Cardiac myocytes and local signaling in nano-domains

Progress in Biophysics and Molecular Biology

Volumn 107, Issue 1, 2011, Pages 48-59

  Winslow, Raimond L ^a   Greenstein, Joseph L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac myocyte; Computational modeling; Excitation contraction coupling; Local signaling domain; Multi scale modeling

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL L TYPE; CALMODULIN;

ANIMAL; CALCIUM SIGNALING; CYTOLOGY; ENZYMOLOGY; HEART MUSCLE CELL; HUMAN; METABOLISM; REVIEW;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALMODULIN; HUMANS; MYOCYTES, CARDIAC; RECEPTORS, ADRENERGIC, BETA;

EID: 80053586910     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2011.06.005     Document Type: Review

References (109)

1. Ackerman M.J., Mohler P.J. Defining a new paradigm for human arrhythmia syndromes: phenotypic manifestations of gene mutations in ion channel- and transporter-associated proteins. Circ. Res. 2010, 107:457-465.
2. Ahrens-Nicklas R.C., Clancy C.E., Christini D.J. Re-evaluating the efficacy of β-adrenergic agonists and antagonists in long QT-3 syndrome through computational modelling. Cardiovasc. Res. 2009, 82:439-447.
3. 2+ leak in heart failure. Circ. Res. 2005, 97:1314-1322.
4. Anderson M.E., Mohler P.J. Rescuing a failing heart: think globally, treat locally. Nat. Med. 2009, 15:25-26.
5. Baddeley D., Jayasinghe I.D., Lam L., Rossberger S., Cannell M.B., Soeller C. Optical single-channel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes. Proc. Natl. Acad. Sci. U S A 2009, 106:22275-22280.
6. Balaban R.S. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J. Mol. Cell. Cardiol. 2002, 34:1259-1271.
7. Beard D.A. A biophysical model of the mitochondrial respiratory system and oxidative phosphorylation. PLoS Comput. Biol. 2005, 1:e36.
8. Bers D.M. Excitation-contraction coupling and Cardiac Contractile Force 2001, Kluwer, Boston.
9. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
10. Bers D.M. Calcium cycling and signaling in cardiac myocytes. Annu. Rev. Physiol. 2008, 70:23-49.
11. Bers D.M., Despa S. Na/K-ATPase-an integral player in the adrenergic fight-or-flight response. Trends Cardiovasc. Med. 2009, 19:111-118.
12. Bhalla U.S. Signaling in small subcellular volumes. I. Stochastic and diffusion effects on individual pathways. Biophys. J. 2004, 87:733-744.
13. Bouchard R.A., Clark R.B., Giles W.R. Role of sodium-calcium exchange in activation of contraction in rat ventricle. J. Physiol. 1993, 472:391-413.
14. Chance B., Williams G.R. Method for the localization of sites for oxidative phosphorylation. Nature 1955, 176:250-254.
15. Cheng H., Lederer W.J., Cannell M.B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993, 262:740-744.
16. Cooper J., Mirams G.R., Niederer S.A. High throughput functional curation of cellular electrophysiology models. Prog. Biophys. Mol. Biol. 2011, 107:11-20.
17. Cortassa S., Aon M.A., Marban E., Winslow R.L., O'Rourke B. An integrated model of cardiac mitochondrial energy metabolism and calcium dynamics. Biophys. J. 2003, 84:2734-2755.
18. Cortassa S., Aon M.A., O'Rourke B., Jacques R., Tseng H.J., Marban E., Winslow R.L. A computational model integrating electrophysiology, contraction, and mitochondrial bioenergetics in the ventricular myocyte. Biophys. J. 2006, 91:1564-1589.
19. Cortassa S., O'Rourke B., Winslow R.L., Aon M.A. Control and regulation of mitochondrial energetics in an integrated model of cardiomyocyte function. Biophys. J. 2009, 96:2466-2478.
20. Csordas G., Renken C., Varnai P., Walter L., Weaver D., Buttle K.F., Balla T., Mannella C.A., Hajnoczky G. Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 2006, 174:915-921.
