Membrane simulations mimicking acidic pH reveal increased thickness and negative curvature in a bilayer consisting of lysophosphatidylcholines and free fatty acids

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 5, 2010, Pages 938-946

  Lähdesmäki, Katariina ^a   Ollila, O H Samuli ^b   Koivuniemi, Artturi ^b   Kovanen, Petri T ^a   Hyvönen, Marja T ^a,c  

^a WIHURI RESEARCH INSTITUTE   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c UNIVERSITY OF OULU   (Finland)

Author keywords

Lateral pressure profile; MD simulation; pH; Phospholipase A2; Phospholipid; Spontaneous curvature

Indexed keywords

FATTY ACID; LYSOPHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A2;

ACIDITY; ARTICLE; LIPID BILAYER; LIPID COMPOSITION; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR MODEL; PH; PRIORITY JOURNAL; PROTON TRANSPORT; SURFACE PROPERTY;

CELL MEMBRANE; FATTY ACIDS, NONESTERIFIED; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; LYSOPHOSPHATIDYLCHOLINES; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE;

EID: 77649271967     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.01.020     Document Type: Article

References (94)

1. Dowhan W., and Bogdanov M. Functional roles of lipids in membranes. In: Vance D.E., and Vance J.E. (Eds). New Comprehensive Biochemistry, vol. 36, Biochemistry of Lipids, Lipoproteins and Membranes (2002), Elsevier Science B.V, Amsterdam 1-35
2. Burger K.N. Greasing membrane fusion and fission machineries. Traffic 1 (2000) 605-613
3. Phillips R., Ursell T., Wiggins P., and Sens P. Emerging roles for lipids in shaping membrane-protein function. Nature 459 (2009) 379-385
4. Chernomordik L.V., and Kozlov M.M. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15 (2008) 675-683
5. Chernomordik L.V., and Kozlov M.M. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72 (2003) 175-207
6. Kooijman E.E., Chupin V., Fuller N.L., Kozlov M.M., de K.B., Burger K.N., and Rand P.R. Spontaneous curvature of phosphatidic acid and lysophosphatidic acid. Biochemistry 44 (2005) 2097-2102
7. Kooijman E.E., Chupin V., de K.B., and Burger K.N. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4 (2003) 162-174
8. Verkleij A.J., De M.R., Leunissen-Bijvelt J., and de K.B. Divalent cations and chlorpromazine can induce non-bilayer structures in phosphatidic acid-containing model membranes. Biochim. Biophys. Acta 684 (1982) 255-262
9. 2H NMR study. Biochem. Biophys. Res. Commun. 111 (1983) 675-682
10. McMahon H.T., and Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438 (2005) 590-596
11. Kinnunen P.K., and Holopainen J.M. Mechanisms of initiation of membrane fusion: role of lipids. Biosci. Rep. 20 (2000) 465-482
12. Zellmer S., Cevc G., and Risse P. Temperature- and pH-controlled fusion between complex lipid membranes. Examples with the diacylphosphatidylcholine/fatty acid mixed liposomes. Biochim. Biophys. Acta 1196 (1994) 101-113
13. Knecht V., and Marrink S.J. Molecular dynamics simulations of lipid vesicle fusion in atomic detail. Biophys. J. 92 (2007) 4254-4261
14. 2 biochemistry. Cardiovasc. Drugs Ther. 23 (2009) 49-59
15. 2. J. Biochem. 131 (2002) 285-292
16. 2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4 (2003) 214-221
17. 2-paradigm. Chem. Rev. 101 (2001) 2613-2654
18. 2 activity is required for Golgi complex and trans Golgi network membrane tubulation. Proc. Natl Acad. Sci. USA 95 (1998) 8642-8647
19. 2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 310 (2005) 1678-1680
20. 2. J. Biol Chem 284 (2009) 5697-5708
21. Boström P., Rutberg M., Ericsson J., Holmdahl P., Andersson L., Frohman M.A., Borén J., and Olofsson S.O. Cytosolic lipid droplets increase in size by microtubule-dependent complex formation. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1945-1951
22. 2 at cytoplasmic arachidonate-rich lipid bodies. Am. J. Pathol. 152 (1998) 759-769
