Fkbp12 activates the cardiac ryanodine receptor ca 2+-release channel and is antagonised by fkbp12.6

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Galfré, Elena ^a   Pitt, Samantha J ^a   Venturi, Elisa ^a   Sitsapesan, Mano ^a   Zaccai, Nathan R ^a   Tsaneva Atanasova, Krasimira ^a   O'Neill, Stephen ^b   Sitsapesan, Rebecca ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FK 506 BINDING PROTEIN; PROTEIN FKBP12; PROTEIN FKBP12.6; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; CALCIUM; PHOSPHOLIPID; TACROLIMUS BINDING PROTEIN 1B;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; HEART MUSCLE CELL; MATHEMATICAL MODEL; NONHUMAN; PHOSPHOLIPID BILAYER; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SARCOPLASMIC RETICULUM; SHEEP; ANIMAL; BIOLOGICAL MODEL; CALCIUM SIGNALING; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; LIPID BILAYER; MALE; METABOLISM; TIME; WISTAR RAT;

OVIS ARIES; RATTUS;

ANIMALS; CALCIUM; CALCIUM SIGNALING; ION CHANNEL GATING; LIPID BILAYERS; MALE; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; PHOSPHOLIPIDS; RATS; RATS, WISTAR; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SHEEP; TACROLIMUS BINDING PROTEIN 1A; TACROLIMUS BINDING PROTEINS; TIME FACTORS;

EID: 84857510566     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031956     Document Type: Article

References (59)

