Chloroform alters interleaflet coupling in lipid bilayers: An entropic mechanism

Journal of the Royal Society Interface

Volumn 12, Issue 106, 2015, Pages

  Reigada, Ramon ^a   Sagués, Francesc ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Anaesthesia; Chloroform; Coarse grained molecular dynamics; Interleaflet interaction; Lipid bilayer

Indexed keywords

CELL MEMBRANES; CHLORINE COMPOUNDS; CYTOLOGY; MOLECULAR DYNAMICS;

ANAESTHESIA; COARSE-GRAINED MOLECULAR DYNAMICS; COARSE-GRAINED MOLECULAR DYNAMICS SIMULATIONS; COMPUTATIONAL STUDIES; DOMAIN REGISTRATIONS; ENTROPIC GAIN; INTERLEAFLET INTERACTION; POLAR COMPOUNDS;

LIPID BILAYERS;

ALCOHOL; CARBON TETRACHLORIDE; CHLOROFORM; LIPID BILAYER;

ALGORITHM; ARTICLE; CONTROLLED STUDY; DIELECTRIC CONSTANT; ENTROPY; GENERAL ANESTHESIA; IONIC STRENGTH; LIPID BILAYER; MEMBRANE COMPONENT; MEMBRANE LEAFLET; MOLECULAR DYNAMICS; NERVE CONDUCTION; PHASE SEPARATION; STATIC ELECTRICITY; SURFACE TENSION; CELL MEMBRANE; CHEMICAL MODEL; CHEMISTRY; MEMBRANE FLUIDITY;

CHLOROFORM; ENTROPY; LIPID BILAYERS; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; MODELS, CHEMICAL; MOLECULAR DYNAMICS SIMULATION;

EID: 84929500846     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2015.0197     Document Type: Article

References (56)

