α-Tocopherol Is Well Designed to Protect Polyunsaturated Phospholipids: MD Simulations

Biophysical Journal

Volumn 109, Issue 8, 2015, Pages 1608-1618

  Leng, Xiaoling ^a   Kinnun, Jacob J ^a   Marquardt, Drew ^b,c   Ghefli, Mikel ^b   Kučerka, Norbert ^d,e   Katsaras, John ^f,g,h   Atkinson, Jeffrey ^b   Harroun, Thad A ^b   Feller, Scott E ⁱ   Wassall, Stephen R ^a  

^a INDIANA UNIVERSITY   (United States)

^b BROCK UNIVERSITY   (Canada)

^c UNIVERSITY OF GRAZ   (Austria)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e Physics and Informatics   (Slovakia)

^f OAK RIDGE NATIONAL LABORATORY   (United States)

^g Joint Institute for Neutron Sciences   (United States)

^h UNIVERSITY OF TENNESSEE   (United States)

ⁱ WABASH COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; LIPID BILAYER; PHOSPHOLIPID;

CHEMISTRY; LIPID BILAYER; LIPID PEROXIDATION; MOLECULAR DYNAMICS; NEUTRON DIFFRACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION REDUCTION REACTION; VALIDATION STUDY;

ALPHA-TOCOPHEROL; LIPID BILAYERS; LIPID PEROXIDATION; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; NEUTRON DIFFRACTION; OXIDATION-REDUCTION; PHOSPHOLIPIDS;

EID: 84944769251     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.08.032     Document Type: Article

References (81)

