Emerging mechanisms of T-tubule remodelling in heart failure

Cardiovascular Research

Volumn 98, Issue 2, 2013, Pages 204-215

  Guo, Ang ^a   Zhang, Caimei ^a   Wei, Sheng ^a   Chen, Biyi ^a   Song, Long Sheng ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Calcium; Excitation contraction coupling; Heart failure; Junctophilin 2; T tubules

Indexed keywords

CALCIUM;

CALCIUM TRANSPORT; CELL VOLUME; CONFOCAL MICROSCOPY; CONGESTIVE CARDIOMYOPATHY; DISEASE COURSE; DOWN REGULATION; EXCITATION CONTRACTION COUPLING; EXTRACELLULAR SPACE; HEART EJECTION FRACTION; HEART FAILURE; HEART HYPERTROPHY; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; ISCHEMIC CARDIOMYOPATHY; LEFT VENTRICULAR SYSTOLIC DYSFUNCTION; MEMBRANE DEPOLARIZATION; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PURKINJE FIBER; REVIEW; SIGNAL TRANSDUCTION; TRANSVERSE TUBULAR SYSTEM; UPREGULATION;

ANIMALS; CALCIUM; CARDIOMEGALY; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HUMANS; MYOCYTES, CARDIAC; SARCOPLASMIC RETICULUM;

EID: 84877299630     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt020     Document Type: Review

References (125)

1. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force. Boston: Kluwer Academic Publishers, 2001.
2. Stern MD. Theory of excitation-contraction coupling in cardiac muscle. Biophys J 1992;63:497-517.
3. Wang SQ, Song LS, Lakatta EG, Cheng H. Ca2+ signalling between single L-type Ca2+ channels and ryanodine receptors in heart cells. Nature 2001;410:592-596.
4. Sun XH, Protasi F, Takahashi M, Takeshima H, Ferguson DG, Franzini-Armstrong C. Molecular architecture of membranes involved in excitation-contraction coupling of cardiac muscle. J Cell Biol 1995;129:659-671.
5. Cheng H, Lederer WJ. Calcium sparks. Physiol Rev 2008;88:1491-1545.
6. Fawcett DW, McNutt NS. The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol 1969;42:1-45.
7. Huxley AF. The activation of striated muscle and its mechanical response. Proc R Soc Lond B Biol Sci 1971;178:1-27.
8. Lindner E. Submicroscopic morphology of the cardiac muscle. Z Zellforsch Mikrosk Anat 1957;45:702-746.
9. Simpson FO, Oertelis SJ. The fine structure of sheep myocardial cells; sarcolemmal invaginations and the transverse tubular system. J Cell Biol 1962;12:91-100.
10. Nelson DA, Benson ES. On the structural continuities of the transverse tubular system of rabbit and human myocardial cells. J Cell Biol 1963;16:297-313.
11. Simpson FO. The transverse tubular system in mammalian myocardial cells. Am J Anat 1965;117:1-17.
12. Sperelakis N, Rubio R. An orderly lattice of axial tubules which interconnect adjacent transverse tubules in guinea-pig ventricular myocardium. J Mol Cell Cardiol 1971;2:211-220.
13. Franzini-Armstrong C, Porter KR. Sarcolemmal invaginations constituting the T system in fish muscle fibers. J Cell Biol 1964;22:675-696.
14. Huxley AF, Taylor RE. Function of Krause's membrane. Nature 1955;176:1068.
15. Brette F, Orchard C. T-tubule function in mammalian cardiac myocytes. Circ Res 2003;92:1182-1192.
16. Song LS, Guatimosim S, Gomez-Viquez L, Sobie EA, Ziman A, Hartmann H et al. Calcium biology of the transverse tubules in heart. Ann NY Acad Sci 2005;1047: 99-111.
17. 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.
18. Ibrahim M, Gorelik J, Yacoub MH, Terracciano CM. The structure and function of cardiac t-tubules in health and disease. Proc Biol Sci 2011.
19. McNutt NS. Ultrastructure of the myocardial sarcolemma. Circ Res 1975;37:1-13.
20. Kostin S, Scholz D, Shimada T, Maeno Y, Mollnau H, Hein S et al. The internal and external protein scaffold of the T-tubular system in cardiomyocytes. Cell Tissue Res 1998;294:449-460.
21. Crossman DJ, Ruygrok PN, Soeller C, Cannell MB. Changes in the organization of excitation-contraction coupling structures in failing human heart. PLoS One 2011;6: e17901.