1. Harding AS, Hancock JF. 2008 Using plasma membrane nanoclusters to build better signaling circuits. Trends Cell Biol. 18, 364-371. (doi:10.1016/j.tcb.2008.05.006)
2. Simons K, Ikonen E. 1997 Functional rafts in cell membranes. Nature 387, 569-572. (doi:10.1038/42408)
3. Simons K, Toomre D. 2000 Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39. (doi:10.1038/35036052)
4. Anderson RG, Jacobson K. 2002 A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821-1825. (doi:10.1126/science.1068886)
5. Munro S. 2003 Lipid rafts: elusive or illusive? Cell 115, 377-388. (doi:10.1016/S0092-8674(03)00882-1)
6. May S. 2009 Transmonolayer coupling of fluid domains in lipid bilayers. Soft Matter 5, 3148-3156. (doi:10.1039/b901647c)
7. Collins MD, Keller SL. 2008 Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl Acad. Sci. USA 105, 124-128. (doi:10.1073/pnas.0702970105)
8. Perlmutter JD, Sachs JN. 2011 Interleaflet interaction and asymmetry in phase separated lipid bilayers: molecular dynamics simulations. J. Am. Chem. Soc. 133, 6563-6577. (doi:10.1021/ja106626r)
9. Chiantia S, London E. 2012 Acyl chain length and saturation modulate interleaflet coupling in asymmetric bilayers: effects on dynamics and structural order. Biophys. J. 103, 2311-2319. (doi:10.1016/j.bpj.2012.10.033)
10. 2+ signaling: single-molecule tracking study. J. Cell Biol. 177, 731-742. (doi:10.1083/jcb.200609175)
11. Janmey PA, Kinnunen PKJ. 2006 Biophysical properties of lipids and dynamic membranes. Trends Cell Biol. 16, 538-546. (doi:10.1016/j.tcb.2006.08.009)
12. Keller SL, Gruner SM, Gawrisch K. 1996 Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim. et Biophys. Acta 1278, 241-246. (doi:10.1016/0005-2736(95)00229-4)
13. 2 activity. Chem. Phys. Lipids 73, 209-222. (doi:10.1016/0009-3084(94)90182-1)
14. Brown MF. 1994 Modulation of rhodopsin function by properties of the membrane bilayer. Chem. Phys. Lipids 73, 159-180. (doi:10.1016/0009-3084 (94)90180-5)
15. Cantor RS. 1997 The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Biochemistry 36, 2339-2344. (doi:10.1021/bi9627323)
16. + channel responds to changes in the inner membrane leaflet. Proc. Natl Acad. Sci. USA 110, 749-754. (doi:10.1073/pnas.1217323110)
17. Gruner SM, Shyamsunder E. 1991 Is the mechanism of general anesthesia related to lipid membrane spontaneous curvature? Ann. N.Y. Acad. Sci. 625, 685-697. (doi:10.1111/j.1749-6632.1991.tb33902.x)
18. Reigada R. 2011 Influence of chloroform in liquid-ordered and liquid-disordered phases in lipid membranes. J. Phys. Chem. B 115, 2527-2535. (doi:10.1021/jp110699h)
19. Reigada R. 2013 Atomistic study of lipid membranes containing chloroform: looking for a lipid-mediated mechanism of anesthesia. PLoS ONE 81, e52631. (doi:10.1371/journal.pone.0052631)
20. Turkyilmaz S, Chen WH, Mitomo H, Regen SL. 2009 Loosening and reorganization of fluid phospholipid bilayers by chloroform. J. Am. Chem. Soc. 131, 5068-5069. (doi:10.1021/ja9011468)
21. Lindahl E, Hess B, van der Spoel D. 2001 GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7, 306-317.
22. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH. 2007 The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824. (doi:10.1021/jp071097f)
23. Risselada H, Marrink SJ. 2008 The molecular face of lipid rafts in model membranes. Proc. Natl Acad. Sci. USA 105, 17 367-17 372. (doi:10.1073/pnas.0807527105)
24. Marrink SJ, Tieleman DP. 2013 Perspective on the Martini model. Chem. Soc. Rev. 42, 6801-6822. (doi:10.1039/c3cs60093a)
25. Yesylevskyy SO, Schäfer LV, Sengupta D, Marrink SJ. 2010 Polarizable water model for coarse-grained MARTINI force field. PLoS Comput. Biol. 6, e1000810. (doi:10.1371/journal.pcbi.1000810)
26. Torrie GM, Valleau JP. 1977 Nonphysical sampling distributions in Monte Carlo free-energy estimation: umbrella sampling. J. Comput. Phys. 23, 187-199. (doi:10.1016/0021-9991(77)90121-8)
27. Hub JS, de Groot BL, van der Spoel D. 2010 g-wham - a free weighted histogram analysis implementation including robust error and autocorrelation estimates. J. Chem. Theory Comput. 6, 3713-3720. (doi:10.1021/ct100494z)
28. Vorobyov I, Bennett WFD, Tieleman DP, Allen TW, Noskov S. 2012 The role of atomic polarization in the thermodynamics of chloroform partitioning to lipid bilayers. J. Chem. Theory Comput. 8, 618-628. (doi:10.1021/ct200417p)
29. Campelo F, Arnarez C, Marrink SJ, Kozlov MM. 2014 Helfrich model of membrane bending: from Gibbs theory of liquid interfaces to membranes as thick anisotropic elastic layers. Adv. Colloid Interface Sci. 208, 25-33. (doi:10.1016/j.cis.2014.01.018)
30. Barnoud J, Rossi G, Marrink SJ, Monticelli L. 2014 Hydrophobic compounds reshape membrane domains. PLoS Comput. Biol. 10, e1003873. (doi:10.1371/journal.pcbi.1003873)