1. J.M. Zingg Vitamin E: an overview of major research directions Mol. Aspects Med. 28 2007 400 422
2. E. Niki, and M.G. Traber A history of vitamin E Ann. Nutr. Metab. 61 2012 207 212
3. L. Ulatowski, and D. Manor Vitamin E trafficking in neurologic health and disease Ann. Rev. Nutr. 33 2013 87 103
4. L. Packer Vitamin E is nature's master antioxidant Sci. Am. Sci. Med. 1 1994 54 63
5. X. Wang, and P.J. Quinn Vitamin E and its function in membranes Prog. Lipid Res. 38 1999 309 336
6. M.G. Traber, and J. Atkinson Vitamin E, antioxidant and nothing more Free Radic. Biol. Med. 43 2007 4 15
7. G.W. Burton, and K.U. Ingold Vitamin E: application of the principles of physical organic chemistry to the exploration of its structure and function Acc. Chem. Res. 19 1986 194 201
8. M. Alessi, and T. Paul K.U. Ingold The contrasting kinetics of peroxidation of vitamin E-containing phospholipid unilamellar vesicles and human low-density lipoprotein J. Am. Chem. Soc. 124 2002 6957 6965
9. A.T. Diplock, and J.A. Lucy The biochemical modes of action of vitamin E and selenium: a hypothesis FEBS Lett. 29 1973 205 210
10. V.E. Kagan Tocopherol stabilizes membrane against phospholipase A, free fatty acids, and lysophospholipids Ann. N. Y. Acad. Sci. 570 1989 121 135
11. J. Atkinson, and T. Harroun J. Katsaras The location and behavior of α-tocopherol in membranes Mol. Nutr. Food Res. 54 2010 641 651
12. D. Marquardt, and J.A. Williams T.A. Harroun Tocopherol activity correlates with its location in a membrane: a new perspective on the antioxidant vitamin E J. Am. Chem. Soc. 135 2013 7523 7533
13. D. Marquardt, and N. Kučerka T.A. Harroun α-Tocopherol's location in membranes is not affected by their composition Langmuir 31 2015 4464 4472
14. W. Stillwell, and S.R. Wassall Docosahexaenoic acid: membrane properties of a unique fatty acid Chem. Phys. Lipids 126 2003 1 27
15. N. Salem Jr., H.-Y. Kim, and J.A. Yergey Docosahexaenoic acid: membrane function and metabolism A.P. Simopoulos, R.R. Kifer, R.E. Martin, Health Effects of Polyunsaturated Fatty Acids in Seafoods 1986 Academic Press New York 263 317
16. S.R. Wassall, and W. Stillwell Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes Biochim. Biophys. Acta 1788 2009 24 32
17. S.R. Shaikh Biophysical and biochemical mechanisms by which dietary N-3 polyunsaturated fatty acids from fish oil disrupt membrane lipid rafts J. Nutr. Biochem. 23 2012 101 105
18. N. Salem Jr., and B. Litman K. Gawrisch Mechanisms of action of docosahexaenoic acid in the nervous system Lipids 36 2001 945 959
19. S.-L. Niu, and D.C. Mitchell B.J. Litman Reduced G protein-coupled signaling efficiency in retinal rod outer segments in response to n-3 fatty acid deficiency J. Biol. Chem. 279 2004 31098 31104
20. M.F. Brown Modulation of rhodopsin function by properties of the membrane bilayer Chem. Phys. Lipids 73 1994 159 180
21. K. Gawrisch, O. Soubias, and M. Mihailescu Insights from biophysical studies on the role of polyunsaturated fatty acids for function of G-protein coupled membrane receptors Prostaglandins Leukot. Essent. Fatty Acids 79 2008 131 134
22. S.R. Shaikh, and J.J. Kinnun S.R. Wassall How polyunsaturated fatty acids modify molecular organization in membranes: insight from NMR studies of model systems Biochim. Biophys. Acta 1848 2015 211 219
23. S.E. Feller Acyl chain conformations in phospholipid bilayers: a comparative study of docosahexaenoic acid and saturated fatty acids Chem. Phys. Lipids 153 2008 76 80
24. K.U. Ingold, and V.W. Bowry C. Walling Autoxidation of lipids and antioxidation by α-tocopherol and ubiquinol in homogeneous solution and in aqueous dispersions of lipids: unrecognized consequences of lipid particle size as exemplified by oxidation of human low density lipoprotein Proc. Natl. Acad. Sci. USA 90 1993 45 49
25. J. Atkinson, R.F. Epand, and R.M. Epand Tocopherols and tocotrienols in membranes: a critical review Free Radic. Biol. Med. 44 2008 739 764
26. L. Saiz, and M.L. Klein Structural properties of a highly polyunsaturated lipid bilayer from molecular dynamics simulations Biophys. J. 81 2001 204 216
