Subconductance states in single-channel activity of skeletal muscle ryanodine receptors after removal of FKBP12

Biophysical Journal

Volumn 72, Issue 1, 1997, Pages 146-162

  Ahern, Gerard P ^a,b   Junankar, Pauline R ^a   Dulhunty, Angela F ^a  

^a Biology and Environment   (Australia)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; MEMBRANE PROTEIN; RUTHENIUM RED; RYANODINE; RYANODINE RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHANNEL GATING; LIPID BILAYER; MEMBRANE CHANNEL; MEMBRANE CONDUCTANCE; MEMBRANE POTENTIAL; NONHUMAN; RABBIT; SKELETAL MUSCLE;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0031020935     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78654-5     Document Type: Article

References (75)

1. Ahern, G. P., P. R. Junankar, and A. F. Dulhunty. 1994. Single channel activity of the ryanodine receptor calcium release channel is modulated by FK-506. FEBS Lett. 352:369-374.
2. Ahern, G. P., P. R. Junankar, and A. F. Dulhunty. 1995. Control of ryanodine receptor function by relative association of FK506-binding protein (FKBP12) monomers. Proc. Aust. Physiol. Pharmacol. Soc. 26(2):180P.
3. Ahern, G. P., P. R. Junankar, and A. F. Dulhunty. 1996. Immunosuppressant/macrolide activation of ryanodine receptor independent of FK506-binding protein (FKBP12) association. Biophys. J. 70: A389.
4. 2+ signaling in neutrophils by the mast cell-released immunophilin FKBP12. Proc. Natl. Acad. Sci. USA. 92:3435-3438.
5. Block, B. A., T. Imagawa, K. P. Campbell, and C. Franzini-Armstrong. 1988. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 107:2587-2600.
6. Brillantes, A.-M. B., K. Ondrias, A. Scott, E. Kobrinsky, E. Ondriasová, M. C. Moschella, T. Jayaraman, M. Landers, B. E. Ehrlich, and A. R. Marks. 1994. Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell. 77:513-523.
7. Buck, E., I. Zimanyi, J. J. Abramson, and I. N. Pessah. 1992. Ryanodine stabilizes multiple conformational states of the skeletal muscle calcium release channel. J. Biol. Chem. 267:23560-23567.
8. 2+ release channel. J. Biol. Chem. 269: 15,876-15,884.
9. Cameron, A. M., J. P. Steiner, D. M. Sabatini, A. I. Kaplin, L. D. Walensky, and S. H. Snyder. 1995. Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. USA. 92:1784-1788.
10. Caswell, A. H., N. R. Brandt, J.-P. Brunschwig, and S. Purkerson. 1991. Localization and partial characterization of the oligomeric disulphide-linked molecular weight 95000 protein (triadin) which binds the ryanodine and dihydropyridine receptors in skeletal muscle triadic vesicles. Biochemistry. 30:7507-7513.
11. Chandler, W. K., R. F. Rakowski, and M. F. Schneider. 1976. Effects of glycerol treatment and maintained depolarization on charge movement in skeletal muscle. J. Physiol. 254:285-316.
12. Chu, A., M. Diaz-Munoz, M. J. Hawkes, K. Brush, and S. L. Hamilton. 1990. Ryanodine as a probe for the functional state of the skeletal muscle sarcoplasmic reticulum calcium release channel. Mol. Pharmacol. 37: 735-741.
13. Collins, J. H., A. Tarcsafalvi, and N. Ikemoto. 1990. Identification of a region of calsequestrin that binds to the junctional face membrane of sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 167: 189-193.
14. Dulhunty, A. F. 1992. The voltage-activation of contraction in skeletal muscle. Prog. Biophys. Molec. Biol. 57:181-223.
15. Fleischer, S., and M. Inui. 1989. Biochemistry and biophysics of excitation-contraction coupling. Annu. Rev. Biophys. Biophys. Chem. 18: 333-364.
16. Galat, A. 1993. Peptidylproline cis-trans-isomerases: immunophilins. Eur. J. Biochem. 216:689-707.
17. Green, N., H. Alexander, A. Olsen, S. Alexander, T. M. Shinnick, J. G. Sutcliffe, and R. A. Lerner. 1982. Immunogenic structure of the influenza virus hemaglutinin. Cell. 28:477-487.
18. Guo, W., and K. P. Campbell. 1995. Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J. Biol. Chem. 270:9027-9030.
19. Harding, M. W., A. Galat, D. E. Uehling, and S. L. Schreiber. 1989. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature (London). 341:758-760.
20. 2+ channels in planar bilayers. Proc. Natl. Acad. Sci. USA. 85:441-445.
21. Ikemoto, N., M. Ronjat, L. G. Meszaros, and M. Koshita. 1989. Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry. 28:6764-6771.
22. Jayaraman, T., A.-M. Brillantes, A. P. Timerman, S. Fleischer, H. Erdjument-Bromage, P. Tempst, and A. R. Marks. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267:9474-9477.
