999, 274:33327-33333.
63. Laver D.R. Coupled calcium release channels and their regulation by luminal and cytosolic ions. Eur. Biophys. J. 2005, 34:359-368.
64. Bassani J.W., Yuan W., Bers D.M. Fractional SR Ca release is regulated by trigger Ca and SR Ca content in cardiac myocytes. Am. J. Physiol. 1995, 268:C1313-1319.
65. Gyorke S., Gyorke I., Terentyev D., Viatchenko-Karpinski S., Williams S.C. Modulation of sarcoplasmic reticulum calcium release by calsequestrin in cardiac myocytes. Biol. Res. 2004, 37:603-607.
66. Beard N.A., Casarotto M.G., Wei L., Varsanyi M., Laver D.R., Dulhunty A.F. Regulation of ryanodine receptors by calsequestrin: effect of high luminal Ca2+ and phosphorylation. Biophys. J. 2005, 88:3444-3454.
67. Stevens S.C., Terentyev D., Kalyanasundaram A., Periasamy M., Gyorke S. Intra-sarcoplasmic reticulum Ca2+ oscillations are driven by dynamic regulation of ryanodine receptor function by luminal Ca2+ in cardiomyocytes. J. Physiol. 2009, 587:4863-4872.
68. Kockskamper J., Zima A.V., Roderick H.L., Pieske B., Blatter L.A., Bootman M.D. Emerging roles of inositol 1, 4, 5-trisphosphate signaling in cardiac myocytes. J. Mol. Cell. Cardiol. 2008, 45:128-147.
69. Bootman M.D., Roderick H.L. Why, where, and when do cardiac myocytes express inositol 1, 4, 5-trisphosphate receptors?. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H579-581.
70. Cardenas C., Escobar M., Garcia A., Osorio-Reich M., Hartel S., Foskett J.K., Franzini-Armstrong C. Visualization of inositol 1, 4, 5-trisphosphate receptors on the nuclear envelope outer membrane by freeze-drying and rotary shadowing for electron microscopy. J. Struct. Biol. 2010, 171:372-381.
71. Li X., Zima A.V., Sheikh F., Blatter L.A., Chen J. Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1, 4, 5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ. Res. 2005, 96:1274-1281.
72. Wu X., Zhang T., Bossuyt J., Li X., McKinsey T.A., Dedman J.R., Olson E.N., Chen J., Brown J.H., Bers D.M. Local InsP3-dependent perinuclear Ca2+ signaling in cardiac myocyte excitation-transcription coupling. J. Clin. Invest. 2006, 116:675-682.
73. Proven A., Roderick H.L., Conway S.J., Berridge M.J., Horton J.K., Capper S.J., Bootman M.D. Inositol 1, 4, 5-trisphosphate supports the arrhythmogenic action of endothelin-1 on ventricular cardiac myocytes. J. Cell Sci. 2006, 119:3363-3375.
74. Roderick H.L., Bootman M.D. Pacemaking, arrhythmias, inotropy and hypertrophy: the many possible facets of IP3 signalling in cardiac myocytes. J. Physiol. 2007, 581:883-884.
75. Bootman M.D., Harzheim D., Smyrnias I., Conway S.J., Roderick H.L. Temporal changes in atrial EC-coupling during prolonged stimulation with endothelin-1. Cell Calcium 2007, 42:489-501.
76. Mackenzie L., Roderick H.L., Proven A., Conway S.J., Bootman M.D. Inositol 1, 4, 5-trisphosphate receptors in the heart. Biol. Res. 2004, 37:553-557.
77. Woodcock E.A., Matkovich S.J. Ins(1, 4, 5)P3 receptors and inositol phosphates in the heart-evolutionary artefacts or active signal transducers?. Pharmacol. Ther. 2005, 107:240-251.
78. Liang X., Xie H., Zhu P.H., Hu J., Zhao Q., Wang C.S., Yang C. Enhanced activity of inositol-1, 4, 5-trisphosphate receptors in atrial myocytes of atrial fibrillation patients. Cardiology 2009, 114:180-191.
