Monte carlo simulation of protein-induced lipid demixing in a membrane with interactions derived from experiment

Biophysical Journal

Volumn 101, Issue 8, 2011, Pages 1930-1937

  Almeida, Paulo F ^a   Best, Alexis ^a   Hinderliter, Anne ^b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b UNIVERSITY OF MINNESOTA DULUTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANNEXIN; CALCIUM; MEMBRANE LIPID;

ADSORPTION; ARTICLE; CELL MEMBRANE; CHEMISTRY; METABOLISM; MONTE CARLO METHOD; PROTEIN TERTIARY STRUCTURE;

ADSORPTION; ANNEXINS; CALCIUM; CELL MEMBRANE; MEMBRANE LIPIDS; MONTE CARLO METHOD; PROTEIN STRUCTURE, TERTIARY;

EUKARYOTA;

EID: 80054711379     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.09.015     Document Type: Article

References (54)

1. J.H. Ipsen, and G. Karlström M.J. Zuckermann Phase equilibria in the phosphatidylcholine-cholesterol system Biochim. Biophys. Acta 905 1987 162 172
2. G.W. Feigenson, and J.T. Buboltz Ternary phase diagram of dipalmitoyl-PC/dilauroyl-PC/cholesterol: nanoscopic domain formation driven by cholesterol Biophys. J. 80 2001 2775 2788 (Pubitemid 32521651)
3. S.L. Veatch, and S.L. Keller Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophys. J. 85 2003 3074 3083 (Pubitemid 37345795)
4. P.F.F. Almeida Thermodynamics of lipid interactions in complex bilayers Biochim. Biophys. Acta 1788 2009 72 85
5. P.F. Almeida A simple thermodynamic model of the liquid-ordered state and the interactions between phospholipids and cholesterol Biophys. J. 100 2011 420 429
6. 2H nuclear magnetic resonance and differential scanning calorimetry Biochemistry 29 1990 451 464 (Pubitemid 20037653)
7. P.J. Quinn, and C. Wolf The liquid-ordered phase in membranes Biochim. Biophys. Acta 1788 2009 33 46
8. J.L. Rubenstein, B.A. Smith, and H.M. McConnell Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines Proc. Natl. Acad. Sci. USA 76 1979 15 18
9. P.F.F. Almeida, W.L.C. Vaz, and T.E. Thompson Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis Biochemistry 31 1992 6739 6747
10. N. Kahya, and D. Scherfeld P. Schwille Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy J. Biol. Chem. 278 2003 28109 28115 (Pubitemid 36900008)
11. P.F.F. Almeida, A. Pokorny, and A. Hinderliter Thermodynamics of membrane domains Biochim. Biophys. Acta 1720 2005 1 13 (Pubitemid 43202129)
12. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature. 387 1997 569 572 (Pubitemid 27248754)
13. K. Jacobson, O.G. Mouritsen, and R.G. Anderson Lipid rafts: at a crossroad between cell biology and physics Nat. Cell Biol. 9 2007 7 14 (Pubitemid 46024188)
14. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 Suppl 2009 S323 S328
15. J.A.F. Op den Kamp Lipid asymmetry in membranes Annu. Rev. Biochem. 48 1979 47 71
16. P.R. Cullis, and M.J. Hope Physical properties and functional roles of lipids in membranes D.E. Vance, J.E. Vance, Biochemistry of Lipids and Membranes 1985 Benjamin-Cummings Menlo Park, CA 28 33
17. A. Zachowski Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement Biochem. J. 294 1993 1 14 (Pubitemid 23251903)
18. T.Y. Wang, and J.R. Silvius Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane Biophys. J. 81 2001 2762 2773 (Pubitemid 33020063)
19. S. Loew, A. Hinderliter, and S. May Stability of protein-decorated mixed lipid membranes: the interplay of lipid-lipid, lipid-protein, and protein-protein interactions J. Chem. Phys. 130 2009 045102
20. A. Hinderliter, and P.F.F. Almeida R.L. Biltonen Domain formation in a fluid mixed lipid bilayer modulated through binding of the C2 protein motif Biochemistry 40 2001 4181 4191 (Pubitemid 32280456)
21. P.F.F. Almeida, and H. Sohma A. Hinderliter Allosterism in membrane binding: a common motif of the annexins? Biochemistry 44 2005 10905 10913 (Pubitemid 41153651)
22. 2+) concentration Biochim. Biophys. Acta 1510 2001 18 28 (Pubitemid 32149882)
23. J. Ayala-Sanmartin Cholesterol enhances phospholipid binding and aggregation of annexins by their core domain Biochem. Biophys. Res. Commun. 283 2001 72 79 (Pubitemid 32912538)
24. A. Radhakrishnan, T.G. Anderson, and H.M. McConnell Condensed complexes, rafts, and the chemical activity of cholesterol in membranes Proc. Natl. Acad. Sci. USA 97 2000 12422 12427
25. R. Leventis, and J.R. Silvius Use of cyclodextrins to monitor transbilayer movement and differential lipid affinities of cholesterol Biophys. J. 81 2001 2257 2267 (Pubitemid 32917174)
26. S.-L. Niu, and B.J. Litman Determination of membrane cholesterol partition coefficient using a lipid vesicle-cyclodextrin binary system: effect of phospholipid acyl chain unsaturation and headgroup composition Biophys. J. 83 2002 3408 3415 (Pubitemid 36041957)