23. 2 alpha fluorescent proteins. Biochim. Biophys. Acta 1783 (2008) 1544-1550
24. 2-modified LDL particles retain the generated hydrolytic products and are more atherogenic at acidic pH. Atherosclerosis 207 (2009) 352-359
25. 2 with ceramide transacylase activity. Glycoconj. J. 20 (2004) 25-32
26. Naghavi M., John R., Naguib S., Siadaty M.S., Grasu R., Kurian K.C., van Winkle W.B., Soller B., Litovsky S., Madjid M., Willerson J.T., and Casscells W. pH Heterogeneity of human and rabbit atherosclerotic plaques; a new insight into detection of vulnerable plaque. Atherosclerosis 164 (2002) 27-35
27. Kimura-Matsumoto M., Ishikawa Y., Komiyama K., Tsuruta T., Murakami M., Masuda S., Akasaka Y., Ito K., Ishiguro S., Morita H., Sato S., and Ishii T. Expression of secretory phospholipase A2s in human atherosclerosis development. Atherosclerosis 196 (2008) 81-91
28. 2 in vascular disease. Circ. Res. 89 (2001) 298-304
29. Berendsen H.J.C., van der Spoel D., and van Drunen R. Gromacs: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91 (1995) 43-56
30. Lindahl E., Hess B., and van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Mod. 7 (2001) 306-317
31. Tieleman D.P., and Berendsen H.J.C. Molecular dynamics simulations of a fully hydrated dipalmitoylphosphatidylcholine bilayer with different macroscopic boundary conditions and parameters. J. Chem. Phys. 105 (1996) 4871
32. Berger O., Edholm O., and Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72 (1997) 2002-2013
33. Chiu S.W., Clark M., Balaji V., Subramaniam S., Scott H.L., and Jakobsson E. Incorporation of surface tension into molecular dynamics simulation of an interface: a fluid phase lipid bilayer membrane. Biophys. J. 69 (1995) 1230-1245
34. W.F. van Gunsteren, P. Krüger, S.R. Billeter, A.E. Mark, A.A. Eising, W.R.P. Scott, Hüneberg P.H., and I.G. Tironi, Biomolecular Simulation: the GROMOS96 Manual and User Guide. Biomos, Groningen and Hochsuchulverlag AG, Germany and Er ETH Zürich, Zurich, Switzerland., 1996.
35. Tieleman D.P., and Berendsen H.J. A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer. Biophys. J. 74 (1998) 2786-2801
36. Ollila S., Hyvönen M.T., and Vattulainen I. Polyunsaturation in lipid membranes: dynamic properties and lateral pressure profiles. J. Phys. Chem B 111 (2007) 3139-3150
37. Small D.M., Cabral D.J., Cistola D.P., Parks J.S., and Hamilton J.A. The ionization behavior of fatty acids and bile acids in micelles and membranes. Hepatology 4 (1984) 77S-79S
38. Hess B., Bekker H., Berendsen H.J.C., and Fraaije J.G.E.M. LINCS: a Linear Constraint Solver for molecular simulations. J. Comp. Chem. 18 (1997) 1463-1472
39. Miyamoto S., and Kollman P.A. Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comp. Chem. 13 (1992) 952-962
40. Essman U., Perela L., Berkowitz M.L., Darden T., Lee H., and Pedersen L.G. A smooth particle mesh Ewald method. J. Chem. Phys. 103 (1995) 8577-8592
41. Patra M., Karttunen M., Hyvönen M.T., Falck E., Lindqvist P., and Vattulainen I. Molecular dynamics simulations of lipid bilayers: major artifacts due to truncating electrostatic interactions. Biophys. J. 84 (2003) 3636-3645
42. Rog T., Murzyn K., and Pasenkiewicz-Gierula M. Molecular dynamics simulations of charged and neutral lipid bilayers: treatment of electrostatic interactions. Acta Biochim. Pol. 50 (2003) 789-798
43. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., DiNola A., and Haak J.R. Molecular dynamics with coupling to an axternal bath. J. Chem. Phys. 81 (1984) 3684-3690
44. Nosé S. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52 (1984) 255-268
45. Hoover W.G. Canonical dynamics: equilibrium phase-space distributions. Physical Review A 31 (1985) 1695-1697
46. Parrinello M., and Rahman A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52 (1981) 7182-7190
