Role of ryanodine receptor subtypes in initiation and formation of calcium sparks in arterial smooth muscle: Comparison with striated muscle

Journal of Biomedicine and Biotechnology

Volumn 2009, Issue , 2009, Pages

  Essin, Kirill ^a,b   Gollasch, Maik ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Experimental and Clinical Research Center   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL L TYPE; RECEPTOR SUBTYPE; RYANODINE RECEPTOR; RYANODINE RECEPTOR 2;

ARTERY MUSCLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CROSS COUPLING REACTION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; REVIEW; SKELETAL MUSCLE; SMOOTH MUSCLE FIBER; ANIMAL; ARTERY; METABOLISM; VASCULAR SMOOTH MUSCLE;

ANIMALS; ARTERIES; CALCIUM; HUMANS; MUSCLE, SMOOTH, VASCULAR; MUSCLE, STRIATED; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 73449096721     PISSN: 11107243     EISSN: 11107251     Source Type: Journal    
DOI: 10.1155/2009/135249     Document Type: Review

References (130)

1. Cheng H., Lederer W. J., Calcium sparks Physiological Reviews 2008 88 4 1491 1545
2. Benham C. D., Bolton T. B., Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit Journal of Physiology 1986 381 385 406
3. Nelson M. T., Cheng H., Rubart M., Relaxation of arterial smooth muscle by calcium sparks Science 1995 270 5236 633 637
4. Perez G. J., Bonev A. D., Patlak J. B., Nelson M. T., Functional coupling of ryanodine receptors to K(Ca) channels in smooth muscle cells from rat cerebral arteries Journal of General Physiology 1999 113 2 229 237
5. Ledoux J., Werner M. E., Brayden J. E., Nelson M. T., Calcium-activated potassium channels and the regulation of vascular tone Physiology 2006 21 1 69 79
6. Tanaka Y., Meera P., Song M., Knaus H.-G., Toro L., Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant + subunit complexes Journal of Physiology 1997 502 3 545 557
7. Cox D. H., Cui J., Aldrich R. W., Separation of gating properties from permeation and block in mslo large conductance Ca-activated K+ channels Journal of General Physiology 1997 109 5 633 646
8. Brenner R., Perz G.J., Bonev A. D., Vasoregulation by the 1 subunit of the calcium-activated potassium channel Nature 2000 407 6806 870 876
9. Pluger S., Faulhaber J., Furstenau M., Mice with disrupted BK channel 1 subunit gene feature abnormal Ca2+ spark/STOC coupling and elevated blood pressure Circulation research 2000 87 11 E53 60
10. Sausbier M., Arntz C., Bucurenciu I., Elevated blood pressure linked to primary hyperaldosteronism and impaired vasodilation in BK channel-deficient mice Circulation 2005 112 1 60 68
11. Wang Q., Hogg R. C., Large W. A., Properties of spontaneous inward currents recorded in smooth muscle cells isolated from the rabbit portal vein Journal of Physiology 1992 451 525 537
12. Gordienko D. V., Zholos A. V., Bolton T. B., Membrane ion channels as physiological targets for local Ca2+ signalling Journal of Microscopy 1999 196 3 305 316
13. Bao R., Lifshitz L. M., Tuft R. A., Bellve K., Fogarty K. E., ZhuGe R., A close association of RyRs with highly dense clusters of Ca2+-activated Cl-channels underlies the activation of STICs by Ca2+ sparks in mouse airway smooth muscle Journal of General Physiology 2008 132 1 145 160
14. Amberg G. C., Bonev A. D., Rossow C. F., Nelson M. T., Santana L. F., Modulation of the molecular composition of large conductance, Ca2+ activated K+ channels in vascular smooth muscle during hypertension The Journal of Clinical Investigation 2003 112 5 717 724
15. Rios E., Brum G., Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle Nature 1987 325 6106 717 720
