MD simulations of the central pore of ryanodine receptors and sequence comparison with 2B protein from coxsackie virus

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 4, 2014, Pages 1122-1131

  Schilling, Roman ^a   Fink, Rainer H A ^a   Fischer, Wolfgang B ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

2B of coxsackie virus; Ca homeostasis; Ion dynamics; Molecular dynamics simulations; Ryanodine receptor; Viral channel proteins

Indexed keywords

CALCIUM; PROTEIN 2B; RYANODINE RECEPTOR; RYANODINE RECEPTOR 1; RYANODINE RECEPTOR 2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CALCIUM METABOLISM; CALCIUM TRANSPORT; COMPARATIVE STUDY; CONTROLLED STUDY; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

COXSACKIEVIRUS;

2B OF COXSACKIE VIRUS; CA HOMEOSTASIS; ION DYNAMICS; MOLECULAR DYNAMICS SIMULATIONS; RYANODINE RECEPTOR; VIRAL CHANNEL PROTEINS;

AMINO ACID SEQUENCE; CALCIUM; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; VIRAL PROTEINS;

EID: 84895527739     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.12.008     Document Type: Article

References (57)

1. 2 + and virus Cell Calcium 46 2009 1 17
2. C. Brisac, F. Teoule, A. Autret, I. Pelletier, F. Colbere-Garapin, C. Brenner, C. Lemaire, and B. Blondel Calcium flux between the endoplasmic reticulum and mitochondrion contributes to poliovirus-induced apoptosis J. Virol. 84 2010 12226 12235
3. R. Zalk, S.E. Lehnart, and A.R. Marks Modulation of the ryanodine receptor and intracellular calcium Annu. Rev. Biochem. 76 2007 367 385
4. J.T. Lanner, D.K. Georgiou, A.D. Joshi, and S.L. Hamilton Ryanodine receptors: structure, expression, molecular details, and function in calcium release Cold Spring Harb. Perspect. Biol. 2 2010 a003996
5. M. Mosqueira, U. Zeiger, M. Förderer, H. Brinkmeier, and R.H. Fink Cardiac and respiratory dysfunction in Duchenne muscular dystrophy and the role of second messengers Med. Res. Rev. 33 2013 1174 1213
6. F. Van Petegem Ryanodine receptors: structure and function J. Biol. Chem. 287 2012 31624 31632
7. S.J. Ludtke, I.I. Serysheva, S.L. Hamilton, and W. Chiu The pore structure of the closed RyR1 channel Structure 13 2005 1203 1211
8. M. Samso, 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
9. M. Samso, W. Feng, I.N. Pessah, and P.D. Allen Coordinated movement of cytoplasmic and transmembrane domains of RyR1 upon gating PLoS Biol. 7 2009 e85
10. 2 + release channel of skeletal muscle sarcoplasmic reticulum (RyR1) Proc. Natl. Acad. Sci. U. S. A. 99 2002 16725 16730
11. G.G. Du, G. Avila, P. Sharma, V.K. Khanna, R.T. Dirksen, and D.H. MacLennan Role of the sequence surrounding predicted transmembrane helix M4 in membrane association and function of the Ca(2 +) release channel of skeletal muscle sarcoplasmic reticulum (ryanodine receptor isoform 1) J. Biol. Chem. 279 2004 37566 37574
12. G. Orthopoulos, K. Triantafilou, and M. Triantafilou Coxsackie B viruses use multiple receptors to infect human cardiac cells J. Med. Virol. 74 2004 291 299
13. F.J.M. van Kuppeveld, J.G.J. Hoenderop, R.L.L. Smeets, P.H.G.M. Willems, H.B.P.M. Dijkman, J.M.D. Galama, and W.J.G. Melchers Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release EMBO J. 16 1997 3519 3532
14. F.J.M. van Kuppeveld, W.J.G. Melchers, K. Kirkegaard, and J.R. Doedens Structure-function analysis of Coxsackie B3 virus protein 2B Virology 227 1997 111 118