22. Soeller C, Cannell MB. Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. Circ Res 1999;84:266-275.
23. Song LS, Sobie EA, McCulle S, Lederer WJ, Balke CW, Cheng H. Orphaned ryanodine receptors in the failing heart. Proc Natl Acad Sci USA 2006;103:4305-4310.
24. Swift F, Franzini-Armstrong C, Oyehaug L, Enger UH, Andersson KB, Christensen G et al. Extreme sarcoplasmic reticulum volume loss and compensatory T-tubule remodeling after Serca2 knockout. Proc Natl Acad Sci USA 2012.
25. Wagner E, Lauterbach MA, Kohl T, Westphal V, Williams GS, Steinbrecher JH et al. Stimulated emission depletion live-cell super-resolution imaging shows proliferative remodeling of T-tubule membrane structures after myocardial infarction. Circ Res 2012;111:402-414.
26. Savio-Galimberti E, Frank J, Inoue M, Goldhaber JI, Cannell MB, Bridge JH et al. Novel features of the rabbit transverse tubular system revealed by quantitative analysis of three-dimensional reconstructions from confocal images. Biophys J 2008;95: 2053-2062.
27. Cannell MB, Crossman DJ, Soeller C. Effect of changes in action potential spike configuration, junctional sarcoplasmic reticulum micro-architecture and altered t-tubule structure in human heart failure. J Muscle Res Cell Motil 2006;27:297-306.
28. Page E, McCallister LP, Power B. Sterological measurements of cardiac ultrastructures implicated in excitation-contraction coupling. Proc Natl Acad Sci USA 1971; 68:1465-1466.
29. Stewart JM, Page E. Improved stereological techniques for studying myocardial cell growth: application to external sarcolemma, T system, and intercalated disks of rabbit and rat hearts. J Ultrastruct Res 1978;65:119-134.
30. Severs NJ, Slade AM, Powell T, Twist VW, Jones GE. Morphometric analysis of the isolated calcium-tolerant cardiac myocyte: organelle volumes, sarcomere length, plasma membrane surface folds, and intramembrane particle density and distribution. Cell Tissue Res 1985;240:159-168.
31. Page E, Surdyk-Droske M. Distribution, surface density, and membrane area of diadic junctional contacts between plasma membrane and terminal cisterns in mammalian ventricle. Circ Res 1979;45:260-267.
32. Heinzel FR, Bito V, Biesmans L, Wu M, Detre E, von Wegner F et al. Remodeling of T-tubules and reduced synchrony of Ca2+ release in myocytes from chronically ischemic myocardium. Circ Res 2008;102:338-346.
33. Kirk MM, Izu LT, Chen-Izu Y, McCulle SL, Wier WG, Balke CW et al. Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes. J Physiol 2003;547:441-451.
34. Tidball JG, Cederdahl JE, Bers DM. Quantitative analysis of regional variability in the distribution of transverse tubules in rabbit myocardium. Cell Tissue Res 1991;264: 293-298.
35. Lenaerts I, Bito V, Heinzel FR, Driesen RB, Holemans P, D'Hooge J 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. Circ Res 2009;105:876-885.
36. Richards MA, Clarke JD, Saravanan P, Voigt N, Dobrev D, Eisner DA et al. Transverse tubules are a common feature in large mammalian atrial myocytes including human. Am J Physiol Heart Circ Physiol 2011;301:H1996-H2005.
37. Sommer JR, Johnson EA. Purkinje fibers of the heart examined with the peroxidase reaction. J Cell Biol 1968;37:570-574.
38. Martinez-Palomo A, Alanis J, Benitez D. Transitional cardiac cells of the conductive system of the dog heart. Distinguishing morphological and electrophysiological features. J Cell Biol 1970;47:1-17.
39. Legato MJ. Ultrastructure of the atrial, ventricular, and Purkinje cell, with special reference to the genesis of arrhythmias. Circulation 1973;47:178-189.
40. Boyden PA, Albala A, Dresdner KP Jr. Electrophysiology and ultrastructure of canine subendocardial Purkinje cells isolated from control and 24-hour infarcted hearts. Circ Res 1989;65:955-970.
41. Di Maio A, Ter Keurs HE, Franzini-Armstrong C. T-tubule profiles in Purkinje fibres of mammalian myocardium. J Muscle Res Cell Motil 2007;28:115-121.