27. S.E. Feller, K. Gawrisch, and A.D. MacKerell Jr. Polyunsaturated fatty acids in lipid bilayers: intrinsic and environmental contributions to their unique physical properties J. Am. Chem. Soc. 124 2002 318 326
28. 2H NMR and molecular dynamics simulations J. Am. Chem. Soc. 124 2002 298 309
29. S. Jo, and T. Kim W. Im CHARMM-GUI: a web-based graphical user interface for CHARMM J. Comput. Chem. 29 2008 1859 1865
30. S. Jo, and J.B. Lim W. Im CHARMM-GUI MEMBRANE BUILDER for mixed bilayers and its application to yeast membranes Biophys. J. 97 2009 50 58
31. 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
32. J.B. Klauda, and V. Monje W. Im Improving the CHARMM force field for polyunsaturated fatty acid chains J. Phys. Chem. B 116 2012 9424 9431
33. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an n-log(n) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
34. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
35. S. Nosé, and M.L. Klein A study of solid and liquid carbon tetrafluoride using the constant pressure molecular dynamics technique J. Chem. Phys. 72 1983 6928 6939
36. T.D. Romo, and A. Grossfield LOOS: an extensible platform for the structural analysis of simulations Proceedings of the 31st International IEEE EMBS Conference 2009 Institute of Electrical and Electronics Engineers Piscataway, NJ 332 2335
37. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28
38. D. Marquardt, and J.A. Williams T.A. Harroun Dimyristoyl phosphatidylcholine: a remarkable exception to α-tocopherol's membrane presence J. Am. Chem. Soc. 136 2014 203 210
39. M.R. Brzustowicz, and V. Cherezov S.R. Wassall Molecular organization of cholesterol in polyunsaturated membranes: microdomain formation Biophys. J. 82 2002 285 298
40. J.A. Williams, and S.E. Batten S.R. Wassall Docosahexaenoic and eicosapentaenoic acids segregate differently between raft and nonraft domains Biophys. J. 103 2012 228 237
41. J.H. Davis, and K.R. Jeffrey T.P. Higgs Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains Chem. Phys. Lett. 42 1976 390 394
42. 2H-NMR Biochim. Biophys. Acta 737 1983 117 171
43. M.A. McCabe, and S.R. Wassall Rapid deconvolution of NMR powder spectra by weighted fast Fourier transformation Solid State Nucl. Magn. Reson. 10 1997 53 61
44. 2H-nuclear magnetic resonance Biophys. J. 56 1989 1037 1041
45. J. Seelig Deuterium magnetic resonance: theory and application to lipid membranes Q. Rev. Biophys. 10 1977 353 418
46. L.L. Holte, F. Separovic, and K. Gawrisch Nuclear magnetic resonance investigation of hydrocarbon chain packing in bilayers of polyunsaturated phospholipids Lipids 31 Suppl 1996 S199 S203
47. 2H NMR experiments Eur. Biophys. J. 36 2007 919 931
48. 2H NMR shows equivalence of dehydration and osmotic pressures in lipid membrane deformation Biophys. J. 100 2011 98 107
49. M.M. Koerner, and L.A. Palacio H.I. Petrache Electrodynamics of lipid membrane interactions in the presence of zwitterionic buffers Biophys. J. 101 2011 362 369
50. M. Bloom, J.H. Davis, and M.I. Valic Spectral distortion effects due to finite pulse widths in deuterium nuclear magnetic resonance spectroscopy Can. J. Phys. 58 1980 1510 1517
51. 2H NMR spectra of magnetically partially oriented lipid bilayers Biophys. J. 74 1998 1007 1014
52. S.R. Wassall, and J.L. Thewalt R.J. Cushley Deuterium NMR study of the interaction of α-tocopherol with a phospholipid model membrane Biochemistry 25 1986 319 326
53. Y.J. Suzuki, and M. Tsuchiya L. Packer Structural and dynamic membrane properties of α-tocopherol and α-tocotrienol: implication to the molecular mechanism of their antioxidant potency Biochemistry 32 1993 10692 10699
54. I.V. Polozov, and K. Gawrisch NMR detection of lipid domains Methods Mol. Biol. 398 2007 107 126
55. M. Mihailescu, and O. Soubias K. Gawrisch Structure and dynamics of cholesterol-containing polyunsaturated lipid membranes studied by neutron diffraction and NMR J. Membr. Biol. 239 2011 63 71
56. K. Gawrisch, and O. Soubias Structure and dynamics of polyunsaturated hydrocarbon chains in lipid bilayers - significance for GPCR function Chem. Phys. Lipids 153 2008 64 75