47. Nosé S., and Klein M.L. Constant pressure molecular dynamics for molecular systems. Mol. Phys. 50 (1983) 1055-1076
48. Ollila O.H.S., Rog T., Karttunen M., and Vattulainen I. Role of sterol type on lateral pressure profiles of lipid membranes affecting membrane protein functionality: comparison between cholesterol, desmosterol, 7-dehydrocholesterol and ketosterol. J. Struct. Biol 159 (2007) 311-323
49. Niemelä P.S., Ollila S., Hyvönen M.T., Karttunen M., and Vattulainen I. Assessing the nature of lipid raft membranes. PLoS. Comput. Biol 3 (2007) e34
50. Terämä E., Ollila O.H., Salonen E., Rowat A.C., Trandum C., Westh P., Patra M., Karttunen M., and Vattulainen I. Influence of ethanol on lipid membranes: from lateral pressure profiles to dynamics and partitioning. J. Phys. Chem B 112 (2008) 4131-4139
51. O.H.S. Ollila and I. Vattulainen, Lateral pressure profiles in lipid membranes: dependence on molecular composition, in: Phillip Biggin, Mark Sansom (Eds.), Molecular Simulations and Biomembranes: From Biophysics to Function, Royal Society of Chemistry (in press).
52. J.H. Irving, J.G. Kirkwood, The Statistical Mechanical Theory of Transport Processes. IV. The Equations of Hydrodynamics, J. Chem. Phys. 18 (1950) 817.
53. Kucerka N., Tristram-Nagle S., and Nagle J.F. Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J. Membr. Biol 208 (2005) 193-202
54. Niemelä P., Hyvönen M.T., and Vattulainen I. Structure and dynamics of sphingomyelin bilayer: insight gained through systematic comparison to phosphatidylcholine. Biophys. J. 87 (2004) 2976-2989
55. Maulik P.R., and Shipley G.G. X-ray diffraction and calorimetric study of N-lignoceryl sphingomyelin membranes. Biophys. J. 69 (1995) 1909-1916
56. Khalifat N., Puff N., Bonneau S., Fournier J.B., and Angelova M.I. Membrane deformation under local pH gradient: mimicking mitochondrial cristae dynamics. Biophys. J. 95 (2008) 4924-4933
57. Safran S.A. Statistical Thermodynamics of Surfaces, Interfaces, and Membranes (1994), Addison-Wesley, Reading, MA
58. Lyklema J. Fundamentals of Interface and Colloid Science, vol. III: Liquid-fluid interfaces (2000), Academic press, London, UK
59. Niemelä P.S., Hyvönen M.T., and Vattulainen I. Influence of chain length and unsaturation on sphingomyelin bilayers. Biophys. J. 90 (2006) 851-863
60. Rowlinson J.S., and Widom B. Molecular Theory of Capillarity (1982), Clarendon press, Oxford
61. Marsh D. Lateral pressure in membranes. Biochim. Biophys. Acta 1286 (1996) 183-223
62. Israelachvili J.N. Intermolecular and Surface Forces (1985), Academic Press, London
63. Robert S. Cantor, lateral pressures in cell membranes: a mechanism for modulation of protein function. The Journal of Physical Chemistry B 101 (1997) 1723-1725
64. Brown M.F. Modulation of rhodopsin function by properties of the membrane bilayer. Chem. Phys. Lipids 73 (1994) 159-180
65. Marrink S.J., Risselada H.J., Yefimov S., Tieleman D.P., and de Vries A.H. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem B 111 (2007) 7812-7824
66. Orsi M., Haubertin D.Y., Sanderson W.E., and Essex J.W. A quantitative coarse-grain model for lipid bilayers. J. Phys. Chem B 112 (2008) 802-815
67. Templer R.H., Khoo B.J., and Seddon J.M. Gaussian curvature modulus of an amphiphilic monolayer. Langmuir 14 (2009) 7427-7434
68. Lindahl E., and Edholm O. Mesoscopic undulations and thickness fluctuations in lipid bilayers from molecular dynamics simulations. Biophys. J. 79 (2000) 426-433
69. May E.R., Kopelevich D.I., and Narang A. Coarse-grained molecular dynamics simulations of phase transitions in mixed lipid systems containing LPA, DOPA, and DOPE lipids. Biophys. J. 94 (2008) 878-890
70. Siegel D.P. The Gaussian curvature elastic energy of intermediates in membrane fusion. Biophys. J. 95 (2008) 5200-5215