16. Klein M. G., Schneider M. F., Ca 2 + sparks in skeletal muscle Progress in Biophysics and Molecular Biology 2006 92 3 308 332
17. Armstrong C. M., Bezanilla F. M., Horowicz P., Twitches in the presence of ethylene glycol bis(-aminoethyl ether)-N,N′-tetraacetic acid Biochimica et Biophysica Acta 1972 267 3 605 608
18. Fabiato A., Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum American Journal of Physiology 1983 245 1 C1 C14
19. Collier M. L., Ji G., Wang Y.-X., Kotlikoff M. I., Calcium-induced calcium release in smooth muscle: loose coupling between the action potential and calcium release Journal of General Physiology 2000 115 5 653 662
20. Kotlikoff M. I., Calcium-induced calcium release in smooth muscle: the case for loose coupling Progress in Biophysics and Molecular Biology 2003 83 3 171 191
21. Essin K., Welling A., Hofmann F., Luft F. C., Gollasch M., Moosmang S., Indirect coupling between Cav 1.2 channels and ryanodine receptors to generate Ca2+ sparks in murine arterial smooth muscle cells The Journal of Physiology 2007 584 1 205 219
22. Lopez-Lopez J. R., Shacklock P. S., Balke C. W., Wier W. G., Local calcium transients triggered by single L-type calcium channel currents in cardiac cells Science 1995 268 5213 1042 1045
23. Santana L. F., Cheng H., Gomez A. M., Cannell M. B., Lederer W. J., Relation between the sarcolemmal Ca2+ Current and Ca2+ sparks and local control theories for cardiac excitation-contraction coupling Circulation Research 1996 78 1 166 171
24. Moosmang S., Schulla V., Welling A., Dominant role of smooth muscle L-type calcium channel Cav1.2 for blood pressure regulation The EMBO Journal 2003 22 22 6027 6034
25. Gyorke S., Gyorke I., Lukyanenko V., Terentyev D., Viatchenko-Karpinski S., Wiesner T. F., Regulation of sarcoplasmic reticulum calcium release by luminal calcium in cardiac muscle Frontiers in Bioscience 2002 7 d1454 d1463
26. Laver D. R., Ca 2 + stores regulate ryanodine receptor Ca2+ release channels via luminal and cytosolic Ca2+ sites Clinical and Experimental Pharmacology and Physiology 2007 34 9 889 896
27. Fill M., Copello J. A., Ryanodine receptor calcium release channels Physiological Reviews 2002 82 4 893 922
28. Ledbetter M. W., Preiner J. K., Louis C. F., Mickelson J. R., Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction The Journal of Biological Chemistry 1994 269 50 31544 31551
29. Sorrentino V., The ryanodine receptor family of intracellular calcium release channels Advances in Pharmacology 1995 33 67 90
30. Santonastasi M., Wehrens X. H. T., Ryanodine receptors as pharmacological targets for heart disease Acta Pharmacologica Sinica 2007 28 7 937 944
31. Pabelick C. M., Prakash Y. S., Kannan M. S., Sieck G. C., Spatial and temporal aspects of calcium sparks in porcine tracheal smooth muscle cells American Journal of Physiology 1999 277 5 L1018 L1025
32. Nakai J., Ogura T., Protasi F., Franzini-Armstrong C., Allen P. D., Beam K. G., Functional nonequality of the cardiac and skeletal ryanodine receptors Proceedings of the National Academy of Sciences of the United States of America 1997 94 3 1019 1022
33. Perez C. F., Voss A., Pessah I. N., Allen P. D., RyR1/RyR3 chimeras reveal that multiple domains of RyR1 are involved in skeletal-type E-C coupling Biophysical Journal 2003 84 4 2655 2663
34. Trafford A. W., Sibbring G. C., Diaz M. E., Eisner D. A., The effects of low concentrations of caffeine on spontaneous Ca release in isolated rat ventricular myocytes Cell Calcium 2000 28 4 269 276
35. Zucchi R., Ronca-Testoni S., The sarcoplasmic reticulum Ca2+ channel/ryanodine receptor: modulation by endogenous effectors, drugs and disease states Pharmacological Reviews 1997 49 1 1 50