79. Xiao J., Liang D., Zhao H., Liu Y., Zhang H., Lu X., Li J., Peng L., Chen Y.H. 2-Aminoethoxydiphenyl borate, a inositol 1, 4, 5-triphosphate receptor inhibitor, prevents atrial fibrillation. Exp. Biol. Med. Maywood 2010, 235:862-868.
80. Go L.O., Moschella M.C., Watras J., Handa K.K., Fyfe B.S., Marks A.R. Differential regulation of two types of intracellular calcium release channels during end-stage heart failure. J. Clin. Invest. 1995, 95:888-894.
81. Harzheim D., Movassagh M., Foo R.S., Ritter O., Tashfeen A., Conway S.J., Bootman M.D., Roderick H.L. Increased InsP3Rs in the junctional sarcoplasmic reticulum augment Ca2+ transients and arrhythmias associated with cardiac hypertrophy. Proc. Natl Acad. Sci. USA 2009, 106:11406-11411.
82. Higazi D.R., Fearnley C.J., Drawnel F.M., Talasila A., Corps E.M., Ritter O., McDonald F., Mikoshiba K., Bootman M.D., Roderick H.L. Endothelin-1-stimulated InsP3-induced Ca2+ release is a nexus for hypertrophic signaling in cardiac myocytes. Mol. Cell 2009, 33:472-482.
83. Harzheim D., Talasila A., Movassagh M., Foo R.S., Figg N., Bootman M.D., Roderick H.L. Elevated InsP(3)R expression underlies enhanced calcium fluxes and spontaneous extra-systolic calcium release events in hypertrophic cardiac myocytes. Channels (Austin) 2010, 4:67-71.
84. Luss I., Boknik P., Jones L.R., Kirchhefer U., Knapp J., Linck B., Luss H., Meissner A., Muller F.U., Schmitz W., Vahlensieck U., Neumann J. Expression of cardiac calcium regulatory proteins in atrium v ventricle in different species. J. Mol. Cell. Cardiol. 1999, 31:1299-1314.
85. Walden A.P., Dibb K.M., Trafford A.W. Differences in intracellular calcium homeostasis between atrial and ventricular myocytes. J. Mol. Cell. Cardiol. 2008.
86. He H., Giordano F.J., Hilal-Dandan R., Choi D.J., Rockman H.A., McDonough P.M., Bluhm W.F., Meyer M., Sayen M.R., Swanson E., Dillmann W.H. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J. Clin. Invest. 1997, 100:380-389.
87. Jorgensen A.O., Shen A.C., Campbell K.P. Ultrastructural localization of calsequestrin in adult rat atrial and ventricular muscle cells. J. Cell Biol. 1985, 101:257-268.
88. Minamisawa S., Wang Y., Chen J., Ishikawa Y., Chien K.R., Matsuoka R. Atrial chamber-specific expression of sarcolipin is regulated during development and hypertrophic remodeling. J. Biol. Chem. 2003, 278:9570-9575.
89. Uemura N., Ohkusa T., Hamano K., Nakagome M., Hori H., Shimizu M., Matsuzaki M., Mochizuki S., Minamisawa S., Ishikawa Y. Down-regulation of sarcolipin mRNA expression in chronic atrial fibrillation. Eur. J. Clin. Invest. 2004, 34:723-730.
90. Kirk M.M., Izu L.T., Chen-Izu Y., McCulle S.L., Wier W.G., Balke C.W., Shorofsky S.R. Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes. J. Physiol. 2003, 547:441-451.
91. Lenaerts I., Bito V., Heinzel F.R., Driesen R.B., Holemans P., D'Hooge J., Heidbuchel H., Sipido K.R., Willems R. Ultrastructural and functional remodeling of the coupling between Ca2+ influx and sarcoplasmic reticulum Ca2+ release in right atrial myocytes from experimental persistent atrial fibrillation. Circ. Res. 2009, 105:876-885.