15. F.J.M. van Kuppeveld, J.M.D. Galama, J. Zoll, P.J.J.C. van den Hurk, and W.J.G. Melchers Coxsackie B3 virus protein 2B contains a cationic amphipathic helix that is required for viral RNA replication J. Virol. 70 1996 3876 3886
16. A.S. de Jong, H.-J. Visch, F. de Mattia, M.M. van Dommelen, H.G. Swart, T. Luyten, G. Callewaert, W.J. Melchers, P.H. Willems, and F.J. Van Kuppeveld The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi J. Biol. Chem. 281 2006 14144 14150
17. G. Patargias, T. Barke, A. Watts, and W.B. Fischer Model generation of viral channel forming 2B protein bundles from polio and coxsackie viruses Mol. Membr. Biol. 26 2009 309 320
18. W.B. Fischer, Y.-T. Wang, C. Schindler, and C.-P. Chen Mechanism of function of viral channel proteins and implications for drug development Int. Rev. Cell Mol. Biol. 294 2012 259 321
19. K. Hsu, J. Seharaseyon, P. Dong, S. Bour, and E. Marbán Mutual functional destruction of HIV-1 Vpu and host TASK-1 channel Mol. Cell 14 2004 259 267
20. A. Krogh, B. Larsson, G. von Heijne, and E.L. Sonnhammer Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 305 2001 567 580
21. T. Hirokawa, S. Boon-Chieng, and S. Mitaku SOSUI: classification and secondary structure prediction system for membrane proteins Bioinformatics 14 1998 378 379
22. Z. Yuan, J.S. Mattick, and R.D. Teasdale SVMtm: support vector machines to predict transmembrane segments J. Comput. Chem. 25 2004 632 636
23. L. Käll, A. Krogh, and E.L. Sonnhammer A combined transmembrane topology and signal peptide prediction method J. Mol. Biol. 338 2004 1027 1036
24. G.E. Tusnady, and I. Simon The HMMTOP transmembrane topology prediction server Bioinformatics 17 2001 849 850
25. H. Viklund, and A. Elofsson OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar Bioinformatics 24 2008 1662 1668
26. T. Nugent, and D.T. Jones Transmembrane protein topology prediction using support vector machines BMC Bioinforma. 10 2009 159
27. + channel and its dependence on the lipid membrane Proc. Natl. Acad. Sci. U. S. A. 102 2005 15441 15446
28. C. Wang, P. Bradley, and D. Baker Protein-protein docking with backbone flexibility J. Mol. Biol. 373 2007 503 519
29. V. Yarov-Yarovoy, J. Schonbrun, and D. Baker Multipass membrane protein structure prediction using Rosetta Proteins 62 2006 1010 1025
30. P. Barth, J. Schonbrun, and D. Baker Toward high-resolution prediction and design of transmembrane helical protein structures Proc. Natl. Acad. Sci. U. S. A. 104 2007 15682 15687
31. S. Pronk, S. Pall, R. Schulz, P. Larsson, P. Bjelkmar, R. Apostolov, M.R. Shirts, J.C. Smith, P.M. Kasson, D. van der Spoel, B. Hess, and E. Lindahl GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29 2013 845 854
32. G.E. Tusnády, Z. Dosztányi, and I. Simon TMDET: web server for detecting transmembrane regions of proteins by using their 3D coordinates Bioinformatics 21 2005 1276 1277
33. M.G. Wolf, M. Hoefling, C. Aponte-Santamaría, H. Grubmüller, and G. Groenhof g-membed: efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation J. Comput. Chem. 31 2010 2169 2174
34. S. Ramachandran, A.W. Serohijos, L. Xu, G. Meissner, and N.V. Dokholyan A structural model of the pore-forming region of the skeletal muscle ryanodine receptor (RyR1) PLoS Comput. Biol. 5 2009 e1000367
35. L.D. Schuler, X. Daura, and W.F. van Gunsteren An improved GROMOS96 force field for aliphatic hydrocarbons in the condensed phase J. Comput. Chem. 22 2001 1205 1218