42. Page E. Tubular systems in Purkinje cells of the cat heart. J Ultrastruct Res 1966;17: 72-83.
43. Brette F, Salle L, Orchard CH. Differential modulation of L-type Ca2+ current by SR Ca2+ release at the T-tubules and surface membrane of rat ventricular myocytes. Circ Res 2004;95:e1-e7.
44. Brette F, Salle L, Orchard CH. Quantification of calcium entry at the T-tubules and surface membrane in rat ventricular myocytes. Biophys J 2006;90:381-389.
45. Houser SR. Ca(2+) signaling domains responsible for cardiac hypertrophy and arrhythmias. Circ Res 2009;104:413-415.
46. Cheng H, Lederer WJ, Cannell MB. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993;262:740-744.
47. Song LS, Sham JS, Stern MD, Lakatta EG, Cheng H. Direct measurement of SR release flux by tracking 'Ca2+ spikes' in rat cardiac myocytes. J Physiol (Lond) 1998; 512:677-691.
48. Sham JS, Song LS, Chen Y, Deng LH, Stern MD, Lakatta EG et al. Termination of Ca2+ release by a local inactivation of ryanodine receptors in cardiac myocytes. Proc Natl Acad Sci USA 1998;95:15096-15101.
49. Page E, McCallister LP. Quantitative electron microscopic description of heart muscle cells: application to normal, hypertrophied and thyroxin-stimulated hearts. Am J Cardiol 1973;31:172-181.
50. Maron BJ, Ferrans VJ, Roberts WC. Ultrastructural features of degenerated cardiac muscle cells in patients with cardiac hypertrophy. Am J Pathol 1975;79:387-434.
51. Schaper J, Froede R, Hein S, Buck A, Hashizume H, Speiser B et al. Impairment of the myocardial ultrastructure and changes of the cytoskeleton in dilated cardiomyopathy. Circulation 1991;83:504-514.
52. Kaprielian RR, Stevenson S, Rothery SM, Cullen MJ, Severs NJ. Distinct patterns of dystrophin organization in myocyte sarcolemma and transverse tubules of normal and diseased human myocardium. Circulation 2000;101:2586-2594.
53. He J, Conklin MW, Foell JD,Wolff MR, Haworth RA, Coronado R et al. Reduction in density of transverse tubules and L-type Ca(2+) channels in canine tachycardia-induced heart failure. Cardiovasc Res 2001;49:298-307.
54. Balijepalli RC, Lokuta AJ, Maertz NA, Buck JM, Haworth RA, Valdivia HH et al. Depletion of T-tubules and specific subcellular changes in sarcolemmal proteins in tachycardia-induced heart failure. Cardiovasc Res 2003;59:67-77.
55. Louch WE, Mork HK, Sexton J, Stromme TA, Laake P, Sjaastad I et al. T-tubule disorganization and reduced synchrony of Ca2+ release in murine cardiomyocytes following myocardial infarction. J Physiol 2006;574:519-533.
56. Swift F, Birkeland JA, Tovsrud N, Enger UH, Aronsen JM, Louch WE et al. Altered Na+/Ca2+-exchanger activity due to downregulation of Na+/K+-ATPase alpha2-isoform in heart failure. Cardiovasc Res 2008;78:71-78.
57. Lyon AR, MacLeod KT, Zhang Y, Garcia E, Kanda GK, Lab MJ et al. Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proc Natl Acad Sci USA 2009;106:6854-6859.
58. Dibb KM, Clarke JD, Horn MA, Richards MA, Graham HK, Eisner DA et al. Characterization of an extensive transverse tubular network in sheep atrial myocytes and its depletion in heart failure. Circ Heart Fail 2009;2:482-489.
59. Ibrahim M, Al Masri A, Navaratnarajah M, Siedlecka U, Soppa GK, Moshkov A et al. Prolonged mechanical unloading affects cardiomyocyte excitation-contraction coupling, transverse-tubule structure, and the cell surface. FASEB J 2010;24:3321-3329.
60. Wei S, Guo A, Chen B, Kutschke W, Xie YP, Zimmerman K et al. T-tubule remodeling during transition from hypertrophy to heart failure. Circ Res 2010;107: 520-531.
61. Kemi OJ, Hoydal MA, Macquaide N, Haram PM, Koch LG, Britton SL et al. The effect of exercise training on transverse tubules in normal, remodeled, and reverse remodeled hearts. J Cell Physiol 2011;226:2235-2243.
62. van Oort RJ, Garbino A, Wang W, Dixit SS, Landstrom AP, Gaur N et al. Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation 2011;123:979-988.