21. Cunha S.R., Mohler P.J. Ankyrin protein networks in membrane formation and stabilization. J. Cell. Mol. Med. 2009, 13:4364-4376.
22. Cunha S.R., Bhasin N., Mohler P.J. Targeting and stability of Na/Ca exchanger 1 in cardiomyocytes requires direct interaction with the membrane adaptor ankyrin-B. J. Biol. Chem. 2007, 282:4875-4883.
23. Currie S., Loughrey C.M., Craig M.A., Smith G.L. Calcium/calmodulin-dependent protein kinase II delta associates with the ryanodine receptor complex and regulates channel function in rabbit heart. Biochem. J. 2004, 377:357-366.
24. Dash R.K., Qi F., Beard D.A. A biophysically based mathematical model for the kinetics of mitochondrial calcium uniporter. Biophys. J. 2009, 96:1318-1332.
25. Despa S., Tucker A.L., Bers D.M. Phospholemman-mediated activation of Na/K-ATPase limits [Na]i and inotropic state during beta-adrenergic stimulation in mouse ventricular myocytes. Circulation 2008, 117:1849-1855.
26. 2+ selectivity in the calmodulin regulation of CaV channels. Nature 2008, 451:830-834.
27. El-Armouche A., Eschenhagen T. Beta-adrenergic stimulation and myocardial function in the failing heart. Heart Fail. Rev. 2009, 14:225-241.
28. Erickson M.G., Alseikhan B.A., Peterson B.Z., Yue D.T. Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells. Neuron 2001, 31:973-985.
29. Faber G.M., Rudy Y. Action potential and contractility changes in [Na(+)](i) overloaded cardiac myocytes: a simulation study. Biophys. J. 2000, 78:2392-2404.
30. Franzini-Armstrong C., Protasi F., Ramesh V. Shape, size, and distribution of Ca(2+) release units and couplons in skeletal and cardiac muscles. Biophys. J. 1999, 77:1528-1539.
31. 2+ signaling. Am. J. Physiol. Cell Physiol. 2003, 284:C475-C486.
32. Grandi E., Puglisi J.L., Wagner S., Maier L.S., Severi S., Bers D.M. Simulation of Ca-calmodulin-dependent protein kinase II on rabbit ventricular myocyte ion currents and action potentials. Biophys. J. 2007, 93:3835-3847.
33. 2+ release. Biophys. J. 2002, 83:2918-2945.
34. Greenstein J.L., Tanskanen A.J., Winslow R.L. Modeling the actions of beta-adrenergic signaling on excitation-contraction coupling processes. Ann. N. Y. Acad. Sci. 2004, 1015:16-27.
35. Greenstein J.L., Hinch R., Winslow R.L. Mechanisms of excitation-contraction coupling in an integrative model of the cardiac ventricular myocyte. Biophys. J. 2006, 90:77-91.
36. 2+ ions in the dyadic cleft; continuous versus random walk description of diffusion. Biophys. J. 2008, 94:4184-4201.
37. Hashambhoy Y.L., Winslow R.L., Greenstein J.L. CaMKII-induced shift in modal gating explains L-type Ca(2+) current facilitation: a modeling study. Biophys. J. 2009, 96:1770-1785.
38. Hashambhoy Y.L., Greenstein J.L., Winslow R.L. Role of CaMKII in RyR leak, EC coupling and action potential duration: a computational model. J. Mol. Cell. Cardiol. 2010, 49:617-624.
39. 2+ signaling in the heart. J. Cell Sci. 2009, 122:1005-1013.
40. Hilgemann D.W., Collins A., Matsuoka S. Steady-state and dynamic properties of cardiac sodium-calcium exchange. Secondary modulation by cytoplasmic calcium and ATP. J. Gen. Physiol. 1992, 100:933-961.
41. Hinch R., Greenstein J.L., Tanskanen A.J., Xu L., Winslow R.L. A simplified local control model of calcium-induced calcium release in cardiac ventricular myocytes. Biophys. J. 2004, 87:3723-3736.
42. Hinch R., Greenstein J.L., Winslow R.L. Multi-scale models of local control of calcium induced calcium release. Prog. Biophys. Mol. Biol. 2006, 90:136-150.
