Pore dynamics and conductance of RyR1 transmembrane domain

Biophysical Journal

Volumn 106, Issue 11, 2014, Pages 2375-2384

  Shirvanyants, David ^a   Ramachandran, Srinivas ^a   Mei, Yingwu ^a   Xu, Le ^a   Meissner, Gerhard ^a   Dokholyan, Nikolay V ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; RYANODINE RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL; CHANNEL GATING; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MUTATION; PROTEIN TERTIARY STRUCTURE; RABBIT;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; ION CHANNEL GATING; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, TERTIARY; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84901992339     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.04.023     Document Type: Article

References (61)

1. F. Dabertrand, M.T. Nelson, and J.E. Brayden Ryanodine receptors, calcium signaling, and regulation of vascular tone in the cerebral parenchymal microcirculation Microcirculation 20 2013 307 316
2. C. Franzini-Armstrong, and F. Protasi Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions Physiol. Rev. 77 1997 699 729 (Pubitemid 27328738)
3. J.T. Lanner, and D.K. Georgiou S.L. Hamilton Ryanodine receptors: structure, expression, molecular details, and function in calcium release Cold Spring Harb. Perspect. Biol. 2 2010 a003996
4. M. Samsó, T. Wagenknecht, and P.D. Allen Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM Nat. Struct. Mol. Biol. 12 2005 539 544 (Pubitemid 43085885)
5. S. Ramachandran, and A. Chakraborty G. Meissner Structural determinants of skeletal muscle ryanodine receptor gating J. Biol. Chem. 288 2013 6154 6165
6. S. Ramachandran, and A.W. Serohijos N.V. Dokholyan A structural model of the pore-forming region of the skeletal muscle ryanodine receptor (RyR1) PLOS Comput. Biol. 5 2009 e1000367
7. W. Treptow, and M.L. Klein Computer simulations of voltage-gated cation channels J. Phys. Chem. Let. 3 2012 1017 1023
8. B. Corry, and M. Thomas Mechanism of ion permeation and selectivity in a voltage gated sodium channel J. Am. Chem. Soc. 134 2012 1840 1846
9. C. Domene, and S. Furini Molecular dynamics simulations of the TrkH membrane protein Biochemistry 51 2012 1559 1565
10. S. Durdagi, and S. Deshpande S.Y. Noskov Modeling of open, closed, and open-inactivated states of the hERG1 channel: structural mechanisms of the state-dependent drug binding J. Chem. Inf. Model. 52 2012 2760 2774
11. T.W. Allen, O.S. Andersen, and B. Roux Ion permeation through a narrow channel: using gramicidin to ascertain all-atom molecular dynamics potential of mean force methodology and biomolecular force fields Biophys. J. 90 2006 3447 3468
12. + channels Proc. Natl. Acad. Sci. USA 107 2010 5833 5838
13. J. Timko, and S. Kuyucak Investigation of polarization effects in the gramicidin A channel from ab initio molecular dynamics simulations J. Chem. Phys. 137 2012 205106
14. D.B. Wells, and S. Bhattacharya A. Aksimentiev Optimization of the molecular dynamics method for simulations of DNA and ion transport through biological nanopores Methods Mol. Biol. 870 2011 165 186
15. S.E. Feller, and A.D. MacKerell An improved empirical potential energy function for molecular simulations of phospholipids J. Phys. Chem. B 104 2000 7510 7515
16. J.B. Klauda, and B.R. Brooks R.W. Pastor An ab initio study on the torsional surface of alkanes and its effect on molecular simulations of alkanes and a DPPC bilayer J. Phys. Chem. B 109 2005 5300 5311 (Pubitemid 40407752)
17. D.X. Yin, and A.D. MacKerell Combined ab initio empirical approach for optimization of Lennard-Jones parameters J. Comput. Chem. 19 1998 334 348
18. J.B. Klauda, and R.M. Venable R.W. Pastor Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types J. Phys. Chem. B 114 2010 7830 7843
19. D.P. Tieleman, M.S. Sansom, and H.J. Berendsen Alamethicin helices in a bilayer and in solution: molecular dynamics simulations Biophys. J. 76 1999 40 49 (Pubitemid 29202436)
20. M.O. Jensen, and V. Jogini D.E. Shaw Mechanism of voltage gating in potassium channels Science 336 2012 229 233
21. K. Lindorff-Larsen, and P. Maragakis D.E. Shaw Systematic validation of protein force fields against experimental data PLoS ONE 7 2012 e32131
22. O.S. Smart, J.M. Goodfellow, and B.A. Wallace The pore dimensions of gramicidin A Biophys. J. 65 1993 2455 2460 (Pubitemid 24005977)
23. 2+ release channel (ryanodine receptor) function FEBS Lett. 412 1997 223 226 (Pubitemid 27310034)
24. 2+ release channel (ryanodine receptor) activity and conductance Biophys. J. 79 2000 828 840 (Pubitemid 30626177)
25. 2+ release channel protein complex into proteoliposomes J. Biol. Chem. 269 1994 13305 13312
26. J.L. Sutko, and J.A. Airey L. Ruest The pharmacology of ryanodine and related compounds Pharmacol. Rev. 49 1997 53 98 (Pubitemid 27142417)