36. Zhao F., Li P., Chen S. R. W., Louis C. F., Fruen B. R., Dantrolene inhibition of ryanodine receptor Ca2+ release channels. Molecular mechanism and isoform selectivity The Journal of Biological Chemistry 2001 276 17 13810 13816
37. Zhang Y., Rodney G. G., Schneider M. F., Effects of azumolene on Ca2+ sparks in skeletal muscle fibers Journal of Pharmacology and Experimental Therapeutics 2005 314 1 94 102
38. Bannister R. A., Pessah I. N., Beam K. G., The skeletal L-type Ca2+ current is a major contributor to excitation-coupled Ca2+ entry Journal of General Physiology 2009 133 1 79 91
39. Valdivia H. H., Kirby M. S., Lederer W. J., Coronado R., Scorpion toxins targeted against the sarcoplasmic reticulum Ca2+-release channel of skeletal and cardiac muscle Proceedings of the National Academy of Sciences of the United States of America 1992 89 24 12185 12189
40. Tripathy A., Resch W., Xu L. E., Valdivia H. H., Meissner G., Imperatoxin A induces subconductance states in Ca2+ release channels (ryanodine receptors) of cardiac and skeletal muscle Journal of General Physiology 1998 111 5 679 690
41. Shtifman A., Ward C. W., Wang J., Valdivia H. H., Schneider M. F., Effects of imperatoxin A on local sarcoplasmic reticulum Ca2+ release in frog skeletal muscle Biophysical Journal 2000 79 2 814 827
42. Terentyev D., Viatchenko-Karpinski S., Valdivia H. H., Escobar A. L., Gyrke S., Luminal Ca2+ controls termination and refractory behavior of Ca2+-induced Ca2+ release in cardiac myocytes Circulation Research 2002 91 5 414 420
43. Takeshima H., Iino M., Takekura H., Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene Nature 1994 369 6481 556 559
44. Takeshima H., Komazaki S., Hirose K., Nishi M., Noda T., Iino M., Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2 The EMBO Journal 1998 17 12 3309 3316
45. Takeshima H., Ikemoto T., Nishi M., Generation and characterization of mutant mice lacking ryanodine receptor type 3 The Journal of Biological Chemistry 1996 271 33 19649 19652
46. Tarroni P., Rossi D., Conti A., Sorrentino V., Expression of the ryanodine receptor type 3 calcium release channel during development and differentiation of mammalian skeletal muscle cells The Journal of Biological Chemistry 1997 272 32 19808 19813
47. Conti A., Reggiani C., Sorrentino V., Selective expression of the type 3 isoform of ryanodine receptor Ca2+ release channel (RyR3) in a subset of slow fibers in diaphragm and cephalic muscles of adult rabbits Biochemical and Biophysical Research Communications 2005 337 1 195 200
48. Conklin M. W., Ahern C. A., Vallejo P., Sorrentino V., Takeshima H., Coronado R., Comparison of Ca2+ sparks produced independently by two ryanodine receptor isoforms (type 1 or type 3) Biophysical Journal 2000 78 4 1777 1785
49. Conti A., Gorza L., Sorrentino V., Differential distribution of ryanodine receptor type 3 (RyR3) gene product in mammalian skeletal muscles Biochemical Journal 1996 316 1 19 23
50. Bertocchini F., Ovitt C. E., Conti A., Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles The EMBO Journal 1997 16 23 6956 6963
51. Shirokova N., Garca J., Ros E., Local calcium release in mammalian skeletal muscle Journal of Physiology 1998 512 2 377 384
52. Ward C. W., Lederer W. J., Ghost sparks Nature Cell Biology 2005 7 5 457 459
53. Wang X., Weisleder N., Collet C., Uncontrolled calcium sparks act as a dystrophic signal for mammalian skeletal muscle Nature Cell Biology 2005 7 5 525 530
54. Weisleder N., Ferrante C., Hirata Y., Systemic ablation of RyR3 alters Ca2+ spark signaling in adult skeletal muscle Cell Calcium 2007 42 6 548 555