23. 2+-release channels from cardiac muscle. Circ. Res. 78:990-997.
24. Kay, J. E. 1996. Structure-function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 314:361-385.
25. Kourie, J. I., D. R. Laver, G. P. Ahern, and A. F. Dulhunty. 1996a. A calcium-activated chloride channel in sarcoplasmic reticulum vesicles from rabbit skeletal muscle. Am. J. Physiol. 270:C1675-C1686.
26. Kourie, J. I., D. R. Laver, P. R. Junankar, P. W. Gage, and A. F. Dulhunty. 1996b. Characteristics of two types of chloride channel in sarcoplasmic reticulum vesicles from rabbit skeletal muscle. Biophys. J. 70:202-221.
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London). 227:680-685.
28. Lai, F. A., H. P. Erickson, E. Rousseau, Q.-Y. Liu, and G. Meissner. 1988. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature (London). 331:315-319.
29. Lam, E., M. M. Martin, A. P. Timerman, C. Sabers, S. Fleischer, T. Lukas, R. T. Abraham, S. J. O'Keefe, E. A. O'Neill, and G. J. Wiederrecht. 1995. A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J. Biol. Chem. 270:26,511-26,522.
30. Lamb, G. D., and D. G. Stephenson. 1996. Effects of FK506 and rapamycin on excitation-contraction coupling in skeletal muscle fibres of the rat. J. Physiol. 494:569-576.
31. 2+ inhibits the ryanodine receptor from cardiac muscle. J. Membr. Biol. 147:7-22.
32. Laver, D. R., T. M. Baynes, and A. F. Dulhunty. 1997. Magnesium inhibition of ryanodine receptor calcium channels: evidence for two independent mechanisms. J. Membr. Biol. In press.
33. Leiva, M. C., and C. R. Lyttle. 1992. Leukocyte chemotactic activity of FKBP and inhibition by FK506. Biochem. Biophys. Res. Commun. 186:1178-1183.
34. Liu, Q. Y., F. A. Lai, E. Rousseau, R. V. Jones, and G. Meissner. 1989. Multiple conductance states of the purified calcium release channel ; complex from skeletal sarcoplasmic reticulum. Biophys. J. 55:415-424.
35. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
36. Ma, J. 1993. Block by ruthenium red of the ryanodine-activated calcium release channel of skeletal muscle. J. Gen. Physiol. 102:1031-1056.
37. Ma, J. 1995. Desensitization of the skeletal muscle ryanodine receptor: evidence for heterogeneity of calcium release channels. Biophys. J. 68:893-899.
38. Ma, J., M. B. Bhat, and J. Y. Zhao. 1995. Rectification of skeletal muscle ryanodine receptor mediated by FK506 binding protein. Biophys. J. 69:2398-2404.
39. Ma, J., M. Fill, C. M. Knudson, K. P. Campbell, and R. Coronado. 1988. Ryanodine receptor of skeletal muscle is a gap junction-type channel. Science. 242:99-102.
40. Ma, J., and J. Zhao. 1994. Highly cooperative and hysteretic response of the skeletal muscle ryanodine receptor to changes in proton concentrations. Biophys. J. 67:626-633.
41. Mack M. M., T. F. Molinski, E. D. Buck, and I. N. Pessah. 1994. Novel modulators of skeletal muscle FKBP12/calcium channel complex from Ianthella basta. Role of FKBP12 in channel gating. J. Biol. Chem. 269:23,236-23,249.
42. Mayrleitner, M., A. P. Timerman, G. Wiederrecht, and S. Fleischer. 1994. The calcium release channel of sarcoplasmic reticulum is modulated by FK-506 binding protein: effect of FKBP-12 on single channel activity of the skeletal muscle ryanodine receptor. Cell Calcium. 15:99-108.
43. McGrew, S. G., C. Wolleben, P. Siegl, M. Inui, and S. Fleischer. 1989. Positive cooperativity of ryanodine binding to the calcium release channel of the sarcoplasmic reticulum from heart and skeletal muscle. Biochemistry. 28:1686-1691.
44. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56:485-508.
45. 2+ ions in excitation-contraction coupling of skeletal muscle fibres. Biochim. Biophys. Acta. 1241:59-116.
46. Menegazzi, P., F. Larini, S. Treves, R. Guerrini, M. Quadroni, and F. Zorzato. 1994. Identification and characterization of three calmodulin binding sites of the skeletal muscle ryanodine receptor. Biochemistry. 33:9078-9084.
47. Orlova E. V., I. I. Serysheva, M. van Heel, S. L. Hamilton, and W. Chiu. 1996. Two structural configurations of the skeletal muscle calcium release channel. Nature Struct. Biol. 3:547-552
48. Patlak, J. B. 1988. Sodium channel subconductance levels measured with a new variance-mean analysis. J. Gen. Physiol. 92:413-430.