27. D. Huster, K. Arnold, and K. Gawrisch Influence of docosahexaenoic acid and cholesterol on lateral lipid organization in phospholipid mixtures Biochemistry 37 1998 17299 17308 (Pubitemid 29013788)
28. R.P. Richter, and J.L.K. Him A.R. Brisson On the kinetics of adsorption and two-dimensional self-assembly of annexin A5 on supported lipid bilayers Biophys. J. 89 2005 3372 3385 (Pubitemid 41636093)
29. M.L. Frazier, and J.R. Wright P.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 (Pubitemid 46536424)
30. R. Jerala, P.F.F. Almeida, and R.L. Biltonen Simulation of the gel-fluid transition in a membrane composed of lipids with two connected acyl chains: application of a dimer-move step Biophys. J. 71 1996 609 615 (Pubitemid 26289145)
31. T. Heimburg Thermal Biophysics of Membranes 2007 Wiley-VCH Weinheim, Germany
32. I.P. Sugár, R.L. Biltonen, and N. Mitchard Monte Carlo simulations of membranes: phase transition of small unilamellar dipalmitoylphosphatidylcholine vesicles Methods Enzymol. 240 1994 569 593
33. K. Binder, and D.W. Heermann Monte Carlo Simulation in Statistical Physics 3rd ed 1997 Springer New York
34. K. Kawasaki Kinetics of Ising models C. Domb, M.S. Green, Phase Transitions and Critical Phenomena Vol. 2 1972 Academic Press New York 443 501
35. N. Metropolis, and A.W. Rosenbluth E. Teller Equation of state calculations by fast computing machines J. Chem. Phys. 21 1953 1087 1092
36. W.H. Press, and S.A. Teukolsky B.P. Flannery Numerical Recipes in FORTRAN: The Art of Scientific Computing 2nd ed. 1994 Cambridge University Press Cambridge
37. J.R. Silvius Thermotropic phase transitions of pure lipids in model membranes and their modification by membrane proteins P.C. Jost, O.H. Griffith, Lipid-Protein Interactions Vol. 2 1982 Wiley-Interscience New York 239 281
38. G. Cevc Phospholipids Handbook 1993 Marcel Dekker New York
39. A. Hinderliter, R.L. Biltonen, and P.F.F. Almeida Lipid modulation of protein-induced membrane domains as a mechanism for controlling signal transduction Biochemistry 43 2004 7102 7110 (Pubitemid 38720527)
40. J. Huang, and J.E. Swanson G.W. Feigenson Nonideal mixing of phosphatidylserine and phosphatidylcholine in the fluid lamellar phase Biophys. J. 64 1993 413 425 (Pubitemid 23093854)
41. Y. Rodríguez, M. Mezei, and R. Osman Association free energy of dipalmitoylphosphatidylserines in a mixed dipalmitoylphosphatidylcholine membrane Biophys. J. 92 2007 3071 3080 (Pubitemid 46684568)
42. A. Tsamaloukas, H. Szadkowska, and H. Heerklotz Nonideal mixing in multicomponent lipid/detergent systems J. Phys. Condens. Matter 18 2006 S1125 S1138
43. J. Zhang, and H. Cao S.L. Regen Cholesterol-phospholipid association in fluid bilayers: a thermodynamic analysis from nearest-neighbor recognition measurements Biophys. J. 91 2006 1402 1406 (Pubitemid 44174256)
44. 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 (Pubitemid 43167189)
45. M.R. Brzustowicz, and V. Cherezov S.R. Wassall Molecular organization of cholesterol in polyunsaturated membranes: microdomain formation Biophys. J. 82 2002 285 298 (Pubitemid 34289802)
46. O. Bakht, P. Pathak, and E. London Effect of the structure of lipids favoring disordered domain formation on the stability of cholesterol-containing ordered domains (lipid rafts): identification of multiple raft-stabilization mechanisms Biophys. J. 93 2007 4307 4318 (Pubitemid 350294478)
47. 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 (Pubitemid 34062762)
48. S.E. Feller, and K. Gawrisch Properties of docosahexaenoic-acid- containing lipids and their influence on the function of rhodopsin Curr. Opin. Struct. Biol. 15 2005 416 422 (Pubitemid 41073832)
49. J.R. Silvius Role of cholesterol in lipid raft formation: lessons from lipid model systems Biochim. Biophys. Acta 1610 2003 174 183 (Pubitemid 36324462)
50. d phase boundary in DSPC/DOPC/cholesterol ternary mixtures using pairwise interactions J. Phys. Chem. B 115 2011 1662 1671
51. A. Tsamaloukas, H. Szadkowska, and H. Heerklotz Thermodynamic comparison of the interactions of cholesterol with unsaturated phospholipid and sphingomyelins Biophys. J. 90 2006 4479 4487 (Pubitemid 43830893)
52. A. Radhakrishnan, and H.M. McConnell Condensed complexes in vesicles containing cholesterol and phospholipids Proc. Natl. Acad. Sci. USA 102 2005 12662 12666 (Pubitemid 41279421)
53. S. Garg, and J.X. Tang C.A. Naumann Actin-induced perturbation of PS lipid-cholesterol interaction: a possible mechanism of cytoskeleton-based regulation of membrane organization J. Struct. Biol. 168 2009 11 20
54. K. Vats, and K. Knutson E.D. Sheets Peripheral protein organization and its influence on lipid diffusion in biomimetic membranes ACS Chem. Biol. 5 2010 393 403