1. Valdeolmillos M, O'Neill SC, Smith GL, Eisner DA, (1989) Calcium-induced calcium-release activates contraction in intact cardiac cells. Pflug Arch Eur J Phy 413: 676-678.
2. Timerman AP, Onoue H, Xin HB, Barg S, Copello J, et al. (1996) Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J Biol Chem 271: 20385-20391.
3. Lam E, Martin MM, Timerman AP, Sabers C, Fleischer S, et al. (1995) A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J Biol Chem 270: 26511-26522.
4. Xin HB, Rogers K, Qi Y, Kanematsu T, Fleischer S, (1999) Three amino acid residues determine selective binding of FK506-binding protein 12.6 to the cardiac ryanodine receptor. J Biol Chem 274: 15315-15319.
5. Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, et al. (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): Defective regulation in failing hearts. Cell 101: 365-376.
6. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, et al. (2003) FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113: 829-840.
7. Wehrens XH, Lehnart SE, Reiken S, van der NR, Morales R, et al. (2005) Enhancing calstabin binding to ryanodine receptors improves cardiac and skeletal muscle function in heart failure. Proc Natl Acad Sci U S A 102: 9607-9612.
8. Marx SO, Gaburjakova J, Gaburjakova M, Henrikson C, Ondrias K, et al. (2001) Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ Res 88: 1151-1158.
9. Kaftan E, Marks AR, Ehrlich BE, (1996) Effects of rapamycin on ryanodine receptor/Ca2+-release channels from cardiac muscle. Circ Res 78: 990-997.
10. Barg S, Copello JA, Fleischer S, (1997) Different interactions of cardiac and skeletal muscle ryanodine receptors with FK-506 binding protein isoforms. Am J Physiol 272: C1726-C1733.
11. Xiao JM, Tian XX, Jones PP, Bolstad J, Kong HH, et al. (2007) Removal of FKBP12.6 does not alter the conductance and activation of the cardiac ryanodine receptor or the susceptibility to stress-induced ventricular arrhythmias. J Biol Chem 282: 34828-34838.
12. Stewart R, Song L, Carter SM, Sigalas C, Zaccai NR, et al. (2008) Single-channel characterization of the rabbit recombinant RyR2 reveals a novel inactivation property of physiological concentrations of ATP. J Membr Biol 222: 65-77.
13. Xiao RP, Valdivia HH, Bogdanov K, Valdivia C, Lakatta EG, et al. (1997) The immunophilin FK506-binding protein modulates calcium release channel closure in rat heart. J Physiol 500: 343-354.
14. Loughrey CM, Seidler T, Miller SL, Prestle J, MacEachern KE, et al. (2004) Over-expression of FK506-binding protein FKBP12.6 alters excitation-contraction coupling in adult rabbit cardiomyocytes. J Physiol 556: 919-934.
15. Guo T, Cornea RL, Huke S, Camors E, Yang Y, et al. (2010) Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca2+ sparks. Circ Res 106: 1743-1752.
16. Prestle J, Janssen PM, Janssen AP, Zeitz O, Lehnart SE, et al. (2001) Overexpression of FK506-binding protein FKBP12.6 in cardiomyocytes reduces ryanodine receptor-mediated Ca2+ leak from the sarcoplasmic reticulum and increases contractility. Circ Res 88: 188-194.
17. Xin HB, Senbonmatsu T, Cheng DS, Wang YX, Copello JA, et al. (2002) Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature 416: 334-338.
18. Shou W, Aghdasi B, Armstrong DL, Guo Q, Bao S, et al. (1998) Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391: 489-492.
19. Timerman AP, Wiederrecht G, Marcy A, Fleischer S, (1995) Characterization of an exchange reaction between soluble FKBP-12 and the FKBP-ryanodine receptor complex. Modulation by FKBP mutants deficient in peptidyl-prolyl isomerase activity. J Biol Chem 270: 2451-2459.
20. Chelu MG, Danila CI, Gilman CP, Hamilton SL, (2004) Regulation of ryanodine receptors by FK506 binding proteins. Trends Cardiovasc Med 14: 227-234.
21. Deivanayagam CCS, Carson M, Thotakura A, Narayana SVL, Chodavarapu RS, (2000) Structure of FKBP12.6 in complex with rapamycin. Acta Crystallogr D56: 266-271.
22. Fulton KF, Jackson SE, Buckle AM, (2003) Energetic and structural analysis of the role of tryptophan 59 in FKBP12. Biochemistry (Mosc) 42: 2364-2372.
23. Sitsapesan R, Montgomery RAP, MacLeod KT, Williams AJ, (1991) Sheep cardiac sarcoplasmic reticulum calcium release channels: modification of conductance and gating by temperature. J Physiol 434: 469-488.
24. Colquhoun D, Sigworth FJ, (1983) Fitting and statistical analysis of single-channel recording. In: Sakmann B, Neher E, editors. Single-channel recording New York & London Plenum pp. 191-263.
25. Sigworth FJ, Sine SM, (1987) Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys J 52: 1047-1054.
26. Eisner DA, Nichols CG, O'Neill SC, Smith GL, Valdeolmillos M, (1989) The effects of metabolic inhibition on intracellular calcium and pH in isolated rat ventricular cells. J Physiol 411: 393-418.
27. Smith GL, O'Neill SC, (2001) A comparison of the effects of ATP and tetracaine on spontaneous Ca2+ release from rat permeabilised cardiac myocytes. J Physiol 534: 37-47.
28. Noble JE, Bailey MJA, (2009) Chapter 8 Quantitation of Protein. In: Richard RB, Murray PD, editors. Methods Enzymol: Academic Press pp. 73-95.
29. Ahern GP, Junankar PR, Dulhunty AF, (1997) Ryanodine receptors from rabbit skeletal muscle are reversibly activated by rapamycin. Neurosci Lett 225: 81-84.