55. Ward C. W., Schneider M. F., Castillo D., Expression of ryanodine receptor RyR3 produces Ca2+ sparks in dyspedic myotubes Journal of Physiology 2000 525 1 91 103
56. Sutko J. L., Airey J. A., Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function? Physiological Reviews 1996 76 4 1027 1071
57. Tsugorka A., Rios E., Blatter L. A., Imaging elementary events of calcium release in skeletal muscle cells Science 1995 269 5231 1723 1726
58. Klein M. G., Cheng H., Santana L. F., Jiang Y.-H., Lederer W. J., Schneider M. F., Two mechanisms of quantized calcium release in skeletal muscle Nature 1996 379 6564 455 458
59. Pouvreau S., Royer L., Yi J., Ca 2 + sparks operated by membrane depolarization require isoform 3 ryanodine receptor channels in skeletal muscle Proceedings of the National Academy of Sciences of the United States of America 2007 104 12 5235 5240
60. Legrand C., Giacomello E., Berthier C., Allard B., Sorrentino V., Jacquemond V., Spontaneous and voltage-activated Ca2+ release in adult mouse skeletal muscle fibres expressing the type 3 ryanodine receptor The Journal of Physiology 2008 586 2 441 457
61. Yang H.-T., Tweedie D., Wang S., The ryanodine receptor modulates the spontaneous beating rate of cardiomyocytes during development Proceedings of the National Academy of Sciences of the United States of America 2002 99 14 9225 9230
62. Gyorke S., Terentyev D., Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease Cardiovascular Research 2008 77 2 245 255
63. Rios E., Gyorke S., Calsequestrin, triadin and more: the molecules that modulate calcium release in cardiac and skeletal muscle Journal of Physiology 2009 587 13 3069 3070
64. Coussin F., Macrez N., Morel J.-L., Mironneau J., Requirement of ryanodine receptor subtypes 1 and 2 for Ca2+-induced Ca2+ release in vascular myocytes The Journal of Biological Chemistry 2000 275 13 9596 9603
65. Lohn M., Jessner W., Furstenau M., Regulation of calcium sparks and spontaneous transient outward currents by RyR3 in arterial vascular smooth muscle cells Circulation Research 2001 89 11 1051 1057
66. Mironneau J., Coussin F., Jeyakumar L. H., Fleischer S., Mironneau C., Macrez N., Contribution of ryanodine receptor subtype 3 to Ca2+ responses in Ca2+-overloaded cultured rat portal vein myocytes The Journal of Biological Chemistry 2001 276 14 11257 11264
67. Ji G., Feldman M. E., Greene K. S., Sorrentino V., Xin H.-B., Kotlikoff M. I., RYR2 proteins contribute to the formation of Ca2+ sparks in smooth muscle Journal of General Physiology 2004 123 4 377 386
68. Fritz N., Morel J.-L., Jeyakumar L. H., RyR1-specific requirement for depolarization-induced Ca2+ sparks in urinary bladder smooth muscle Journal of Cell Science 2007 120 21 3784 3791
69. Hotta S., Morimura K., Ohya S., Muraki K., Takeshima H., Imaizumi Y., Ryanodine receptor type 2 deficiency changes excitation-contraction coupling and membrane potential in urinary bladder smooth muscle Journal of Physiology 2007 582 2 489 506
70. Li X.-Q., Zheng Y.-M., Rathore R., Ma J., Takeshima H., Wang Y.-X., Genetic evidence for functional role of ryanodine receptor 1 in pulmonary artery smooth muscle cells Pflugers Archiv European Journal of Physiology 2009 457 4 771 783
71. Wang Y.-X., Zheng Y.-M., Mei Q.-B., FKBP12.6 and cADPR regulation of Ca2+ release in smooth muscle cells American Journal of Physiology 2004 286 C538 C546
72. Morimura K., Ohi Y., Yamamura H., Ohya S., Muraki K., Imaizumi Y., Two-step Ca2+ intracellular release underlies excitation-contraction coupling in mouse urinary bladder myocytes American Journal of Physiology 2006 290 2 C388 C403
73. Sonnleitner A., Conti A., Bertocchini F., Schindler H., Sorrentino V., Functional properties of the ryanodine receptor type 3 (RyR3) Ca2+ release channel The EMBO Journal 1998 17 10 2790 2798
