Molecular dynamics simulation of dipalmitoylphosphatidylcholine modified with a MTSL nitroxide spin label in a lipid membrane

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 11, 2013, Pages 2770-2777

  Kemmerer, Sabrina ^a,b   Voss, John C ^c   Faller, Roland ^a  

^a University of California Davis   (United States)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DPPC; ESR; Molecular dynamics; Spin marker

Indexed keywords

(2,2,5,5 TETRAMETHYL 2,5 DIHYDRO 1H PYRROL 3 YL)METHYL METHANESULFONOTHIOATE; DIPALMITOYLPHOSPHATIDYLCHOLINE; NITROXIDE; UNCLASSIFIED DRUG;

ARTICLE; COVALENT BOND; DIFFUSION COEFFICIENT; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; SPIN LABELING;

EID: 84883223952     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.07.030     Document Type: Article

References (70)

1. M.R. Alecio, D.E. Golan, W.R. Veatch, and R.R. Rando Use of a fluorescent cholesterol derivative to measure lateral mobility of cholesterol in membranes Proc. Natl. Acad. Sci. USA 79 1982 5171 5174
2. T. Baumgart, S.T. Hess, and W.W. Webb Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 425 2003 821 824 (Pubitemid 37351463)
3. B. Hoff, E. Strandberg, A.S. Ulrich, D.P. Tieleman, and C. Posten 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers Biophys. J. 88 3 2005 1818 1827 (Pubitemid 40976195)
4. J. Curdova, P. Capkova, J. Plasek, J. Repakova, and I. Vattulainen Free pyrene probes in gel and fluid membranes: perspective through atomistic simulations J. Phys. Chem. B 111 14 2007 3640 3650 (Pubitemid 46723992)
5. M.J. Skaug, M.L. Longo, and R. Faller Computational studies of Texas red DHPE - model building and applications J. Phys. Chem. B 113 2009 8758 8766
6. P. Hakansson, P.O. Westlund, E. Lindahl, and O. Edholm A direct simulation of EPR slow-motion spectra of spin labelled phospholipids in liquid crystalline bilayers based on a molecular dynamics simulation of the lipid dynamics Phys. Chem. Chem. Phys. 3 2001 5311 5319
7. J. Mravljak, J. Konc, M. Hodoscek, T. Solmajer, and S. Pecar Spin-labeled alkylphospholipids in a dipalmitoylphosphatidylcholine bilayer: molecular dynamics simulations J. Phys. Chem. B 110 51 2006 25559 25561 (Pubitemid 46137753)
8. L. Stimson, L. Dong, M. Karttunen, A. Wisniewska, M. Dutka, and T. Rog Stearic acid spin labels in lipid bilayers: insight through atomistic simulations J. Phys. Chem. B 111 43 2007 12447 12453 (Pubitemid 350097590)
9. M.R. Vartorelli, A.S. Garay, and D.E. Rodrigues Spin-labeled stearic acid behavior and perturbations on the structure of a gel-phase-lipid bilayer in water: 5-, 12- and 16-SASL J. Phys. Chem. B 112 51 2008 16830 16842
10. W.L. Hubbell, D.S. Cafiso, and C. Altenbach Identifying conformational changes with site-directed spin labeling Nat. Struct. Mol. Biol. 7 9 2000 735 739
11. H. Mchaourab, P. Steed, and K. Kazmier Toward the fourth dimension of membrane protein structure: insight into dynamics from spin-labeling EPR spectroscopy Structure 19 11 2011 1549 1561
12. D. Marsh Electron spin resonance in membrane research: protein-lipid interactions from challenging beginnings to state of the art Eur. Biophys. J. 39 4 2010 513 525
13. A.M. Gotto, H. Kon, and M.E. Birnbaumer Electron spin resonance studies of lipid-protein interaction in human serum lipoproteins Proc. Natl. Acad. Sci. U. S. A. 65 1 1970 145 151
14. S.D. Tetali, M.S. Budamagunta, C. Simion, L.J. den Hartigh, T. Kálai, K. Hideg, D.M. Hatters, K.H. Weisgraber, J.C. Voss, and J.C. Rutledge VLDL lipolysis products increase VLDL fluidity and convert apolipoprotein E4 into a more expanded conformation J. Lipid Res. 51 6 2010 1273 1283
15. M.N. Oda, T.M. Forte, R.O. Ryan, and J.C. Voss The C-terminal domain of apolipoprotein A-I contains a lipid-sensitive conformational trigger Nat. Struct. Mol. Biol. 10 6 2003 455 460 (Pubitemid 36637643)
16. M. Renault, A. Cukkemane, and M. Baldus Solid-state NMR spectroscopy on complex biomolecules Angew. Chem. Int. Ed. 49 45 2010 8346 8357
17. M.A. Hemminga, and L.J. Berliner ESR Spectroscopy in Membrane Biophysics 2007 Springer
18. M.A. Hemminga Interpretation of ESR and saturation transfer ESR spectra of spin labeled lipids and membranes Chem. Phys. Lipids 32 1983 323 383