63. Wu CY, Jia Z, Wang W, Ballou LM, Jiang YP, Chen B et al. PI3Ks maintain the structural integrity of T-tubules in cardiac myocytes. PLoS One 2011;6:e24404.
64. Sachse FB, Torres NS, Savio-Galimberti E, Aiba T, Kass DA, Tomaselli GF et al. Subcellular structures and function of myocytes impaired during heart failure are restored by cardiac resynchronization therapy. Circ Res 2012;110:588-597.
65. Ibrahim M, Navaratnarajah M, Siedlecka U, Rao C, Dias P, Moshkov AV et al. Mechanical unloading reverses transverse tubule remodelling and normalizes local Ca(2+)-induced Ca(2+)release in a rodent model of heart failure. Eur J Heart Fail 2012;14:571-580.
66. Lyon AR, Nikolaev VO, Miragoli M, Sikkel MB, Paur H, Benard L et al. Plasticity of surface structures and beta(2)-adrenergic receptor localization in failing ventricular cardiomyocytes during recovery from heart failure. Circ Heart Fail 2012;5:357-365.
67. Stolen TO, Hoydal MA, Kemi OJ, Catalucci D, Ceci M, Aasum E et al. Interval training normalizes cardiomyocyte function, diastolic Ca2+ control, and SR Ca2+ release synchronicity in a mouse model of diabetic cardiomyopathy. Circ Res 2009;105: 527-536.
68. Ohler A, Weisser-Thomas J, Piacentino V, Houser SR, Tomaselli GF, O'Rourke B. Two-photon laser scanning microscopy of the transverse-axial tubule system in ventricular cardiomyocytes from failing and non-failing human hearts. Cardiol Res Pract 2009;2009:802373.
69. Houser SR. Reduced abundance of transverse tubules and L-type calcium channels: another cause of defective contractility in failing ventricular myocytes. Cardiovasc Res 2001;49:253-256.
70. Brette F, Komukai K, Orchard CH. Validation of formamide as a detubulation agent in isolated rat cardiac cells. Am J Physiol Heart Circ Physiol 2002;283:H1720-H1728.
71. Brette F, Despa S, Bers DM, Orchard CH. Spatiotemporal characteristics of SR Ca(2+) uptake and release in detubulated rat ventricular myocytes. J Mol Cell Cardiol 2005;39:804-812.
72. 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;497:589-597.
73. Louch WE, Bito V, Heinzel FR, Macianskiene R, Vanhaecke J, Flameng W et al. 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.
74. Bito V, Heinzel FR, Biesmans L, Antoons G, Sipido KR. Crosstalk between L-type Ca2+ channels and the sarcoplasmic reticulum: alterations during cardiac remodelling. Cardiovasc Res 2008;77:315-324.
75. Gomez AM, Guatimosim S, Dilly KW, Vassort G, Lederer WJ. Heart failure after myocardial infarction: altered excitation-contraction coupling. Circulation 2001;104: 688-693.
76. Houser SR, Piacentino V III,Weisser J. Abnormalities of calcium cycling in the hypertrophied and failing heart. J Mol Cell Cardiol 2000;32:1595-1607.
77. Xu M, Zhou P, Xu SM, Liu Y, Feng X, Bai SH et al. Intermolecular failure of L-type Ca2+ channel and ryanodine receptor signaling in hypertrophy. PLoS Biol 2007;5:e21.
78. Hasenfuss G, Reinecke H, Studer R, Meyer M, Pieske B, Holtz J et al. Relation between myocardial function and expression of sarcoplasmic reticulum Ca(2+)-ATPase in failing and nonfailing human myocardium. Circ Res 1994;75:434-442.
79. Kiss E, Ball NA, Kranias EG, Walsh RA. Differential changes in cardiac phospholamban and sarcoplasmic reticular Ca2+-ATPase protein levels-effects on Ca2+ transport and mechanics in compensated pressure-overload hypertrophy and congestive heart failure. Circ Res 1995;77:759-764.
80. O'Rourke B, Kass DA, Tomaselli GF, Kaab S, Tunin R, Marban E. Mechanisms of altered excitation-contraction coupling in canine tachycardia-induced heart failure, I: experimental studies. Circ Res 1999;84:562-570.
81. del Monte F, Harding SE, Schmidt U, Matsui T, Kang ZB, Dec GW et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 1999;100:2308-2311.
82. Minamisawa S, Hoshijima M, Chu G, Ward CA, Frank K, Gu Y et al. Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 1999;99:313-322.
