Aspirin inhibits formation of cholesterol rafts in fluid lipid membranes

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 3, 2015, Pages 805-812

  Alsop, Richard J ^a   Toppozini, Laura ^a   Marquardt, Drew ^b   Kučerka, Norbert ^c,d,e   Harroun, Thad A ^b   Rheinstädter, Maikel C ^a,c  

^a MCMASTER UNIVERSITY   (Canada)

^b BROCK UNIVERSITY   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d Physics and Informatics   (Slovakia)

^e JOINT INSTITUTE FOR NUCLEAR RESEARCH   (Russian Federation)

Author keywords

Aspirin; Aspirincholesterol interaction; Cholesterol; Cholesterol rafts; Lipid membranes

Indexed keywords

ACETYLSALICYLIC ACID; CHOLESTEROL; DIPALMITOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; MEMBRANE LIPID; NONSTEROID ANTIINFLAMMATORY AGENT;

ARTICLE; CALORIMETRY; COMPRESSIBILITY MODULUS; DRUG DETERMINATION; DRUG EFFECT; DRUG INTERACTION; DRUG LIPID INTERACTION; DRUG MECHANISM; DRUG STRUCTURE; LANGMUIR BLODGETT FILM; LIPID ANALYSIS; LIPID BILAYER; LIPID MEMBRANE; LIPID RAFT; MEMBRANE FLUIDITY; MEMBRANE STRUCTURE; NEUTRON DIFFRACTION; PHASE TRANSITION; PHYSICAL PARAMETERS; CELL MEMBRANE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; DIFFERENTIAL SCANNING CALORIMETRY; DRUG EFFECTS; HUMAN; KINETICS;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; CALORIMETRY, DIFFERENTIAL SCANNING; CELL MEMBRANE; CHOLESTEROL; HUMANS; KINETICS; LIPID BILAYERS; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NEUTRON DIFFRACTION;

EID: 84919782929     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.11.023     Document Type: Article

References (62)

1. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569572
2. K. Simons, and E. Ikonen How cells handle cholesterol Science 290 2000 1721 1726
3. D.M. Engelman Membranes are more mosaic than fluid Nature 438 2005 578 580
4. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 2009 S323 S328
5. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
6. C. Eggeling, C. Ringemann, R. Medda, G. Schwarzmann, and K. Sandhoff Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 2009 1159 1162
7. F.G. van der Goot, and T. Harder Raft membrane domains: from a liquid-ordered membrane phase to a site of pathogen attack Semin. Immunol. 13 2001 89 97
8. T. Apajalahti, P. Niemelä, P.N. Govindan, M.S. Miettinen, and E. Salonen Concerted diffusion of lipids in raft-like membranes Faraday Discuss. 144 2010 411 430
9. A. Hall, T. Róg, M. Karttunen, and I. Vattulainen Role of glycolipids in lipid rafts: a view through atomistic molecular dynamics simulations with galactosylceramide J. Phys. Chem. B 114 2010 7797 7807
10. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nat. Rev. Mol. Cell Biol. 11 2010 688 699
11. J. Ehrig, E.P. Petrov, and P. Schwille Phase separation and near-critical fluctuations in two-component lipid membranes: Monte Carlo simulations on experimentally relevant scales New J. Phys. 13 2011 045019
12. T. Murtola, T. Róg, E. Falck, M. Karttunen, and I. Vattulainen Transient ordered domains in single-component phospholipid bilayers Phys. Rev. Lett. 97 2006 238102
13. B. Brüning, E. Wald, W. Schrader, R. Behrends, and U. Kaatze Slowing down in lipid bilayers: domain structure fluctuations and axial diffusion Soft Matter 5 2009 3340 3346
14. M.C. Rheinstädter, and O.G. Mouritsen Small-scale structure in fluid cholesterol-lipid bilayers Curr. Opin. Colloid Interface Sci. 18 2013 440 447
15. 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
16. M.R. Vist, and J.H. Davis Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: deuterium nuclear magnetic resonance and differential scanning calorimetry Biochemistry 29 1990 451 464
17. C.L. Armstrong, M.A. Barrett, A. Hiess, T. Salditt, and J. Katsaras Effect of cholesterol on the lateral nanoscale dynamics of fluid membranes Eur. Biophys. J. 41 2012 901 913
18. C.L. Armstrong, W. Häußler, T. Seydel, J. Katsaras, and M.C. Rheinstädter Nanosecond lipid dynamics in membranes containing cholesterol Soft Matter 10 2014 2600 2611
19. S. Meinhardt, R.L.C. Vink, and F. Schmid Monolayer curvature stabilizes nanoscale raft domains in mixed lipid bilayers Proc. Natl. Acad. Sci. U. S. A. 110 2013 4476 4481
20. C.L. Armstrong, D. Marquardt, H. Dies, N. Kučerka, and Z. Yamani The observation of highly ordered domains in membranes with cholesterol PLoS ONE 8 2013 e66162
21. A.J. Sodt, M.L. Sandar, K. Gawrisch, R.W. Pastor, and E. Lyman The molecular structure of the liquid-ordered phase of lipid bilayers J. Am. Chem. Soc. 136 2014 725 732
22. Y. Zhang, A. Lervik, J. Seddon, and F. Bresme A coarse-grained molecular dynamics investigation of the phase behavior of dppc/cholesterol mixtures Chem. Phys. Lipids 2014 10.1016/j.chemphyslip.2014.07.011
23. L. Toppozini, S. Meinhardt, C. Armstrong, Z. Yamani, and N. Kučerka The structure of cholesterol in lipid rafts Phys. Rev. Lett. 113 2014 228101
24. M. Barrett, S. Zheng, L. Toppozini, R. Alsop, and H. Dies Solubility of cholesterol in lipid membranes and the formation of immiscible cholesterol plaques at high cholesterol concentrations Soft Matter 9 2013 9342 9351
25. R. Ziblat, L. Leiserowitz, and L. Addadi Crystalline domain structure and cholesterol crystal nucleation in single hydrated DPPC:cholesterol:POPC bilayers J. Am. Chem. Soc. 132 2010 9920 9927
26. R. Ziblat, L. Leiserowitz, and L. Addadi Crystalline lipid domains: characterization by X-ray diffraction and their relation to biology Angew. Chem. Int. Ed. 50 2011 3620 3629
27. R. Ziblat, I. Fargion, L. Leiserowitz, and L. Addadi Spontaneous formation of two-dimensional and three-dimensional cholesterol crystals in single hydrated lipid bilayers Biophys. J. 103 2012 255 264
28. I. Solomonov, J. Daillant, G. Fragneto, K. Kjaer, and J. Micha Hydrated cholesterol: phospholipid domains probed by synchrotron radiation Eur. Phys. J. A. 30 2009 215 221
29. M. Lucio, J. Lima, and S. Reis Drug-membrane interactions: significance for medicinal chemistry Curr. Med. Chem. 17 2010 1795 1809
30. L.M. Lichtenberger, Y. Zhou, V. Jayaraman, J.R. Doyen, and R.G. O'Neil Insight into nsaid-induced membrane alterations, pathogenesis and therapeutics: characterization of interaction of nsaids with phosphatidylcholine Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1821 2012 994 1002
31. C. Pereira-Leite, C. Nunes, and S. Reis Interaction of nonsteroidal anti-inflammatory drugs with membranes: in vitro assessment and relevance for their biological actions Prog. Lipid Res. 52 2013 571 584
32. M. Barrett, S. Zheng, G. Roshankar, R. Alsop, and R. Belanger Interaction of aspirin (acetylsalicylic acid) with lipid membranes PLoS ONE 7 2012 e34357
33. M. Suwalsky, J. Belmar, F. Villena, M.J. Gallardo, and M. Jemiola-Rzeminska Acetylsalicylic acid (aspirin) and salicylic acid interaction with the human erythrocyte membrane bilayer induce in vitro changes in the morphology of erythrocytes Arch. Biochem. Biophys. 539 2013 9 19