57. J. Seelig, and N. Waespe-Sarcevic Molecular order in cis and trans unsaturated phospholipid bilayers Biochemistry 17 1978 3310 3315
58. 2H NMR and MD simulations of positional isomers of a monounsaturated phospholipid membrane: structural implications of double bond location J. Phys. Chem. B 114 2010 11474 11483
59. S.P. Soni, and J.A. Ward S.R. Wassall Effect of trans unsaturation on molecular organization in a phospholipid membrane Biochemistry 48 2009 11097 11107
60. A.K. Engel, and D. Cowburn The origin of multiple quadrupole couplings in the deuterium NMR spectra of the 2 chain of 1,2 dipalmitoyl-sn-glycero-3-phosphorylcholine FEBS Lett. 126 1981 169 171
61. T.A. Harroun, J. Katsaras, and S.R. Wassall Cholesterol hydroxyl group is found to reside in the center of a polyunsaturated lipid membrane Biochemistry 45 2006 1227 1233
62. S.-S. Qin, and Z.-W. Yu Molecular dynamics simulations of α-tocopherol in model membranes Wuli Huaxue Xuebao 27 2011 213 227
63. K. Fukuzawa, and W. Ikebata S. Urano Location of α-tocopherol in phospholipid vesicles and its dynamics in inhibiting lipid peroxidation M. Mino, H. Nakamura, A.T. Diplock, H.J. Kayden, Vitamin E: Its Usefulness in Health and in Curing Diseases 1993 Japan Scientific Societies Press Tokyo, Japan 31 40
64. R.H. Bisby, and S. Ahmed Transverse distribution of α-tocopherol in bilayer membranes studied by fluorescence quenching Free Radic. Biol. Med. 6 1989 231 239
65. J.C. Gomez-Fernandez, and J. Villalain M.J. Prieto Localization of α-tocopherol in membranes Ann. N. Y. Acad. Sci. 570 1989 109 120
66. 19F NMR and fluorescence polarization techniques Arch. Biochem. Biophys. 303 1993 10 14
67. M. Afri, and B. Ehrenberg A.A. Frimer Active oxygen chemistry within the liposomal bilayer. Part III: locating vitamin E, ubiquinol and ubiquinone and their derivatives in the lipid bilayer Chem. Phys. Lipids 131 2004 107 121
68. 13C-NMR spectroscopy Biochim. Biophys. Acta 819 1985 131 135
69. S.-S. Qin, Z.-W. Yu, and Y.-X. Yu Structural and kinetic properties of α-tocopherol in phospholipid bilayers, a molecular dynamics simulation study J. Phys. Chem. B 113 2009 16537 16546
70. O. Soubias, and K. Gawrisch Docosahexaenoyl chains isomerize on the sub-nanosecond time scale J. Am. Chem. Soc. 129 2007 6678 6679
71. M. Mihailescu, and K. Gawrisch The structure of polyunsaturated lipid bilayers important for rhodopsin function: a neutron diffraction study Biophys. J. 90 2006 L4 L6
72. F.-X. Contreras, and L. Sánchez-Magraner F.M. Goñi Transbilayer (flip-flop) lipid motion and lipid scrambling in membranes FEBS Lett. 584 2010 1779 1786
73. R. Homan, and H.J. Pownall Transbilayer diffusion of phospholipids: dependence on headgroup structure and acyl chain length Biochim. Biophys. Acta 938 1988 155 166
74. V.T. Armstrong, and M.R. Brzustowicz W. Stillwell Rapid flip-flop in polyunsaturated (docosahexaenoate) phospholipid membranes Arch. Biochem. Biophys. 414 2003 74 82
75. F. Bellemare, and M. Fragata Transmembrane distribution of α-tocopherol in single-lamellar mixed lipid vesicles J. Membr. Biol. 58 1981 67 74
76. V.A. Tyurin, and V.E. Kagan T.S. Stoichev Interaction of α-tocopherol with phospholipid liposomes: absence of transbilayer mobility Bull. Exp. Biol. Med. 102 1986 1677 1680
77. J.A. Hamilton Fast flip-flop of cholesterol and fatty acids in membranes: implications for membrane transport proteins Curr. Opin. Lipidol. 14 2003 263 271
78. E. Niki Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence Free Radic. Biol. Med. 66 2014 3 12
79. K.M. Lebold, and M.G. Traber Interactions between α-tocopherol, polyunsaturated fatty acids, and lipoxygenases during embryogenesis Free Radic. Biol. Med. 66 2014 13 19
80. N.V. Eldho, and S.E. Feller K. Gawrisch Polyunsaturated docosahexaenoic vs docosapentaenoic acid-differences in lipid matrix properties from the loss of one double bond J. Am. Chem. Soc. 125 2003 6409 6421
81. J. Garrec, and A. Monari M. Tarek Lipid peroxidation in membranes: the peroxyl radical does not "float" J. Phys. Chem. Lett. 5 2014 1653 1658