74. Murayama T., Oba T., Katayama E., Further characterization of the type 3 ryanodine receptor (RyR3) purified from rabbit diaphragm The Journal of Biological Chemistry 1999 274 24 17297 17308
75. Gollasch M., Wellman G. C., Knot H. J., Ontogeny of local sarcoplasmic reticulum Ca2+ signals in cerebral arteries: Ca2+ sparks as elementary physiological events Circulation Research 1998 83 11 1104 1114
76. Reading S. A., Brayden J. E., Central role of TRPM4 channels in cerebral blood flow regulation Stroke 2007 38 8 2322 2328
77. Blher M., Engeli S., Klting N., Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity Diabetes 2006 55 11 3053 3060
78. Kong H., Wang R., Chen W., Skeletal and cardiac ryanodine receptors exhibit different responses to Ca2+ overload and luminal Ca2+ Biophysical Journal 2007 92 8 2757 2770
79. Laver D. R., Luminal Ca2+ activation of cardiac ryanodine receptors by luminal and cytoplasmic domains European Biophysics Journal 2009 39 1 19 26
80. Xu L., Meissner G., Regulation of cardiac muscle Ca2+ release channel by sarcoplasmic reticulum lumenal Ca2+ Biophysical Journal 1998 75 5 2302 2312
81. Gyorke I., Gyorke S., Regulation of the cardiac ryanodine receptor channel by luminal Ca2+ involves luminal Ca2+ sensing sites Biophysical Journal 1998 75 6 2801 2810
82. Gyorke S., Lukyanenko V., Gyorke I., Dual effects of tetracaine on spontaneous calcium release in rat ventricular myocytes Journal of Physiology 1997 500 2 297 309
83. Cheranov S. Y., Jaggar J. H., Sarcoplasmic reticulum calcium load regulates rat arterial smooth muscle calcium sparks and transient Kca currents Journal of Physiology 2002 544 1 71 84
84. Curtis T. M., Tumelty J., Stewart M. T., Modification of smooth muscle Ca2+-sparks by tetracaine: evidence for sequential RyR activation Cell Calcium 2008 43 2 142 154
85. ZhuGe R., Tuft R. A., Fogarty K. E., Bellve K., Fay F. S., Walsh J. V. Jr., The influence of sarcoplasmic reticulum Ca2+ concentration on Ca2+ sparks and spontaneous transient outward currents in single smooth muscle cells Journal of General Physiology 1999 113 2 215 228
86. Wellman G. C., Santana L. F., Bonev A. D., Nelson M. T., Role of phospholamban in the modulation of arterial Ca2+ sparks and Ca2+-activated K+ channels by cAMP American Journal of Physiology 2001 70281 C1029 C1037
87. Farrell E. F., Antaramian A., Rueda A., Gomez A. M., Valdivia H. H., Sorcin inhibits calcium release and modulates excitation-contraction coupling in the heart The Journal of Biological Chemistry 2003 278 36 34660 34666
88. Rueda A., Song M., Toro L., Stefani E., Valdivia H. H., Sorcin modulation of Ca2+ sparks in rat vascular smooth muscle cells Journal of Physiology 2006 576 3 887 901
89. Fowler M. R., Colotti G., Chiancone E., Higuchi Y., Seidler T., Smith G. L., Complex modulation of L-type Ca2+ current inactivation by sorcin in isolated rabbit cardiomyocytes Pflugers Archiv European Journal of Physiology 2009 457 5 1049 1060
90. Matsumoto T., Hisamatsu Y., Ohkusa T., Sorcin interacts with sarcoplasmic reticulum Ca2+-ATPase and modulates excitation-contraction coupling in the heart Basic Research in Cardiology 2005 100 3 250 262
91. Collis L. P., Meyers M. B., Zhang J., Expression of a sorcin missense mutation in the heart modulates excitation-contraction coupling FASEB Journal 2007 21 2 475 487
92. Valdivia H. H., Modulation of intracellular Ca2+ levels in the heart by sorcin and FKBP12, two accessory proteins of ryanodine receptors Trends in Pharmacological Sciences 1998 19 12 479 483
