Hexagonal Substructure and Hydrogen Bonding in Liquid-Ordered Phases Containing Palmitoyl Sphingomyelin

Biophysical Journal

Volumn 109, Issue 5, 2015, Pages 948-955

  Sodt, Alexander J ^a   Pastor, Richard W ^a   Lyman, Edward ^b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; CHOLESTEROL; PALMITOYLSPHINGOMYELIN; SPHINGOMYELIN;

CHEMISTRY; CONFORMATION; HYDROGEN BOND; METABOLISM; MOLECULAR MODEL;

AMIDES; CHOLESTEROL; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; SPHINGOMYELINS;

EID: 84940688642     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.07.036     Document Type: Article

References (59)

1. E. Oldfield, and D. Chapman Dynamics of lipids in membranes: heterogeneity and the role of cholesterol FEBS Lett. 23 1972 285 297
2. M.K. Jain, and H.B. White III Long-range order in biomembranes P. Rodolfo, K. David, Advances in Lipid Research 1977 Elsevier Amsterdam
3. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
4. C. Eggeling, and C. Ringemann S.W. Hell Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 2009 1159 1162
5. A. Honigmann, and V. Mueller C. Eggeling Scanning STED-FCS reveals spatiotemporal heterogeneity of lipid interaction in the plasma membrane of living cells Nat. Commun. 5 2014 5412
6. A. Honigmann, and S. Sadeghi R. Vink A lipid bound actin meshwork organizes liquid phase separation in model membranes eLife 3 2014 e01671
7. S.A. Sanchez, M.A. Tricerri, and E. Gratton Laurdan generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo Proc. Natl. Acad. Sci. USA 109 2012 7314 7319
8. E. Sezgin, and T. Gutmann P. Schwille Adaptive lipid packing and bioactivity in membrane domains PLoS One 10 2015 e0123930
9. G.W. Feigenson Phase boundaries and biological membranes Annu. Rev. Biophys. Biomol. Struct. 36 2007 63 77
10. S.L. Veatch, and S.L. Keller Seeing spots: complex phase behavior in simple membranes Biochim. Biophys. Acta 1746 2005 172 185
11. I. Levental, M. Grzybek, and K. Simons Raft domains of variable properties and compositions in plasma membrane vesicles Proc. Natl. Acad. Sci. USA 108 2011 11411 11416
12. M.R. Vist, and J.H. Davis Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry Biochemistry 29 1990 451 464
13. J.H. Ipsen, O.G. Mouritsen, and M.J. Zuckermann Theory of thermal anomalies in the specific heat of lipid bilayers containing cholesterol Biophys. J. 56 1989 661 667
14. J.H. Davis, J.J. Clair, and J. Juhasz Phase equilibria in DOPC/DPPC-d62/cholesterol mixtures Biophys. J. 96 2009 521 539
15. S.L. Veatch, and O. Soubias K. Gawrisch Critical fluctuations in domain-forming lipid mixtures Proc. Natl. Acad. Sci. USA 104 2007 17650 17655
16. T. Bartels, and R.S. Lankalapalli M.F. Brown Raftlike mixtures of sphingomyelin and cholesterol investigated by solid-state 2H NMR spectroscopy J. Am. Chem. Soc. 130 2008 14521 14532
17. A. Bunge, and P. Müller D. Huster Characterization of the ternary mixture of sphingomyelin, POPC, and cholesterol: support for an inhomogeneous lipid distribution at high temperatures Biophys. J. 94 2008 2680 2690
18. F.A. Heberle, and R.S. Petruzielo J. Katsaras Bilayer thickness mismatch controls domain size in model membranes J. Am. Chem. Soc. 135 2013 6853 6859
19. T.T. Mills, and S. Tristram-Nagle G.W. Feigenson Liquid-liquid domains in bilayers detected by wide angle X-ray scattering Biophys. J. 95 2008 682 690
20. J. Zhao, and J. Wu G.W. Feigenson Phase studies of model biomembranes: complex behavior of DSPC/DOPC/cholesterol Biochim. Biophys. Acta 1768 2007 2764 2776
21. S.L. Veatch, and S.L. Keller Miscibility phase diagrams of giant vesicles containing sphingomyelin Phys. Rev. Lett. 94 2005 148101
22. D. Marsh Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams Biochim. Biophys. Acta 1798 2010 688 699
23. D. Marsh Cholesterol-induced fluid membrane domains: a compendium of lipid-raft ternary phase diagrams Biochim. Biophys. Acta 1788 2009 2114 2123
24. F.A. Heberle, and J. Wu G.W. Feigenson Comparison of three ternary lipid bilayer mixtures: FRET and ESR reveal nanodomains Biophys. J. 99 2010 3309 3318
25. R.S. Petruzielo, and F.A. Heberle G.W. Feigenson Phase behavior and domain size in sphingomyelin-containing lipid bilayers Biochim. Biophys. Acta 1828 2013 1302 1313
26. S.L. Veatch, and I.V. Polozov S.L. Keller Liquid domains in vesicles investigated by NMR and fluorescence microscopy Biophys. J. 86 2004 2910 2922
27. M.J. Gerl, and J.L. Sampaio K. Simons Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane J. Cell Biol. 196 2012 213 221
28. R.F.M. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416