92. Dibb K.M., Clarke J.D., Horn M.A., Richards M.A., Graham H.K., Eisner D.A., Trafford A.W. Characterization of an extensive transverse tubular network in sheep atrial myocytes and its depletion in heart failure. Circ. Heart Fail. 2009, 2:482-489.
93. Wakili R., Yeh Y.H., Yan Qi X., Greiser M., Chartier D., Nishida K., Maguy A., Villeneuve L.R., Boknik P., Voigt N., Krysiak J., Kaab S., Ravens U., Linke W.A., Stienen G.J., Shi Y., Tardif J.C., Schotten U., Dobrev D., Nattel S. Multiple potential molecular contributors to atrial hypocontractility caused by atrial tachycardia remodeling in dogs. Circ. Arrhythm. Electrophysiol. 2010, 3:530-541.
94. Freestone N.S., HJahangiri M., MKaminisky Y., Bolton T., Gordienko D. Human atrial cell morphology is linked to heterogeneous distribution of Ca2+ sparks. Proc. Life Sci. 2007, PC342.
95. Woo S.H., Cleemann L., Morad M. Diversity of atrial local Ca2+ signalling: evidence from 2-D confocal imaging in Ca2+-buffered rat atrial myocytes. J. Physiol. 2005, 567:905-921.
96. Miura M., Nishio T., Hattori T., Murai N., Stuyvers B.D., Shindoh C., Boyden P.A. Effect of nonuniform muscle contraction on sustainability and frequency of triggered arrhythmias in rat cardiac muscle. Circulation 2010, 121:2711-2717.
97. Cordeiro J.M., Spitzer K.W., Giles W.R., Ershler P.E., Cannell M.B., Bridge J.H. Location of the initiation site of calcium transients and sparks in rabbit heart Purkinje cells. J. Physiol. 2001, 531:301-314.
98. Boyden P.A., Pu J., Pinto J., Keurs H.E. Ca(2+) transients and Ca(2+) waves in purkinje cells: role in action potential initiation. Circ. Res. 2000, 86:448-455.
99. Boyden P.A., Hirose M., Dun W. Cardiac Purkinje cells. Heart Rhythm 2010, 7:127-135.
100. Di Maio A., Ter Keurs H.E., Franzini-Armstrong C. T-tubule profiles in Purkinje fibres of mammalian myocardium. J. Muscle Res. Cell Motil. 2007, 28:115-121.
101. Stuyvers B.D., Dun W., Matkovich S., Sorrentino V., Boyden P.A., ter Keurs H.E. Ca2+ sparks and waves in canine purkinje cells: a triple layered system of Ca2+ activation. Circ. Res. 2005, 97:35-43.
102. Robinson R.B. The long and short of calcium-dependent automaticity in the sinoatrial node. Am. J. Physiol. Heart Circ. Physiol. 2011, 300:H31-32.
103. Lakatta E.G., Maltsev V.A., Vinogradova T.M. A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circ. Res. 2010, 106:659-673.
104. Lipsius S.L., Huser J., Blatter L.A. Intracellular Ca2+ release sparks atrial pacemaker activity. News Physiol. Sci. 2001, 16:101-106.
105. Mackenzie L., Bootman M.D., Laine M., Berridge M.J., Thuring J., Holmes A., Li W.H., Lipp P. The role of inositol 1, 4, 5-trisphosphate receptors in Ca(2+) signalling and the generation of arrhythmias in rat atrial myocytes. J. Physiol. 2002, 541:395-409.
106. Chen B., Wu Y., Mohler P.J., Anderson M.E., Song L.S. Local control of Ca2+-induced Ca2+ release in mouse sinoatrial node cells. J. Mol. Cell. Cardiol. 2009, 47:706-715.
107. Huser J., Blatter L.A., Lipsius S.L. Intracellular Ca2+ release contributes to automaticity in cat atrial pacemaker cells. J. Physiol. 2000, 524(Pt 2):415-422.