93. Mohiddin S., Antaramian A., Farrell E. F., A naturally-occurring sorcin missense mutation (F112L) is associated with hypertrophic cardiomyopathy, hypertension, and impaired modulation of cardiac ryanodine receptor Circulation 2002 106 319
94. Franceschini S., Ilari A., Verzili D., Molecular basis for the impaired function of the natural F112L sorcin mutant: X-ray crystal structure, calcium affinity, and interaction with annexin VII and the ryanodine receptor FASEB Journal 2008 22 1 295 306
95. Worley P. F., Zeng W., Huang G., Homer proteins in Ca2+ signaling by excitable and non-excitable cells Cell Calcium 2007 42 4-5 363 371
96. Soloviev M. M., Ciruela F., Chan W.-Y., McIlhinney R. A. J., Mouse brain and muscle tissues constitutively express high levels of homer proteins European Journal of Biochemistry 2000 267 3 634 639
97. Feng W., Tu J., Pouliquin P., Dynamic regulation of ryanodine receptor type 1 (RyR1) channel activity by Homer 1 Cell Calcium 2008 43 3 307 314
98. Pouliquin P., Pace S. M., Dulhunty A. F., In vitro modulation of the cardiac ryanodine receptor activity by Homer1 Pflugers Archiv European Journal of Physiology 2009 458 4 723 732
99. Ward C. W., Feng W., Tu J., Pessah I. N., Worley P. K., Schneider M. F., Homer protein increases activation of Ca2+ sparks in permeabilized skeletal muscle The Journal of Biological Chemistry 2004 279 7 5781 5787
100. Huang G., Kim J. Y., Dehoff M., Ca 2 + signaling in microdomains: homer1 mediates the interaction between RyR2 and Cav 1.2 to regulate excitation-contraction coupling The Journal of Biological Chemistry 2007 282 19 14283 14290
101. Zalk R., Lehnart S. E., Marks A. R., Modulation of the ryanodine receptor and intracellular calcium Annual Review of Biochemistry 2007 76 367 385
102. Liu J., Farmer J. D. Jr., Lane W. S., Friedman J., Weissman I., Schreiber S. L., Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes Cell 1991 66 4 807 815
103. Heitman J., Movva N. R., Hall M. N., Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast Science 1991 253 5022 905 909
104. Lam E., Martin M. M., Timerman A. P., A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor The Journal of Biological Chemistry 1995 270 44 26511 26522
105. Tang W., Ingalls C. P., Durham W. J., Altered excitation-contraction coupling with skeletal muscle specific FKBP12 deficiency FASEB Journal 2004 18 13 1597 1599
106. Reiken S., Lacampagne A., Zhou H., PKA phosphorylation activates the calcium release channel (ryanodine receptor)-in skeletal muscle: defective regulation in heart failure Journal of Cell Biology 2003 160 6 919 928
107. Almassy J., Sztretye M., Lukacs B., Effects of K-201 on the calcium pump and calcium release channel of rat skeletal muscle Pflugers Archiv European Journal of Physiology 2008 457 1 171 183
108. Xin H.-B., Senbonmatsu T., Cheng D.-S., Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy Nature 2002 416 6878 334 337
109. Xiao R.-P., Valdivia H. H., Bogdanov K., Valdivia C., Lakatta E. G., Cheng H., The immunophilin FK506-binding protein modulates Ca2+ release channel closure in rat heart Journal of Physiology 1997 500 2 343 354
110. Su Z., Sugishita K., Li F., Ritter M., Barry W. H., Effects of FK506 on [Ca2+] i differ in mouse and rabbit ventricular myocytes Journal of Pharmacology and Experimental Therapeutics 2003 304 1 334 341
111. McCall E., Li L., Satoh H., Shannon T. R., Blatter L. A., Bers D. M., Effects of FK-506 on contraction and Ca2+ transients in rat cardiac myocytes Circulation Research 1996 79 6 1110 1121
112. Gomez A. M., Schuster I., Fauconnier J., Prestle J., Hasenfuss G., Richard S., FKBP12.6 overexpression decreases Ca2+ spark amplitude but enhances [Ca2+] i transient in rat cardiac myocytes American Journal of Physiology 2004 287 5 H1987 H1993