29. M.L. Frazier, and J.R. Wright P.F.F. Almeida Investigation of domain formation in sphingomyelin/cholesterol/POPC mixtures by fluorescence resonance energy transfer and Monte Carlo simulations Biophys. J. 92 2007 2422 2433
30. A.J. Sodt, and M.L. Sandar E. Lyman The molecular structure of the liquid-ordered phase of lipid bilayers J. Am. Chem. Soc. 136 2014 725 732
31. S. Baoukina, and E. Mendez-Villuendas D.P. Tieleman Computer simulations of the phase separation in model membranes Faraday Discuss. 161 2013 63 75 discussion 113-150
32. H.J. Risselada, and S.J. Marrink The molecular face of lipid rafts in model membranes Proc. Natl. Acad. Sci. USA 105 2008 17367 17372
33. J. Aittoniemi, and P.S. Niemelä I. Vattulainen Insight into the putative specific interactions between cholesterol, sphingomyelin, and palmitoyl-oleoyl phosphatidylcholine Biophys. J. 92 2007 1125 1137
34. S.A. Pandit, and S. Vasudevan H.L. Scott Sphingomyelin-cholesterol domains in phospholipid membranes: atomistic simulation Biophys. J. 87 2004 1092 1100
35. Z. Zhang, S.Y. Bhide, and M.L. Berkowitz Molecular dynamics simulations of bilayers containing mixtures of sphingomyelin with cholesterol and phosphatidylcholine with cholesterol J. Phys. Chem. B 111 2007 12888 12897
36. R.M. Venable, and A.J. Sodt J.B. Klauda CHARMM all-atom additive force field for sphingomyelin: elucidation of hydrogen bonding and of positive curvature Biophys. J. 107 2014 134 145
37. T. Yasuda, and M. Kinoshita N. Matsumori Detailed comparison of deuterium quadrupole profiles between sphingomyelin and phosphatidylcholine bilayers Biophys. J. 106 2014 631 638
38. D.E. Shaw, and P. Maragakis W. Wriggers Atomic-level characterization of the structural dynamics of proteins Science 330 2010 341 346
39. S. Jo, and T. Kim W. Im CHARMM-GUI: a web-based graphical user interface for CHARMM J. Comput. Chem. 29 2008 1859 1865
40. E.L. Wu, and X. Cheng W. Im CHARMM-GUI Membrane Builder toward realistic biological membrane simulations J. Comput. Chem. 35 2014 1997 2004
41. 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
42. M.C. Pitman, and F. Suits S.E. Feller Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol Biochemistry 43 2004 15318 15328
43. G.J. Martyna, D.J. Tobias, and M.L. Klein Constant pressure molecular dynamics algorithms J. Chem. Phys. 101 1994 4177 4189
44. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985 1695 1697
45. S. Nosé A unified formulation of the constant temperature molecular dynamics methods J. Chem. Phys. 81 1984 511 519
46. Y. Shan, and J.L. Klepeis D.E. Shaw Gaussian split Ewald: a fast Ewald mesh method for molecular simulation J. Chem. Phys. 122 2005 54101
47. M.R. Krause, and S.L. Regen The structural role of cholesterol in cell membranes: from condensed bilayers to lipid rafts Acc. Chem. Res. 47 2014 3512 3521
48. S.M. Krisovitch, and S.L. Regen Nearest-neighbor recognition in phospholipid bilayers. Probing lateral organization at the molecular level J. Am. Chem. Soc. 113 1991 8175 8177
49. P.F.F. Almeida Thermodynamics of lipid interactions in complex bilayers Biochim. Biophys. Acta 1788 2009 72 85
50. A. Radhakrishnan, and H. McConnell Condensed complexes in vesicles containing cholesterol and phospholipids Proc. Natl. Acad. Sci. USA 102 2005 12662 12666
51. A. Radhakrishnan, and H.M. McConnell Condensed complexes of cholesterol and phospholipids Biophys. J. 77 1999 1507 1517
52. I.P. Sugár, and P.L.G. Chong A statistical mechanical model of cholesterol/phospholipid mixtures: linking condensed complexes, superlattices, and the phase diagram J. Am. Chem. Soc. 134 2012 1164 1171
53. C. Wang, M.R. Krause, and S.L. Regen Push and pull forces in lipid raft formation: the push can be as important as the pull J. Am. Chem. Soc. 137 2015 664 666
54. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
55. N. Matsumori, and T. Yamaguchi M. Murata Orientation and order of the amide group of sphingomyelin in bilayers determined by solid-state NMR Biophys. J. 108 2015 2816 2824
56. C.L. Armstrong, and D. Marquardt M.C. Rheinstädter The observation of highly ordered domains in membranes with cholesterol PLoS One 8 2013 e66162
57. M.C. Rheinstädter, and O.G. Mouritsen Small-scale structure in fluid cholesterol-lipid bilayers Curr. Opin. Colloid Interface Sci. 18 2013 440 447
58. L. Toppozini, and S. Meinhardt M.C. Rheinstädter Structure of cholesterol in lipid rafts Phys. Rev. Lett. 113 2014 228101
59. B.B. Diaz-Rohrer, and K.R. Levental I. Levental Membrane raft association is a determinant of plasma membrane localization Proc. Natl. Acad. Sci. USA 111 2014 8500 8505