43. 2+ signals for facilitation. J. Cell Biol. 2005, 171:537-547.
44. Iancu R.V., Jones S.W., Harvey R.D. Compartmentation of cAMP signaling in cardiac myocytes: a computational study. Biophys. J. 2007, 92:3317-3331.
45. 2+ dynamics: the roles of ryanodine receptor adaptation and sarcoplasmic reticulum load. Biophys. J. 1998, 74:1149-1168.
46. Jayasinghe I.D., Cannell M.B., Soeller C. Organization of ryanodine receptors, transverse tubules, and sodium-calcium exchanger in rat myocytes. Biophys. J. 2009, 97:2664-2673.
47. Katsnelson L.B., Solovyova O., Balakin A., Lookin O., Konovalov P., Protsenko Y., Sulman T., Markhasin V.S. Contribution of mechanical factors to arrhythmogenesis in calcium overloaded cardiomyocytes: model predictions and experiments. Prog. Biophys. Mol. Biol. 2011, 107:81-89.
48. Kizhatil K., Sandhu N.K., Peachey N.S., Bennett V. Ankyrin-B is required for coordinated expression of beta-2-spectrin, the Na/K-ATPase and the Na/Ca exchanger in the inner segment of rod photoreceptors. Exp. Eye Res. 2009, 88:57-64.
49. Kline C.F., Cunha S.R., Lowe J.S., Hund T.J., Mohler P.J. Revisiting ankyrin-InsP(3) receptor interactions: ankyrin-B associates with the cytoplasmic N-terminus of the InsP(3) receptor. J. Cell. Biochem. 2008, 104:1244-1253.
50. - homeostasis during beta 1-adrenergic stimulation of cardiac myocyte. Prog. Biophys. Mol. Biol. 2008, 96:171-186.
51. Langer G.A., Peskoff A. Calcium concentration and movement in the diadic cleft space of the cardiac ventricular cell. Biophys. J. 1996, 70:1169-1182.
52. 2+ transient: evidence from NCX knockout mice. J. Physiol. 2010, 588:3267-3276.
53. Litwin S.E., Li J., Bridge J.H. Na-Ca exchange and the trigger for sarcoplasmic reticulum Ca release: studies in adult rabbit ventricular myocytes. Biophys. J. 1998, 75:359-371.
54. Liu X., Spicarova Z., Rydholm S., Li J., Brismar H., Aperia A. Ankyrin B modulates the function of Na, K-ATPase/inositol 1,4,5-trisphosphate receptor signaling microdomain. J. Biol. Chem. 2008, 283:11461-11468.
55. Lohn M., Furstenau M., Sagach V., Elger M., Schulze W., Luft F.C., Haller H., Gollasch M. Ignition of calcium sparks in arterial and cardiac muscle through caveolae. Circ. Res. 2000, 87:1034-1039.
56. Maack C., O'rourke B. Excitation-contraction coupling and mitochondrial energetics. Basic Res. Cardiol. 2007, 102:369-392.
57. 2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 2006, 99:172-182.
58. 2+/calmodulin-dependent protein kinase (CaMK) in excitation-contraction coupling in the heart. Cardiovasc. Res. 2007, 73:631-640.
59. Matsuoka S., Jo H., Sarai N., Noma A. An in silico study of energy metabolism in cardiac excitation-contraction coupling. Jpn. J. Physiol. 2004, 54:517-522.
60. Matsuoka S., Sarai N., Jo H., Noma A. Simulation of ATP metabolism in cardiac excitation-contraction coupling. Prog. Biophys. Mol. Biol. 2004, 85:279-299.
61. Modchang C., Nadkarni S., Bartol T.M., Triampo W., Sejnowski T.J., Levine H., Rappel W.J. A comparison of deterministic and stochastic simulations of neuronal vesicle release models. Phys. Biol. 2010, 7:026008.
62. Mohler P.J., Wehrens X.H. Mechanisms of human arrhythmia syndromes: abnormal cardiac macromolecular interactions. Physiology (Bethesda) 2007, 22:342-350.
63. Mohler P.J., Schott J.J., Gramolini A.O., Dilly K.W., Guatimosim S., duBell W.H., Song L.S., Haurogne K., Kyndt F., Ali M.E., Rogers T.B., Lederer W.J., Escande D., Le Marec H., Bennett V. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 2003, 421:634-639.