49. Radermacher, M., V. Rao, R. Grassucci, J. Frank, A. P. Timerman, S. Fleischer, and T. Wagenknecht. 1994. Cryo-electron microscopy and three-dimensional reconstruction of the calcium release channel/ ryanodine receptor from skeletal muscle. J. Cell Biol. 127:411-423.
50. Radermacher, M., T. Wagenknecht, R. Grassucci, J. Frank, M. Inui, C. Chadwick and S. Fleischer. 1992. Cryo-EM of the native structure of the calcium release channel/ryanodine receptor from sarcoplasmic reticulum. Biophys. J. 61:936-940.
51. Reik, L. M., S. L. Maines, D. E. Ryan, W. Levin, S. Bandiera, and P. E. Thomas. 1987. A simple, non-chromatographic purification procedure for monoclonal antibodies. J. Immunol. Methods. 100:123-130.
52. Rios, E., G. Pizarro, and E. Stefani. 1992. Charge movement and the nature of signal transduction in skeletal muscle excitation-contraction coupling. Annu. Rev. Physiol. 54:109-133.
53. Saito, A., S. Seiler, A. Chu, and S. Fleischer. 1984. Preparation and morphology of sarcoplasmic reticulum terminal cistemae from rabbit skeletal muscle. J. Cell Biol. 99:875-885.
54. Schreiber, S. L., and G. R. Crabtree. 1992. The mechanism of action of cyclosporin A and FK506. Immunol. Today 13:136-142.
55. Serysheva, I. I., E. V. Orlova, W. Chiu, M. B. Sherman, S. L. Hamilton, and M. Van Heel. 1995. Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel. Nature Struct. Biol. 2:18-24.
56. Sigworth, F. J., and S. M. Sine. 1987. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52:1047-1054.
57. 2+. J. Membr. Biol. 146:133-144.
58. 2+ release channel of rabbit skeletal muscle. Biophys. J. 70:A128
59. Smith, J. S., R. Coronado, and G. Meissner. 1986. Single channel measurements of the calcium release channel from skeletal muscle sarcoplasmic reticulum. J. Gen. Physiol. 88:573-588.
60. Smith, J. S., T. Imagawa, J. Ma, M. Fill, K. P. Campbell, and R. Coronado. 1988. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J. Gen. Physiol. 92:1-26.
61. Standaert, R. F., A. Galat, G. L. Verdine, and S. L. Schreiber. 1990. Molecular cloning and overexpression of the human FK506-binding protein FKBP. Nature (London). 346:671-674.
62. Takeda, K., and A. Trautmann. 1984. A patch-clamp study of the partial agonist actions of tubocurarine on rat myotubes. J. Physiol. 349: 353-374.
63. Timerman, A. P., T. Jayaraman, G. Wiederrecht, H. Onoue, A. R. Marks, and S. Fleischer. 1994. The ryanodine receptor from canine heart sarcoplasmic reticulum is associated with a novel FK-506 binding protein. Biochem. Biophys. Res. Commun. 198:701-716.
64. Timerman, A. P., E. Ogunbumni, E. Freund, G. Wiederrecht, A. R. Marks, and S. Fleischer. 1993. The calcium release channel of sarcoplasmic reticulum is modulated by FK-506-binding protein. Dissociation and reconstitution of the FKBP-12 to the calcium release channel of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 268:22,992-22,999.
65. Timerman, A. P., H. Onoue, H.-B. Xin, S. Barg, J. Copello, G. Wiederrecht, and S. Fleischer. 1996. Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J. Biol. Chem. 271:20,385-20,391.
66. Timerman, A. P., G. Wiederrecht, A. Marcy, and S. Fleischer. 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.
67. Tinker, A., A. R. G. Lindsay, and A. J. Williams. 1992. A model for ionic conduction in the ryanodine receptor channel of sheep cardiac muscle sarcoplasmic reticulum. J. Gen. Physiol. 100:495-517.
68. 2+ release channel (ryanodine receptor). Biophys. J. 69:106-119.
69. + channel from Chara corallina shown by a transient analysis method. Biophys. J. 61:736-749.
70. Wagenknecht, T., J. Berkowitz, R. Grassucci, A. P. Timerman, and S. Fleischer. 1994. Localization of calmodulin binding sites on the ryanodine receptor from skeletal muscle by electron microscopy. Biophys. J. 67:2286-2295.
71. Wagenknecht, T., R. Grassucci, J. Berkowitz, G. J. Wiederrecht, H. B. Xin, and S. Fleischer. 1996. Cryoelectron microscopy resolves FK506-binding protein sites on the skeletal muscle ryanodine receptor. Biophys. J. 70:1709-1715.
72. Wagenknecht, T., and M. Radermacher. 1995. Three-dimensional architecture of the skeletal muscle ryanodine receptor. FEBS Lett. 369:43-46.
73. 2+ release channel. J. Biol. Chem. 268: 20,974-20,982.
74. Wang, T., P. K. Donahoe, and A. S. Zervos. 1994. Specific interaction of type 1 receptors of the TGF-B family with the immunophilin FKBP-12. Science. 265:674-676.
75. 2+ release channel with an azido derivative of ryanodine. J. Biol. Chem. 269:13,076-13,079.