36. J. Krüger, and W.B. Fischer Exploring the conformational space of Vpu from HIV-1: a versatile adaptable protein J. Comput. Chem. 29 2008 2416 2424
37. I. Chandrasekhar, M. Kastenholz, R.D. Lins, C. Oostenbrink, L.D. Schuler, D.P. Tieleman, and W.F. van Gunsteren A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field Eur. Biophys. J. 32 2003 67 77
38. G.M. Torrie, and J.P. Valleau Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling J. Comput. Phys. 23 1977 187 199
39. B. Corry, and M. Thomas Mechanism of ion permeation and selectivity in a voltage gated sodium channel J. Am. Chem. Soc. 134 2011 1840 1846
40. S. Furini, and C. Domene On conduction in a bacterial sodium channel PLoS Comput. Biol. 8 2012 e1002476
41. J.S. Hub, B.L. de Groot, and D. van der Spoel g-wham - a free weighted histogram analysis implementation including robust error and autocorrelation estimates J. Chem. Theory Comput. 6 2010 3713 3720
42. 2 + release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum J. Biol. Chem. 265 1990 2244 2256
43. Y. Wang, L. Xu, D.A. Pasek, D. Gillespie, and 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
44. W. Welch, S. Rheault, D.J. West, and A.J. Williams A model of the putative pore region of the cardiac ryanodine receptor channel Biophys. J. 87 2004 2335 2351
45. Y. Jiang, A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon The open pore conformation of potassium channels Nature 417 2002 523 526
46. + channel-Fab complex at 2.0 A resolution Nature 414 2001 43 48
47. S.A. Goonasekera, N.A. Beard, L. Groom, T. Kimura, A.D. Lyfenko, A. Rosenfeld, I. Marty, A.F. Dulhunty, and R.T. Dirksen Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation-contraction coupling J. Gen. Physiol. 130 2007 365 378
48. S. Ramachandran, A. Chakraborty, L. Xu, Y. Mei, M. Samso, N.V. Dokholyan, and G. Meissner Structural determinants of skeletal muscle ryanodine receptor gating J. Biol. Chem. 288 2013 6154 6165
49. L. Gao, D. Balshaw, L. Xu, A. Tripathy, C. Xin, and G. Meissner Evidence for a role of the lumenal M3-M4 loop in skeletal muscle Ca(2 +) release channel (ryanodine receptor) activity and conductance Biophys. J. 79 2000 828 840
50. F.C. Mead-Savery, R. Wang, B. Tanna-Topan, S.R. Chen, W. Welch, and A.J. Williams Changes in negative charge at the luminal mouth of the pore alter ion handling and gating in the cardiac ryanodine-receptor Biophys. J. 96 2009 1374 1387
51. W.A. Sather, and E.W. McCleskey Permeation and selectivity in calcium channels Annu. Rev. Physiol. 65 2003 133 159
52. R. Chen, and S.H. Chung Complex structures between the N-type calcium channel (CaV2.2) and omega-conotoxin GVIA predicted via molecular dynamics Biochemistry 52 2013 3765 3772
53. D. Gillespie Energetics of divalent selectivity in a calcium channel: the ryanodine receptor case study Biophys. J. 94 2008 1169 1184
54. D. Gillespie, L. Xu, Y. Wang, and 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
55. B. Corry, T.W. Allen, S. Kuyucak, and S.H. Chung Mechanisms of permeation and selectivity in calcium channels Biophys. J. 80 2001 195 214
56. B. Corry, T. Vora, and S.H. Chung Electrostatic basis of valence selectivity in cationic channels Biochim. Biophys. Acta 1711 2005 72 86
57. L. Xu, Y. Wang, D. Gillespie, and 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