83. Hobai IA, O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 2001;103:1577-1584.
84. Feldman AM, Weinberg EO, Ray PE, Lorell BH. Selective changes in cardiac gene expression during compensated hypertrophy and the transition to cardiac decompensation in rats with chronic aortic banding. Circ Res 1993;73:184-192.
85. Hasenfuss G. Alterations of calcium-regulatory proteins in heart failure. Cardiovasc Res 1998;37:279-289.
86. Yao A, Su Z, Nonaka A, Zubair I, Spitzer KW, Bridge JH et al. Abnormal myocyte Ca2+ homeostasis in rabbits with pacing-induced heart failure. Am J Physiol 1998; 275:H1441-H1448.
87. Litwin SE, Zhang D, Bridge JH. Dyssynchronous Ca(2+) sparks in myocytes from infarcted hearts. Circ Res 2000;87:1040-1047.
88. Pogwizd SM, Qi M, YuanW, Samarel AM, Bers DM. Upregulation of Na(+)/Ca(2+) exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 1999;85:1009-1019.
89. Hobai IA, O'Rourke B. Enhanced Ca(2+)-activated Na(+)-Ca(2+) exchange activity in canine pacing-induced heart failure. Circ Res 2000;87:690-698.
90. Bers DM, Pogwizd SM, Schlotthauer K. Upregulated Na/Ca exchange is involved in both contractile dysfunction and arrhythmogenesis in heart failure. Basic Res Cardiol 2002;97(Suppl. 1):I36-I42-.
91. Weisser-Thomas J, Piacentino V III, Gaughan JP, Margulies K, Houser SR. Calcium entry via Na/Ca exchange during the action potential directly contributes to contraction of failing human ventricular myocytes. Cardiovasc Res 2003;57:974-985.
92. Piacentino V III, Weber CR, Chen X, Weisser-Thomas J, Margulies KB, Bers DM et al. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res 2003;92:651-658.
93. Dipla K, Mattiello JA, Margulies KB, Jeevanandam V, Houser SR. The sarcoplasmic reticulum and the Na+/Ca2+ exchanger both contribute to the Ca2+ transient of failing human ventricular myocytes. Circ Res 1999;84:435-444.
94. Sipido KR, Volders PG, Vos MA, Verdonck F. Altered Na/Ca exchange activity in cardiac hypertrophy and heart failure: a new target for therapy Cardiovasc Res 2002;53:782-805.
95. O'Neill SC, Valdeolmillos M, Smith GL, Eisner DA. The effects of metabolic inhibition on intracellular pH and Ca. Mol Cell Biochem 1989;89:199-203.
96. Goldhaber JI, Parker JM, Weiss JN. Mechanisms of excitation-contraction coupling failure during metabolic inhibition in guinea-pig ventricular myocytes. J Physiol (Lond) 1991;443:371-386.
97. Overend CL, Eisner DA, O'Neill SC. Altered cardiac sarcoplasmic reticulum function of intact myocytes of rat ventricle during metabolic inhibition. Circ Res 2001; 88:181-187.
98. Fukumoto GH, Lamp ST, Motter C, Bridge JH, Garfinkel A, Goldhaber JI. Metabolic inhibition alters subcellular calcium release patterns in rat ventricular myocytes: implications for defective excitation-contraction coupling during cardiac ischemia and failure. Circ Res 2005;96:551-557.
99. Gomez AM, Valdivia HH, Cheng H, Lederer MR, Santana LF, Cannell MB et al. Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 1997;276:800-806.
100. Yang Z, Pascarel C, Steele DS, Komukai K, Brette F, Orchard CH. Na+-Ca2+ exchange activity is localized in the T-tubules of rat ventricular myocytes. Circ Res 2002;91:315-322.
101. Sipido KR, Acsai K, Antoons G, Bito V, Macquaide N. T-tubule remodelling and ryanodine receptor organization modulate sodium-calcium exchange. Adv Exp Med Biol 2013;961:375-383.
102. Sacconi L, Ferrantini C, Lotti J, Coppini R, Yan P, Loew LM et al. Action potential propagation in transverse-axial tubular system is impaired in heart failure. Proc Natl Acad Sci USA 2012;109:5815-5819.
103. Tao W, Shi J, Dorn GW II, Wei L, Rubart M. Spatial variability in T-tubule and electrical remodeling of left ventricular epicardium in mouse hearts with transgenic Galphaq overexpression-induced pathological hypertrophy. J Mol Cell Cardiol 2012; 53:409-419.