31. Braun AR, Lacy MM, Ducas VC, Rhoades E, Sachs JN. 2014 α-Synuclein-induced membrane remodeling is driven by binding affinity, partition depth and interleaflet order asymmetry. J. Am. Chem. Soc. 136, 9962-9972. (doi:10.1021/ja5016958)
32. Santo KP, Berkowitz ML. 2014 Shock wave interaction with a phospholipid membrane: coarse-grained computer simulations. J. Chem. Phys. 140, 054906. (doi:10.1063/1.4862987)
33. Gray E, Karslake J, Machta BB, Veatch SL. 2013 Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophys. J. 105, 2751-2759. (doi:10.1016/j.bpj.2013.11.005)
34. Lindblom G, Orädd G. 1994 NMR studies of translational diffusion in lyotropic liquid crystals and lipid membranes. Prog. Nucl. Magn. Res. Spectr. 26, 483-515. (doi:10.1016/0079-6565(94)80014-6)
35. Lindblom G, Orädd G. 2009 Lipid lateral diffusion and membrane heterogeneity. Biophys. Biochim. Acta 1788, 234-244. (doi:10.1016/j.bbamem.2008.08.016)
36. Kahya N, Scherfeid D, Bacia K, Poolman B, Schwille P. 2003 Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 278, 28 109-28 115. (doi:10.1074/jbc.M302969200)
37. Almeida PF, Vaz WL, Thompson TE. 1992 Lateral diffusion in the liquid phase of DMPC/cholesterol lipid bilayers: a free volume analysis. Biochemistry 31, 6739-6747. (doi:10.1021/bi00144a013)
38. Wohlert J, Edholm O. 2006 Dynamics in atomistic simulations of phospholipid membranes: nuclear magnetic resonance relaxation rates and lateral diffusion. J. Chem. Phys. 125, 204703. (doi:10.1063/1.2393240)
39. Wang CY, Hill RJ. 2014 Transmembrane protein diffusion in gel-supported dual-leaflet membranes. Biophys. J. 107, 2296-2304. (doi:10.1016/j.bpj.2014.10.016)
40. Wimley WC, Thompson TE. 1990 Exchange and flip-flop of dimyristoyl phosphatidylcholine in liquid-crystalline, gel and two-component, two-phase large unilamellar vesicles. Biochemistry 29, 1296-1303. (doi:10.1021/bi00457a027)
41. Steck TL, Ye J, Lange Y. 2002 Probing red cell membrane cholesterol movement with cyclodextrin. Biophys. J. 83, 2118-2125. (doi:10.1016/S0006-3495(02)73972-6)
42. Bennett WFD, MacCallum JL, Hinner MJ, Marrink SJ, Tieleman DP. 2009 Molecular view of cholesterol flip-flop and chemical potential in different membrane environments. J. Am. Chem. Soc. 131, 12 714-12 720. (doi:10.1021/ja903529f)
43. Bennett WFD, Tieleman DP. 2012 Cholesterol translocation in a phospholipid membrane. J. Lipid Res. 53, 421-429. (doi:10.1194/jlr.M022491)
44. Lange Y, Dolde J, Steck TL. 1981 The effect of cholesterol and other intercalated amphipaths on the contour and stability of the isolated red cell membrane. J. Biol. Chem. 256, 5321-5323.
45. Khelashvili G, Kollmitzer B, Heftberger P, Pabst G, Harries D. 2013 Calculating the bending modulus for multicomponent lipid membranes in different thermodynamic phases. J. Chem. Theory Comput. 9, 3866-3871. (doi:10.1021/ct400492e)
46. Fischer TM. 1992 Bending stiffness of lipid bilayers. I. Bilayer couple or single-layer bending?Biophys. J. 63, 1328-1335. (doi:10.1016/S0006-3495(92)81710-1)
47. Patra M, Salonen E, Terama E, Vattulainen I, Faller R, Lee BW, Holopainen J, Karttunen M. 2006 Under the influence of alcohol: the effect of ethanol and methanol on lipid bilayers. Biophys. J. 90, 1121-1135. (doi:10.1529/biophysj.105.062364)
48. Garbès Putzel G, Uline MJ, Szleifer I, Schick M. 2011 Interleaflet coupling and domain registry in phaseseparated lipid bilayers. Biophys. J. 100, 996-1004. (doi:10.1016/j.bpj.2011.01.021)
49. Collins MD. 2008 Interleaflet coupling mechanisms in bilayers of lipids and cholesterol. Biophys. J. 940, L32-L34. (doi:10.1529/biophysj.107.124362)
50. Heimburg T. 2010 Lipid ion channels. Biophys. Chem. 150, 2-22. (doi:10.1016/j.bpc.2010.02.018)
51. + channel behavior induced by a lipid phase transition. Biophys. J. 99, 3675-3683. (doi:10.1016/j.bpj.2010.10.042)
52. Li X, Serwanski DR, De Blas AL. 2007 Two pools of Triton X-100-insoluble GABAA receptors are present on the brain, one associated to lipid rafts and another one to the postsynaptic GABAergic complex. J. Neurochem. 102, 1329-1345. (doi:10.1111/j.1471-4159.2007.04635.x)
53. North C, Cafiso DS. 1997 Contrasting membrane localization and behavior of halogenated cyclobutanes that follow or violate the Meyer-Overton hypothesis of general anesthetic potency. Biophys. J. 72, 1754-1761. (doi:10.1016/S0006-3495(97)78821-0)
54. Seeman P. 1972 The membrane action of anesthetics and tranquilizers. Pharmacol. Rev. 24, 583-655.
55. Reyes J, Latorre R. 1979 Effect of the anesthetics benzyl alcohol and chloroform on bilayers made from monolayers. Biophys. J. 28, 259-280. (doi:10.1016/S0006-3495(79)85175-9)
56. Kamaya H, Kaneshina S, Ueda I. 1981 Partition equilibrium of inhalation anesthetics and alcohols between water and membranes of phospholipids with varying acyl chain-lengths. Biochim. Biophys. Acta 646, 135-142. (doi:10.1016/0005-2736(81)90280-7)