64. Mohler P.J., Davis J.Q., Bennett V. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol. 2005, 3:e423.
65. Neco P., Rose B., Huynh N., Zhang R., Bridge J.H., Philipson K.D., Goldhaber J.I. Sodium-calcium exchange is essential for effective triggering of calcium release in mouse heart. Biophys. J. 2010, 99:755-764.
66. Ostrom R.S., Gregorian C., Drenan R.M., Xiang Y., Regan J.W., Insel P.A. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem. 2001, 276:42063-42069.
67. Perkins G.A., Renken C.W., Frey T.G., Ellisman M.H. Membrane architecture of mitochondria in neurons of the central nervous system. J. Neurosci. Res. 2001, 66:857-865.
68. Puglisi J.L., Bers D.M. LabHEART: an interactive computer model of rabbit ventricular myocyte ion channels and Ca transport. Am. J. Physiol. Cell Physiol. 2001, 281:C2049-C2060.
69. Risken H. The Fokker-Planck Equation 1997, Springer, Berlin.
70. 2+ responses. Science 1998, 280:1763-1766.
71. 2+ channels in guinea-pig heart cells. J. Physiol. 1992, 456:267-284.
72. Rovetti R., Cui X., Garfinkel A., Weiss J.N., Qu Z. Spark-induced sparks as a mechanism of intracellular calcium alternans in cardiac myocytes. Circ. Res. 2010, 106:1582-1591.
73. Ruehr M.L., Russell M.A., Bond M. A-kinase anchoring protein targeting of protein kinase A in the heart. J. Mol. Cell. Cardiol. 2004, 37:653-665.
74. 2+ in cardiac myocytes. Biophys. J. 2008, 95:4597-4612.
75. Saucerman J.J., McCulloch A.D. Cardiac beta-adrenergic signaling: from subcellular microdomains to heart failure. Ann. N. Y. Acad. Sci. 2006, 1080:348-361.
76. Saucerman J.J., Brunton L.L., Michailova A.P., McCulloch A.D. Modeling beta-adrenergic control of cardiac myocyte contractility in silico. J. Biol. Chem. 2003, 278:47997-48003.
77. Saucerman J.J., Zhang J., Martin J.C., Peng L.X., Stenbit A.E., Tsien R.Y., McCulloch A.D. Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc. Natl. Acad. Sci. U S A 2006, 103:12923-12928.
78. Scarpa A., Graziotti P. Mechanisms for intracellular calcium regulation in heart. I. Stopped-flow measurements of Ca++ uptake by cardiac mitochondria. J. Gen. Physiol. 1973, 62:756-772.
79. Scriven D.R., Dan P., Moore E.D. Distribution of proteins implicated in excitation-contraction coupling in rat ventricular myocytes. Biophys. J. 2000, 79:2682-2691.
80. 2+ signals by mitochondria in cat ventricular myocytes. Am. J. Physiol. Cell Physiol. 2006, 291:C840-C850.
81. 2+ release channel at 14 A resolution. J. Mol. Biol. 2005, 345:427-431.
82. 2+ exchange. Science 1992, 255:850-853.
83. 2+ release by a local inactivation of ryanodine receptors in cardiac myocytes. Proc. Natl. Acad. Sci. U S A 1998, 95:15096-15101.
84. Shannon T.R., Ginsburg K.S., Bers D.M. Reverse mode of the sarcoplasmic reticulum calcium pump and load-dependent cytosolic calcium decline in voltage-clamped cardiac ventricular myocytes. Biophys. J. 2000, 78:322-333.
85. Shannon T.R., Wang F., Puglisi J., Weber C., Bers D.M. A mathematical treatment of integrated Ca dynamics within the ventricular myocyte. Biophys. J. 2004, 87:3351-3371.
86. 2+ exchange. Circ. Res. 1997, 81:1034-1044.
87. 2+ release in ventricular myocytes. Biophys. J. 2008, 94:L54-L56.
88. Soeller C., Cannell M.B. Numerical simulation of local calcium movements during L-type calcium channel gating in the cardiac diad. Biophys. J. 1997, 73:97-111.