34. L.M. Lichtenberger, Y. Zhou, E.J. Dial, and R.M. Raphael Nsaid injury to the gastrointestinal tract: evidence that nsaids interact with phospholipids to weaken the hydrophobic surface barrier and induce the formation of unstable pores in membranes J. Pharm. Pharmacol. 58 2006 1421 1428
35. Y. Zhou, K.J. Cho, S.J. Plowman, and J.F. Hancock Nonsteroidal anti-inflammatory drugs alter the spatiotemporal organization of ras proteins on the plasma membrane J. Biol. Chem. 287 2012 16586 16595
36. R.J. Alsop, M.A. Barrett, S. Zheng, H. Dies, and M.C. Rheinstädter Acetylsalicylic acid (asa) increases the solubility of cholesterol when incorporated in lipid membranes Soft Matter 10 2014 4275 4286
37. Y. Choi, S.J. Attwood, M.I. Hoopes, E. Drolle, and M. Karttunen Melatonin directly interacts with cholesterol and alleviates cholesterol effects in dipalmitoylphosphatidylcholine monolayers Soft Matter 10 2014 206 213
38. P. Wydro, and K. Hac-Wydro Thermodynamic description of the interactions between lipids in ternary Langmuir monolayers: the study of cholesterol distribution in membranes J. Phys. Chem. B 111 2007 2495 2502
39. J. Katsaras, and K.R. Jeffrey Evidence of the hydration force in gel phase lipid multibilayers Europhys. Lett. 38 1997 43 48
40. D. Marsh Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams Biochim. Biophys. Acta Biomembr. 1798 2010 688 699
41. T. Heimburg Thermal biophysics of membranes 2008 John Wiley & Sons.
42. J. Jones, L. Lue, A. Saiani, and G. Tiddy Density, DSC, X-ray and NMR measurements through the gel and lamellar phase transitions of 1-myristoyl-2-stearoyl-sn-glycero-3-phosphatidylcholine (MSPC) and 1-stearoyl-2-myristoyl-sn-glycero-3-phosphatidylcholine (SMPC): observation of slow relaxation processes and mechanisms of phase transitions Phys. Chem. Chem. Phys. 14 2012 5452 5469
43. A.M. Alaouie, and A.I. Smirnov Formation of a ripple phase in nanotubular dimyristoylphosphatidylcholine bilayers confined inside nanoporous aluminum oxide substrates observed by DSC Langmuir 22 2006 5563 5565
44. C.L. Armstrong, M.A. Barrett, L. Toppozini, N. Kučerka, and Z. Yamani Co-existence of gel and fluid domains in single-component phospholipid membranes Soft Matter 8 2012 4687 4694
45. C.F. Majkrzak, C. Metting, B.B. Maranville, J.A. Dura, and S. Satija Determination of the effective transverse coherence of the neutron wave packet as employed in reflectivity investigations of condensed-matter structures. I. Measurements Phys. Rev. A 89 2014 033851
46. G.J. Roth, N. Stanford, and P.W. Majerus Acetylation of prostaglandin synthase by aspirin Proc. Natl. Acad. Sci. U. S. A. 72 1975 3073 3076
47. C. Patrono, L.A. Garca Rodrguez, R. Landolfi, and C. Baigent Low-dose aspirin for the prevention of atherothrombosis N. Engl. J. Med. 353 2005 2373 2383
48. V.B. O'Donnell, R.C. Murphy, and S.P. Watson Platelet lipidomics modern day perspective on lipid discovery and characterization in platelets Circ. Res. 114 2014 1185 1203
49. S.J. Shattil, and R.A. Cooper Membrane microviscosity and human platelet function Biochemistry (Mosc) 15 1976 4832 4837
50. P. Padmavathi, V.D. Reddy, P. Maturu, and N. Varadacharyulu Smoking-induced alterations in platelet membrane fluidity and na +/k+-ATPpase activity in chronic cigarette smokers J. Atheroscler. Thromb. 17 2010 619 627
51. K. Gousset, W.F. Wolkers, N.M. Tsvetkova, A.E. Oliver, and C.L. Field Evidence for a physiological role for membrane rafts in human platelets J. Cell. Physiol. 190 2002 117 128
52. N. Kučerka, S. Tristram-Nagle, and J.F. Nagle Closer look at structure of fully hydrated fluid phase DPPC bilayers Biophys. J. 90 2006 L83 L85
53. J. Gallová, D. Uhrková, N. Kučerka, S. Doktorovová, and S.S. Funari The effects of cholesterol and β-sitosterol on the structure of saturated diacylphosphatidylcholine bilayers Eur. Biophys. J. 40 2011 153 163
54. M. Lúcio, C. Nunes, D. Gaspar, K. Golebska, and M. Wisniewski Effect of anti-inflammatory drugs in phosphatidylcholine membranes: a fluorescence and calorimetric study Chem. Phys. Lett. 471 2009 300 309
55. K. Nag, K. Keough, M. Montero, J. Trias, and M. Pons Evidence of segregation of a quinolone antibiotic in dipalmitoylphosphatidylcholine environment J. Liposome Res. 6 1996 713 736
56. A.V. Kityk, M.C. Rheinstädter, K. Knorr, and H. Rieger Aging and memory effects in β-hydroquinone-clathrate Phys. Rev. B 65 2002 144415
57. M.C. Rheinstädter, K. Knorr, and H. Rieger Aging and scaling laws in β-hydroquinone-clathrate Phys. Rev. B 69 2004 144427
58. T.T. Mills, G.E.S. Toombes, S. Tristram-Nagle, D.M. Smilgies, and G.W. Feigenson Order parameters and areas in fluid-phase oriented lipid membranes using wide angle X-ray scattering Biophys. J. 95 2008 669 681
59. M.C. Rheinstädter, C. Ollinger, G. Fragneto, and T. Salditt Collective dynamics in phospholipid bilayers investigated by inelastic neutron scattering: exploring the dynamics of biological membranes with neutrons Physica B 350 2004 136 139
60. J. Katsaras, R. Epand, and R. Epand Absence of chiral domains in mixtures of dipalmitoylphosphatidylcholine molecules of opposite chirality Phys. Rev. E. 55 1997 3751
61. S. Mabrey, and J.M. Sturtevant Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry Proc. Natl. Acad. Sci. 73 1976 3862 3866
62. A. Zheludev Reslib http://www.neutron.ethz.ch/research/resources/reslib 2009