104. Orchard CH, Pasek M, Brette F. The role of mammalian cardiac t-tubules in excitation-contraction coupling: experimental and computational approaches. Exp Physiol 2009;94:509-519.
105. Pasek M, Simurda J, Christe G, Orchard CH. Modelling the cardiac transverse-axial tubular system. Prog Biophys Mol Biol 2008;96:226-243.
106. Sah R, Ramirez RJ, Backx PH. Modulation of Ca(2+) release in cardiac myocytes by changes in repolarization rate: role of phase-1 action potential repolarization in excitation-contraction coupling. Circ Res 2002;90:165-173.
107. Harris DM, Mills GD, Chen X, Kubo H, Berretta RM, Votaw VS et al. Alterations in early action potential repolarization causes localized failure of sarcoplasmic reticulum Ca2+ release. Circ Res 2005;96:543-550.
108. Nikolaev VO, Moshkov A, Lyon AR, Miragoli M, Novak P, Paur H et al. Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 2010;327:1653-1657.
109. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K. Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 2000;6:11-22.
110. Nishi M, Mizushima A, Nakagawara K, Takeshima H. Characterization of human junctophilin subtype genes. Biochem Biophys Res Commun 2000;273:920-927.
111. Komazaki S, Nishi M, Takeshima H. Abnormal junctional membrane structures in cardiac myocytes expressing ectopic junctophilin type 1. FEBS Lett 2003;542:69-73.
112. McNary TG, Bridge JH, Sachse FB. Strain transfer in ventricular cardiomyocytes to their transverse tubular system revealed by scanning confocal microscopy. Biophys J 2011;100:L53-L55.
113. McNary TG, Spitzer KW, Holloway H, Bridge JH, Kohl P, Sachse FB. Mechanical modulation of the transverse tubular system of ventricular cardiomyocytes. Prog Biophys Mol Biol 2012;110:218-225.
114. Xie YP, Chen B, Sanders P, Guo A, Li Y, Zimmerman K et al. Sildenafil prevents and reverses transverse-tubule remodeling and Ca2+ handling dysfunction in right ventricle failure induced by pulmonary artery hypertension. Hypertension 2012;59: 355-362.
115. Chen B, Li Y, Jiang S, Xie YP, Guo A, Kutschke W et al. beta-Adrenergic receptor antagonists ameliorate myocyte T-tubule remodeling following myocardial infarction. FASEB J 2012;26:2531-2537.
116. Minamisawa S, Oshikawa J, Takeshima H, Hoshijima M,Wang Y, Chien KR et al. Junctophilin type 2 is associated with caveolin-3 and is down-regulated in the hypertrophic and dilated cardiomyopathies. Biochem Biophys Res Commun 2004;325: 852-856.
117. Landstrom AP, Kellen CA, Dixit SS, van Oort RJ, Garbino A, Weisleder N et al. Junctophilin-2 expression silencing causes cardiocyte hypertrophy and abnormal intracellular calcium-handling. Circ Heart Fail 2011;4:214-223.
118. Wu HD, Xu M, Li RC, Guo L, Lai YS, Xu SM et al. Ultrastructural remodelling of Ca2+ signalling apparatus in failing heart cells. Cardiovasc Res 2012;95:430-438.
119. Xu M, Wu HD, Li RC, Zhang HB, Wang M, Tao J et al. Mir-24 regulates junctophilin-2 expression in cardiomyocytes. Circ Res 2012;111:837-841.
120. Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M et al. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J Biol Chem 2001; 276:21425-21433.
121. Hong TT, Smyth JW, Gao D, Chu KY, Vogan JM, Fong TS et al. BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol 2010;8:e1000312.
122. Zhang R, Yang J, Zhu J, Xu X. Depletion of zebrafish Tcap leads to muscular dystrophy via disrupting sarcomere-membrane interaction, not sarcomere assembly. Hum Mol Genet 2009;18:4130-4140.
123. Lee E, Marcucci M, Daniell L, Pypaert M,Weisz OA, Ochoa GC et al. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 2002;297:1193-1196.
124. Fugier C, Klein AF, Hammer C, Vassilopoulos S, Ivarsson Y, Toussaint A et al. Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat Med 2011;17:720-725.
125. Ibrahim M, Siedlecka U, Buyandelger B, Harada M, Rao C, Moshkov A et al. A critical role for Telethonin in regulating t-tubule structure and function in the mammalian heart. Hum Mol Genet 2013;22:372-383.