113. Loughrey C. M., Seidler T., Miller S. L. W., Over-expression of FK506-binding protein FKB12.6 alters excitation-contraction coupling in adult rabbit cardiomyocytes Journal of Physiology 2004 556 3 919 934
114. Gellen B., Fernandez-Velasco M., Briec F., Conditional FKBP12.6 overexpression in mouse cardiac myocytes prevents triggered ventricular tachycardia through specific alterations in excitation-contraction coupling Circulation 2008 117 14 1778 1786
115. Xiao J., Tian X., Jones P. P., Removal of FKBP12.6 does not alter the conductance and activation of the cardiac ryanodine receptor or the susceptibility to stress-induced ventricular arrhythmias The Journal of Biological Chemistry 2007 282 48 34828 34838
116. Weidelt Th., Isenberg G., Augmentation of SR Ca2+ release by rapamycin and FK506 causes K+-channel activation and membrane hyperpolarization in bladder smooth muscle British Journal of Pharmacology 2000 129 7 1293 1300
117. Tang W.-X., Chen Y.-F., Zou A.-P., Campbell W. B., Li P.-L., Role of FKBP12.6 in cADPR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle American Journal of Physiology 2002 282 4 H1304 H1310
118. Long C., Cook L. G., Wu G.-Y., Mitchell B. M., Removal of Fkbp12/12.6 from endothelial ryanodine receptors leads to an intracellular calcium leak and endothelial dysfunction Arteriosclerosis, Thrombosis, and Vascular Biology 2007 27 7 1580 1586
119. Weisleder N., Brotto M., Komazaki S., Muscle aging is associated with compromised Ca2+ spark signaling and segregated intracellular Ca2+ release Journal of Cell Biology 2006 174 5 639 645
120. Shorofsky S. R., Aggarwal R., Corretti M., Cellular mechanisms of altered contractility in the hypertrophied heart: big hearts, big sparks Circulation Research 1999 84 4 424 434
121. Harzheim D., Movassagh M., Foo R. S.-Y., Increased InsP3Rs in the junctional sarcoplasmic reticulum augment Ca2+ transients and arrhythmias associated with cardiac hypertrophy Proceedings of the National Academy of Sciences of the United States of America 2009 106 27 11406 11411
122. Pereira L., Matthes J., Schuster I., Mechanisms of [Ca2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice Diabetes 2006 55 3 608 615
123. Yaras N., Ugur M., Ozdemir S., Effects of diabetes on ryanodine receptor Ca release channel (RyR2) and Ca2+ homeostasis in rat heart Diabetes 2005 54 11 3082 3088
124. Wehrens X. H. T., Lehnart S. E., Huang F., FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death Cell 2003 113 7 829 840
125. Lehnart S. E., Wehrens X. H., Laitinen P. J., Sudden death in familial polymorphic ventricular tachycardia associated with calcium release channel (ryanodine receptor) leak Circulation 2004 109 25 3208 3214
126. Lehnart S. E., Mongillo M., Bellinger A., Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice The Journal of Clinical Investigation 2008 118 6 2230 2245
127. Gyorke S., Molecular basis of catecholaminergic polymorphic ventricular tachycardia Heart Rhythm 2009 6 1 123 129
128. McGahon M. K., Dash D. P., Arora A., Diabetes downregulates large-conductance Ca2+-activated potassium 1 channel subunit in retinal arteriolar smooth muscle Circulation Research 2007 100 5 703 711
129. Zhao G., Zhao Y., Pan B., Hypersensitivity of BKCa to Ca2+ sparks underlies hyporeactivity of arterial smooth muscle in shock Circulation Research 2007 101 5 493 502
130. Werner M. E., Zvara P., Meredith A. L., Aldrich R. W., Nelson M. T., Erectile dysfunction in mice lacking the large-conductance calcium-activated potassium (BK) channel Journal of Physiology 2005 567 2 545 556