71. Pentikäinen M.O., Hyvönen M.T., Öörni K., Hevonoja T., Korhonen A., Lehtonen-Smeds E.M., Ala-Korpela M., and Kovanen P.T. Altered phospholipid-apoB-100 interactions and generation of extra membrane material in proteolysis-induced fusion of LDL particles. J. Lipid Res. 42 (2001) 916-922
72. Blokhuis E.M., and Sager W.F.C. Vesicle adhesion and microemulsion droplet dimerization: small bending rigidity regime. J. Chem. Phys. 111 (1999) 7062
73. Petsev D.N. Structure and film formation in charged emulsions and microemulsions. Physica A 250 (1998) 115-132
74. Kabalnov A., and Wennerström H. Macroemulsion Stability. The Oriented Wedge Theory Revisited (1996) 276-292
75. Ichikawa S., and Walde P. Phospholipase D-mediated aggregation, fusion, and precipitation of phospholipid vesicles. Langmuir 20 (2004) 941-949
76. Sundler R., Duzgunes N., and Papahadjopoulos D. Control of membrane fusion by phospholipid head groups. II. The role of phosphatidylethanolamine in mixtures with phosphatidate and phosphatidylinositol. Biochim. Biophys. Acta 649 (1981) 751-758
77. Park J.B. Interaction of phospholipase D to vesicles induces membrane fusion. Experimental and Molecular Medicine 28 (1996) 141
78. Churchward M.A., Rogasevskaia T., Brandman D.M., Khosravani H., Nava P., Atkinson J.K., and Coorssen J.R. Specific lipids supply critical negative spontaneous curvature-an essential component of native Ca2+-triggered membrane fusion. Biophys. J. 94 (2008) 3976-3986
79. Park J.B., Lee T.H., and Kim H. Fusion of phospholipid vesicles induced by phospholipase D in the presence of calcium ion. Biochem. Int. 27 (1992) 417-422
80. Swietach P., Vaughan-Jones R.D., and Harris A.L. Regulation of tumor pH and the role of carbonic anhydrase 9. Cancer Metastasis Rev. 26 (2007) 299-310
81. 2 enzymes in atherogenesis. Curr. Opin. Lipidol. 16 (2005) 341-344
82. Boström M.A., Boyanovsky B.B., Jordan C.T., Wadsworth M.P., Taatjes D.J., de Beer F.C., and Webb N.R. Group V Secretory Phospholipase A2 Promotes Atherosclerosis. Evidence From Genetically Altered Mice. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 600-606
83. 2 enzymes contributes to the initiation and progression of atherosclerosis. Curr. Opin. Lipidol. 20 (2009) 421-427
84. Humphrey W., Dalke A., and Schulten K. VMD-Visual Molecular Dynamics. J. Molec. Graphics 14 (1996) 33-38
85. Andersen O.S., and Koeppe R.E. Bilayer thickness and membrane protein function: an energetic perspective. Annu. Rev. Biophys. Biomol. Struct. 36 (2007) 107-130
86. Lundbaek J.A., and Andersen O.S. Spring constants for channel-induced lipid bilayer deformations. Estimates using gramicidin channels. Biophys. J. 76 (1999) 889-895
87. Böckmann R.A., Hac A., Heimburg T., and Grubmüller H. Effect of sodium chloride on a lipid bilayer. Biophys. J. 85 (2003) 1647-1655
88. Cantor R.S. Lipid composition and the lateral pressure profile in bilayers. Biophys. J. 76 (1999) 2625-2639
89. Tauchi-Sato K., Ozeki S., Houjou T., Taguchi R., and Fujimoto T. The surface of lipid droplets is a phospholipid monolayer with a unique Fatty Acid composition. J. Biol. Chem. 277 (2002) 44507-44512
90. Prassl R., and Laggner P. Molecular structure of low density lipoprotein: current status and future challenges. Eur. Biophys. J. 38 (2009) 145-158
91. Koivuniemi A., Heikelä M., Kovanen P.T., Vattulainen I., and Hyvönen M.T. Atomistic simulations of phosphatidylcholines and cholesteryl esters in high-density lipoprotein-sized lipid droplet and trilayer: clues to cholesteryl ester transport and storage. Biophys. J. 96 (2009) 4099-4108
92. Goodman J.M. The gregarious lipid droplet. J. Biol Chem 283 (2008) 28005-28009
93. Olofsson S.O., Boström P., Andersson L., Rutberg M., Perman J., and Borén J. Lipid droplets as dynamic organelles connecting storage and efflux of lipids. Biochim. Biophys. Acta 1791 (2009) 448-458
94. Öörni K., Pentikäinen M.O., Ala-Korpela M., and Kovanen P.T. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J. Lipid Res. 41 (2000) 1703-1714