19. T.C. Squier, and D.D. Thomas Selective detection of the rotational dynamics of the protein-associated lipid hydrocarbon chains in sarcoplasmic reticulum membranes Biophys. J. 56 1989 735 748 (Pubitemid 19242209)
20. N. Atherton Electron Spin Resonance: A Review of Recent Literature to 1993 1994 Royal Society of Chemistry
21. G. Jeschke DEER distance measurements on proteins Annu. Rev. Phys. Chem. 63 2012 419 446
22. C. Altenbach, K.-J. Oh, R.J. Trabanino, K. Hideg, and W.L. Hubbell Estimation of inter-residue distances in spin labeled proteins at physiological temperatures: experimental strategies and practical limitations Biochemistry 40 2001 15471 15482 (Pubitemid 34015174)
23. W.L. Hubbell, and C. Altenbach Investigation of structure and dynamics in membrane proteins using site-directed spin labeling Curr. Opin. Struct. Biol. 4 1994 566 573 (Pubitemid 24268990)
24. M.L. Mangels, T.B. Cardon, A.C. Harper, K.P. Howard, and G.A. Lorigan Spectroscopic characterization of spin-labeled magnetically oriented phospholipid bilayers by EPR spectroscopy J. Am. Chem. Soc. 122 29 2000 7052 7058 (Pubitemid 30639880)
25. T.B. Cardon, E.K. Tiburu, A. Padmanabhan, K.P. Howard, and G.A. Lorigan Magnetically aligned phospholipid bilayers at the parallel and perpendicular orientations for X-band spin-label EPR studies J. Am. Chem. Soc. 123 12 2001 2913 2914 (Pubitemid 32910730)
26. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, and J. Hermans Interaction models for water in relation to protein hydration Intermolecular Forces 1981 Reidel, Dordrecht The Netherlands 331 342
27. F. Neese ORCA an Ab Initio, Density Functional and Semiempirical Program Package version 2.9 2012 University of Bonn
28. P.A.M. Dirac Note on exchange phenomena in the Thomas atom Proc. Camb. Phil. Soc. 26 1930 376 385
29. J.C. Slater The quantum theory of atoms molecules and solids vol. 4 1974 McGraw Hill London
30. S.H. Vosko, L. Wilk, and M. Nusair Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis Can. J. Phys. 58 1980 1200 1211
31. R.A. Kendall, and H.A. Früchtl The impact of the resolution of the identity approximate integral method on modern ab initio algorithm development Theor. Chem. Acc. 97 1997 158 163
32. J.T. Fermann, and E.F. Valeev Libint: Machine-generated Library for Efficient Evaluation of Molecular Integrals over Gaussians 2003
33. J.S. Binkley, J.A. Pople, and W.J. Hehre Self-consistent molecular orbital methods. 21. Small split-valence basis sets for first-row elements J. Am. Chem. Soc. 102 1980 939 947
34. M.S. Gordon, J.S. Binkley, J.A. Pople, W.J. Pietro, and W.J. Hehre Self-consistent molecular-orbital methods. 22. Small split-valence basis sets for second-row elements J. Am. Chem. Soc. 104 1983 2797 2803
35. K.D. Dobbs, and W.J. Hehre Molecular orbital theory of the properties of inorganic and organometallic compounds 4. Extended basis sets for third- and fourth-row, main-group elements J. Comput. Chem. 7 1986 359 378
36. K.D. Dobbs, and W.J. Hehre Molecular orbital theory of the properties of inorganic and organometallic compounds 5. Extended basis sets for first-row transition metals J. Comput. Chem. 8 1987 861 879
37. K.D. Dobbs, and W.J. Hehre Molecular orbital theory of the properties of inorganic and organometallic compounds. 6. Extended basis sets for second-row transition metals J. Comput. Chem. 8 1987 880 893
38. 2O)n clusters for alkali metals, M = Li, Na, K, Rb, and Cs J. Phys. Chem. 99 1995 3060 3065
39. N. Godbout, D.R. Salahub, J. Andzelm, and E. Wimmer Optimization of Gaussian-type basis sets for local spin density functional calculations. Part I. Boron through neon, optimization technique and validation Can. J. Chem. 70 1992 560 571
40. P.-O. Löwdin On the non-orthogonality problem connected with the use of atomic wave functions in the theory of molecules and crystals J. Chem. Phys. 18 1950 365 375
41. S.-W. Chiu, S.A. Pandit, H.L. Scott, and E. Jakobsson An improved united atom force field for simulation of mixed lipid bilayers J. Phys. Chem. B 113 2009 2748 2763
42. V.S. Oganesyan A general approach for prediction of motional EPR spectra from molecular dynamics (MD) simulations: application to spin labelled protein Phys. Chem. Chem. Phys. 13 2011 4724 4737
43. Z. Guo, D. Cascio, K. Hideg, and W.L. Hubbell Structural determinants of nitroxide motion in spin-labeled proteins: solvent-exposed sites in helix b of t4 lysozyme Protein Sci. 17 2 2008 228 239 10.1110/ps.073174008 (Pubitemid 351171835)