30. Ahern GP, Junankar PR, Dulhunty AF, (1997) Subconductance States in Single-channel Activity of Skeletal Muscle Ryanodine Receptors After Removal of FKBP12. Biophys J 72: 146-162.
31. Laver DR, Lamb GD, (1998) Inactivation of Ca2+ release channels (ryanodine receptors RyR1 and RyR2) with rapid steps in Ca2+ and voltage. Biophys J 74: 2352-2364.
32. Zahradnikova A, Dura M, Gyorke S, (1999) Modal gating transitions in cardiac ryanodine receptors during increases of Ca2+ concentration produced by photolysis of caged Ca2+. Pflug Arch Eur J Phy 438: 283-288.
33. Sitsapesan R, Williams AJ, (1994) Regulation of the gating of the sheep cardiac sarcoplasmic reticulum Ca2+-release channel by luminal Ca2+. J Membr Biol 137: 215-226.
34. Copello JA, Barg S, Onoue H, Fleischer S, (1997) Heterogeneity of Ca2+ gating of skeletal muscle and cardiac ryanodine receptors. Biophys J 73: 141-156.
35. Saftenku E, Williams AJ, Sitsapesan R, (2001) Markovian Models of Low and High Activity Levels of Cardiac Ryanodine Receptors. Biophys J 80: 2727-2741.
36. Wagenknecht T, Radermacher M, Grassucci R, Berkowitz J, Xin HB, et al. (1997) Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor. J Biol Chem 272: 32463-32471.
37. Sharma MR, Jeyakumar LH, Fleischer S, Wagenknecht T, (2006) Three-dimensional visualization of FKBP12.6 binding to an open conformation of cardiac ryanodine receptor. Biophys J 90: 164-172.
38. Samso M, Shen XH, Allen PD, (2006) Structural characterization of the RyR1-FKBP12 interaction. J Mol Biol 356: 917-927.
39. Carter S, Pitt SJ, Colyer J, Sitsapesan R, (2011) Ca2+-dependent phosphorylation of RyR2 can uncouple channel gating from direct cytosolic Ca2+ regulation. J Membr Biol 240: 21-33.
40. Sigalas C, Bent S, Kitmitto A, O'Neill S, Sitsapesan R, (2009) Ca2+-calmodulin can activate and inactivate cardiac ryanodine receptors. Br J Pharmacol 156: 794-806.
41. Sitsapesan R, Williams AJ, (1990) Mechanisms of caffeine activation of single calcium-release channels of sheep cardiac sarcoplasmic reticulum. J Physiol 423: 425-439.
42. Lehnart SE, Wehrens XH, Marks AR, (2004) Calstabin deficiency, ryanodine receptors, and sudden cardiac death. Biochem Biophys Res Commun 322: 1267-1279.
43. Huang F, Shan J, Reiken S, Wehrens XH, Marks AR, (2006) Analysis of calstabin2 (FKBP12.6)-ryanodine receptor interactions: rescue of heart failure by calstabin2 in mice. Proc Natl Acad Sci U S A 103: 3456-3461.
44. Pogwizd SM, Bers DM, (2004) Cellular Basis of Triggered Arrhythmias in Heart Failure. Trends Cardiovasc Med 14: 61-66.
45. Eisner DA, Kashimura T, O'Neill SC, Venetucci LA, Trafford AW, (2009) What role does modulation of the ryanodine receptor play in cardiac inotropy and arrhythmogenesis? J Mol Cell Cardiol 46: 474-481.
46. Venetucci LA, Trafford AW, O'Neill SC, Eisner DA, (2008) The sarcoplasmic reticulum and arrhythmogenic calcium release. Cardiovasc Res 77: 285-292.
47. Ng GA, Cobbe SM, Smith GL, (1998) Non-uniform prolongation of intracellular Ca2+ transients recorded from the epicardial surface of isolated hearts from rabbits with heart failure. Cardiovasc Res 37: 489-502.
48. Sobie EA, Guatimosim S, Gómez-Viquez L, Song L-S, Hartmann H, et al. (2005) The Ca2+ leak paradox and "rogue ryanodine receptors": SR Ca2+ efflux theory and practice. Prog Biophys Mol Biol 90: 172-185.
49. Trafford AW, Sibbring GC, Diaz ME, Eisner DA, (2000) The effects of low concentrations of caffeine on spontanteous Ca2+ release in isolated rat ventricular myocytes. Cell Calcium 28: 269-276.
50. Seidler T, Teucher N, Hellenkamp K, Unsöld B, Grebe C, et al. (2011) Limitations of FKBP12.6-directed treatment strategies for maladaptive cardiac remodeling and heart failure. J Mol Cell Cardiol 50: 33-42.
51. Huang F, Shan J, Reiken S, Wehrens XH, Marks AR, (2006) Analysis of calstabin2 (FKBP12.6)-ryanodine receptor interactions: rescue of heart failure by calstabin2 in mice. Proc Natl Acad Sci U S A 103: 3456-3461.
52. Jeyakumar LH, Ballester L, Cheng DS, McIntyre JO, Chang P, et al. (2001) FKBP binding characteristics of cardiac microsomes from diverse vertebrates. Biochem Biophys Res Commun 281: 979-986.
53. Ahern GP, Junankar PR, Dulhunty AF, (1994) Single channel activity of the ryanodine receptor calcium release channel is modulated by FK-506. FEBS Lett 352: 369-374.
54. Sitsapesan R, Williams AJ, (1994) Gating of the native and purified cardiac SR Ca 2+-release channel with monovalent cations as permeant species. Biophys J 67: 1484-1494.
55. Overend CL, Eisner DA, O'Neill SC, (1997) The effect of tetracaine on spontaneous Ca2+ release and sarcoplasmic reticulum calcium content in rat ventricular myocytes. J Physiol 502 (Pt 3): 471-479.
56. Seidler T, Loughrey CM, Zibrova D, Kettlewell S, Teucher N, et al. (2007) Overexpression of FK-506 binding protein 12.0 modulates excitation contraction coupling in adult rabbit ventricular cardiomyocytes. Circ Res 101: 1020-1029.
57. Marks AR, (2000) Cardiac intracellular calcium release channels- Role in heart failure. Circ Res 87: 8-11.
58. Valdivia HH, (2001) Cardiac Ryanodine Receptors and Accessory Proteins. Augmented Expression Does Not Necessarily Mean Big Function. Circ Res 88: 134-136.
59. Valdivia HH, Jiang MT, Lokuta AJ, Farrell EF, Wolff MR, et al. (2002) Abnormal Ca2+ release, but normal ryanodine receptors, in canine and human heart failure. Circ Res 91: 1015-1022.