108. Balijepalli R.C., Lokuta A.J., Maertz N.A., Buck J.M., Haworth R.A., Valdivia H.H., Kamp T.J. Depletion of T-tubules and specific subcellular changes in sarcolemmal proteins in tachycardia-induced heart failure. Cardiovasc. Res. 2003, 59:67-77.
109. He J., Conklin M.W., Foell J.D., Wolff M.R., Haworth R.A., Coronado R., Kamp T.J. Reduction in density of transverse tubules and L-type Ca(2+) channels in canine tachycardia-induced heart failure. Cardiovasc. Res. 2001, 49:298-307.
110. Wei S., Guo A., Chen B., Kutschke W., Xie Y.P., Zimmerman K., Weiss R.M., Anderson M.E., Cheng H., Song L.S. T-tubule remodeling during transition from hypertrophy to heart failure. Circ. Res. 2010, 107:520-531.
111. Louch W.E., Bito V., Heinzel F.R., Macianskiene R., Vanhaecke J., Flameng W., Mubagwa K., Sipido K.R. Reduced synchrony of Ca2+ release with loss of T-tubules-a comparison to Ca2+ release in human failing cardiomyocytes. Cardiovasc. Res. 2004, 62:63-73.
112. Song L.S., Sobie E.A., McCulle S., Lederer W.J., Balke C.W., Cheng H. Orphaned ryanodine receptors in the failing heart. Proc. Natl Acad. Sci. USA 2006, 103:4305-4310.
113. Brette F., Rodriguez P., Komukai K., Colyer J., Orchard C.H. beta-adrenergic stimulation restores the Ca transient of ventricular myocytes lacking t-tubules. J. Mol. Cell. Cardiol. 2004, 36:265-275.
114. Lipp P., Huser J., Pott L., Niggli E. Spatially non-uniform Ca2+ signals induced by the reduction of transverse tubules in citrate-loaded guinea-pig ventricular myocytes in culture. J. Physiol. 1996, 497(Pt 3):589-597.
115. Hammer K., Ruppenthal S., Viero C., Scholz A., Edelmann L., Kaestner L., Lipp P. Remodelling of Ca2+ handling organelles in adult rat ventricular myocytes during long term culture. J. Mol. Cell. Cardiol. 2010, 49:427-437.
116. Sedarat F., Xu L., Moore E.D., Tibbits G.F. Colocalization of dihydropyridine and ryanodine receptors in neonate rabbit heart using confocal microscopy. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H202-209.
117. Chen F., Mottino G., Klitzner T.S., Philipson K.D., Frank J.S. Distribution of the Na+/Ca2+ exchange protein in developing rabbit myocytes. Am. J. Physiol. 1995, 268:C1126-1132.
118. Haddock P.S., Coetzee W.A., Cho E., Porter L., Katoh H., Bers D.M., Jafri M.S., Artman M. Subcellular [Ca2+]i gradients during excitation-contraction coupling in newborn rabbit ventricular myocytes. Circ. Res. 1999, 85:415-427.
119. Perez C.G., Copello J.A., Li Y., Karko K.L., Gomez L., Ramos-Franco J., Fill M., Escobar A.L., Mejia-Alvarez R. Ryanodine receptor function in newborn rat heart. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H2527-2540.
120. Shiels H.A., White E. Temporal and spatial properties of cellular Ca2+ flux in trout ventricular myocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R1756-1766.
121. Protasi F., Sun X.H., Franzini-Armstrong C. Formation and maturation of the calcium release apparatus in developing and adult avian myocardium. Dev. Biol. 1996, 173:265-278.
122. Sommer J.R., Jennings R.B. Ultrastructure of cardic muscle 1992, Raven Press Ltd.
123. Franzini-Armstrong C., Protasi F., Tijskens P. The assembly of calcium release units in cardiac muscle. Ann. NY Acad. Sci. 2005, 1047:76-85.