44. M.M. Hatmal, Y. Li, B.G. Hegde, P.B. Hegde, C.C. Jao, R. Langen, and I.S. Haworth Computer modeling of nitroxide spin labels on proteins Biopolymers 97 1 2012 35 44
45. S.A. Pandit, S.-W. Chiu, E. Jakobsson, A. Grama, and H.L. Scott Cholesterol packing around lipids with saturated and unsaturated chains: a simulation study Langmuir 24 2008 6858 6865
46. S.A. Pandit, S.-W. Chiu, E. Jakobsson, A. Grama, and H.L. Scott Cholesterol surrogates: a comparison of cholesterol and 16:0 ceramide in POPC bilayers Biophys. J. 92 2007 920 927 (Pubitemid 46203221)
47. S.A. Pandit, S. Vasudevan, S.W. Chiu, R.J. Mashl, E. Jakobsson, and H.L. Scott Sphingomyelin-cholesterol domains in phospholipid membranes: atomistic simulation Biophys. J. 87 2004 1092 1100 (Pubitemid 39095087)
48. S.W. Chiu, S. Vasudevan, E. Jakobsson, R.J. Mashl, and H.L. Scott Structure of sphingomyelin bilayers: a simulation study Biophys. J. 85 2003 3624 3636
49. J.M. Vanegas, M.L. Longo, and R. Faller Crystalline, ordered and disordered lipid membranes: convergence of stress profiles due to ergosterol J. Am. Chem. Soc. 133 11 2011 3720 3723
50. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
51. U. Essmann, L. Perera, M. Berkowitz, T. Darden, H. Lee, and L. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
52. B. Hess, H. Bekker, H. Berendsen, and J. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472 (Pubitemid 127637344)
53. C. Anézo, A.H. de Vries, H.-D. Höltje, D.P. Tieleman, and S.-J. Marrink Methodological issues in lipid bilayer simulations J. Phys. Chem. B 107 2003 9424 9433
54. O. Berger, O. Edholm, and F. Jähnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013 (Pubitemid 27184429)
55. M. Patra, M. Karttunen, M.T. Hyvönen, E. Falck, P. Lindqvist, and I. Vattulainen Molecular dynamics simulations: major artifacts due to truncation of electrostatic interactions Biophys. J. 84 2003 3636 3645 (Pubitemid 36637862)
56. M. Patra, M. Karttunen, M.T. Hyvönen, E. Falck, and I. Vattulainen Lipid bilayers driven to a wrong plane in molecular dynamics simulations by truncation of long-range electrostatic interactions J. Phys. Chem. B 108 2004 4485 4494
57. W. Humphrey, A. Dalke, and K. Schulten VMD - visual molecular dynamics J. Mol. Graph. 14 1996 33 38
58. S. Nose A molecular dynamics method for simulations in the canonical ensemble Mol. Phys. 52 1984 255 268
59. W.G. Hoover, A.J.C. Ladd, and B. Moran High-strain-rate plastic flow studied via nonequilibrium molecular dynamics Phys. Rev. Lett. 48 1982 1818 1820
60. M. Parrinello, and A. Rahman Polymorphic transitions in single crystals: a new molecular dynamics method J. Appl. Phys. 52 1981 7182 7190 (Pubitemid 12456820)
61. S.E. Feller, R.M. Venable, and R.W. Pastor Computer simulation of a DPPC phospholipid bilayer: structural changes as a function of molecular surface Langmuir 13 1997 6555 6561 (Pubitemid 127592075)
62. J.F. Nagle, R. Zhang, S. Tristram-Nagle, W. Sun, H.I. Petrache, and R.M. Suter X-ray structure determination of fully hydrated L(a) phase dipalmitoylphosphatidylcholine bilayers Biophys. J. 70 1996 1419 1431
63. T. Williams, and C. Kelley Gnuplot 4.4: an interactive plotting program March 2010 (http://gnuplot.sourceforge.net/)
64. E. Kuprusevicius, G. White, and V.S. Oganesyan Prediction of nitroxide spin label EPR spectra from MD trajectories: application to myoglobin Faraday Discuss. 148 2011 283 298
65. G. Williams, and D.C. Watts Non-symmetrical dielectric relaxation behaviour arising from a simple empirical decay function Trans. Faraday Soc. 66 1970 80 85
66. B. Hess Determining the shear viscosity of model liquids from molecular simulation J. Chem. Phys. 116 2002 209 217 (Pubitemid 34061816)
67. W.J. Allen, J.A. Lemkul, and D.R. Bevan GridMAT-MD: a grid-based membrane analysis tool for use with molecular dynamics J. Comput. Chem. 30 2009 1952 1958
68. M. Edidin Rotational and translational diffusion in membranes Annu. Rev. Biophys. Bioeng. 3 1974 179 201
69. A. Filippov, M. Rudakova, and B. Munavirov Lateral diffusion in sphingomyelin bilayers Magn. Reson. Chem. 48 2010 945 950
70. A.K. Smith, and J.H. Freed Dynamics and ordering of lipid spin-labels along the coexistence curve of two membrane phases: an ESR study Chem. Phys. Lipids 165 3 2012 348 361