27. T.W. Allen, S. Kuyucak, and S.H. Chung Molecular dynamics estimates of ion diffusion in model hydrophobic and KcsA potassium channels Biophys. Chem. 86 2000 1 14 (Pubitemid 30440625)
28. T.A. Hilder, and S.H. Chung Conductance properties of the inwardly rectifying channel, Kir3.2: molecular and Brownian dynamics study Biochim. Biophys. Acta 1828 2013 471 478
29. T.W. Allen, O.S. Andersen, and B. Roux On the importance of atomic fluctuations, protein flexibility, and solvent in ion permeation J. Gen. Physiol. 124 2004 679 690 (Pubitemid 39628135)
30. + channel Nature 414 2001 73 77 (Pubitemid 33041625)
31. 2+-release channel by tetra-alkyl ammonium cations J. Membr. Biol. 127 1992 149 159
32. B. Roux, and M. Karplus Ion-transport in a gramicidin-like channel - dynamics and mobility J. Phys. Chem. 95 1991 4856 4868
33. + selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates J. Mol. Biol. 333 2003 965 975 (Pubitemid 37324499)
34. D. Gillespie, and L. Xu G. Meissner (De)constructing the ryanodine receptor: modeling ion permeation and selectivity of the calcium release channel J. Phys. Chem. B 109 2005 15598 15610 (Pubitemid 41260811)
35. + selectivity filter Nature 414 2001 37 42
36. B. Hille, and A.E. Stuart Ion Channels of Excitable Membranes 2001 Sinauer Sunderland, MA
37. G. Meissner Molecular regulation of cardiac ryanodine receptor ion channel Cell Calcium 35 2004 621 628 (Pubitemid 38618574)
38. J.S. Smith, and T. Imagawa R. Coronado Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum J. Gen. Physiol. 92 1988 1 26
39. + channel-Fab complex at 2.0 Å resolution Nature 414 2001 43 48 (Pubitemid 33041616)
40. S.Y. Noskov, S. Bernèche, and B. Roux Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands Nature 431 2004 830 834 (Pubitemid 39434076)
41. D. Gillespie, and R.S. Eisenberg Physical descriptions of experimental selectivity measurements in ion channels Eur. Biophys. J. 31 2002 454 466 (Pubitemid 36163886)
42. D. Gillespie, W. Nonner, and R.S. Eisenberg Coupling Poisson-Nernst- Planck and density functional theory to calculate ion flux J. Phys. Condens. Matter 14 2002 12129 12145 (Pubitemid 35434013)
43. L. Xu, and Y. Wang G. Meissner Two rings of negative charges in the cytosolic vestibule of type-1 ryanodine receptor modulate ion fluxes Biophys. J. 90 2006 443 453
44. Y. Wang, and L. Xu G. Meissner Probing the role of negatively charged amino acid residues in ion permeation of skeletal muscle ryanodine receptor Biophys. J. 89 2005 256 265 (Pubitemid 41098280)
45. 2+ release channels? Trends Cardiovasc. Med. 12 2002 189 197 (Pubitemid 34823628)
46. 2+ release Biochem. J. 382 2004 557 564 (Pubitemid 39243922)
47. L. Xu, and Y. Wang G. Meissner Single channel properties of heterotetrameric mutant RyR1 ion channels linked to core myopathies J. Biol. Chem. 283 2008 6321 6329
48. 2+ ion permeation and release from the sarcoplasmic reticulum J. Gen. Physiol. 137 2011 43 57
49. + conduction and selectivity Science 280 1998 69 77 (Pubitemid 28169082)
50. Y. Jiang, and A. Lee R. MacKinnon Crystal structure and mechanism of a calcium-gated potassium channel Nature 417 2002 515 522 (Pubitemid 34595912)
51. A. Alam, and Y. Jiang Structural analysis of ion selectivity in the NaK channel Nat. Struct. Mol. Biol. 16 2009 35 41
52. A. Kuo, and J.M. Gulbis D.A. Doyle Crystal structure of the potassium channel KirBac1.1 in the closed state Science 300 2003 1922 1926 (Pubitemid 36734594)
53. A. Tinker, and A.J. Williams Probing the structure of the conduction pathway of the sheep cardiac sarcoplasmic reticulum calcium-release channel with permeant and impermeant organic cations J. Gen. Physiol. 102 1993 1107 1129 (Pubitemid 24004322)
54. 2+ release channel Biophys. J. 67 1994 2280 2285 (Pubitemid 24369651)
55. T.W. Allen, S. Kuyucak, and S.H. Chung Molecular dynamics study of the KcsA potassium channel Biophys. J. 77 1999 2502 2516 (Pubitemid 29519497)
56. W. Welch, and S. Rheault A.J. Williams A model of the putative pore region of the cardiac ryanodine receptor channel Biophys. J. 87 2004 2335 2351 (Pubitemid 41071334)
57. 2+-release channel tunnel: structures and mechanisms involved in ion translocation in ryanodine receptor channels Q. Rev. Biophys. 34 2001 61 104 (Pubitemid 32510204)
58. + channel Nature 423 2003 33 41 (Pubitemid 36569577)
59. + permeation Proc. Natl. Acad. Sci. USA 108 2011 16634 16639
60. D. Balshaw, L. Gao, and G. Meissner Luminal loop of the ryanodine receptor: a pore-forming segment? Proc. Natl. Acad. Sci. USA 96 1999 3345 3347 (Pubitemid 29168914)
61. J. Euden, S.A. Mason, and A.J. Williams Functional characterization of the cardiac ryanodine receptor pore-forming region PLoS ONE 8 2013 e66542