89. Soeller C., Cannell M.B. Analysing cardiac excitation-contraction coupling with mathematical models of local control. Prog. Biophys. Mol. Biol. 2004, 85:141-162.
90. Song L.S., Wang S.Q., Xiao R.P., Spurgeon H., Lakatta E.G., Cheng H. Beta-adrenergic stimulation synchronizes intracellular Ca(2+) release during excitation-contraction coupling in cardiac myocytes. Circ. Res. 2001, 88:794-801.
91. Sosinsky G.E., Deerinck T.J., Greco R., Buitenhuys C.H., Bartol T.M., Ellisman M.H. Development of a model for microphysiological simulations: small nodes of Ranvier from peripheral nerves of mice reconstructed by electron tomography. Neuroinformatics 2005, 3:133-162.
92. Stern M.D. Theory of excitation-contraction coupling in cardiac muscle. Biophys. J. 1992, 63:497-517.
93. Stern M.D., Song L.S., Cheng H., Sham J.S., Yang H.T., Boheler K.R., Rios E. Local control models of cardiac excitation-contraction coupling. A possible role for allosteric interactions between ryanodine receptors. J. Gen. Physiol. 1999, 113:469-489.
94. Su Z., Sugishita K., Ritter M., Li F., Spitzer K.W., Barry W.H. The sodium pump modulates the influence of I-Na on [Ca2+](i) transients in mouse ventricular myocytes. Biophys. J. 2001, 80:1230-1237.
95. Swift F., Tovsrud N., Enger U.H., Sjaastad I., Sejersted O.M. The Na+/K+-ATPase alpha2-isoform regulates cardiac contractility in rat cardiomyocytes. Cardiovasc. Res. 2007, 75:109-117.
96. 2+ channel. Cell 2008, 133:1228-1240.
97. Tanskanen A., Winslow R.L. Integrative, structurally-detailed model of calcium dynamics in the cardiac diad. SIAM J. Multiscale Model. Simul. 2006, 5:1280-1296.
98. 2+ channels on early after-depolarizations. Biophys. J. 2005, 88:85-95.
99. Tanskanen A.J., Greenstein J.L., Chen A., Sun S.X., Winslow R.L. Protein geometry and placement in the cardiac dyad influence macroscopic properties of calcium-induced calcium release. Biophys. J. 2007, 92:3379-3396.
100. 2+ exchanger-mediated relaxation in rabbit ventricular myocytes. J. Physiol. 2001, 533:165-173.
101. Territo P.R., French S.A., Dunleavy M.C., Evans F.J., Balaban R.S. Calcium activation of heart mitochondrial oxidative phosphorylation - rapid kinetics of m(V) over dot (O2), NADH, and light scattering. J. Biol. Chem. 2001, 276:2586-2599.
102. 2+-exchanger in normal and detubulated rat cardiomyocytes. J. Mol. Cell. Cardiol. 2003, 35:1325-1337.
103. Wang H., Peskin C.S., Elston T.C. A robust numerical algorithm for studying biomolecular transport processes. J. Theor. Biol. 2003, 221.
104. Wang M.C., Collins R.F., Ford R.C., Berrow N.S., Dolphin A.C., Kitmitto A. The three-dimensional structure of the cardiac L-type voltage-gated calcium channel: comparison with the skeletal muscle form reveals a common architectural motif. J. Biol. Chem. 2004, 279:7159-7168.
105. 2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells. Proc. Natl. Acad. Sci. U S A 2004, 101:3979-3984.
106. 2+ exchange in activation of excitation-contraction coupling in rat ventricular myocytes. J. Physiol. 1996, 493(Pt 2):529-542.
107. 2+-bound calmodulin: an analysis of disorder and implications for functionally relevant plasticity. J. Mol. Biol. 2000, 301(5):1237-1256.
108. Yang J.H., Saucerman J.J. Computational models reduce complexity and accelerate insight into cardiac signaling networks. Circ. Res. 2011, 108:85-97.
109. 2+ exchange activity is localized in the T-tubules of rat ventricular myocytes. Circ. Res. 2002, 91:315-322.