Biophysical changes induced by xenon on phospholipid bilayers

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 5, 2013, Pages 1347-1356

  Booker, Ryan D ^a   Sum, Amadeu K ^a  

^a Department of Geology and Geological Engineering   (United States)

Author keywords

General anesthesia; Lipid membrane; Molecular dynamics; Phase transition; Simulation

Indexed keywords

DIOLEOYLPHOSPHATIDYLCHOLINE; PHOSPHOLIPID; XENON;

ARTICLE; BIOPHYSICS; CONCENTRATION (PARAMETERS); DIFFERENTIAL SCANNING CALORIMETRY; HYDROPHOBICITY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE FLUIDITY; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR MODEL; PHASE TRANSITION; PRIORITY JOURNAL; TEMPERATURE SENSITIVITY; THERMODYNAMICS;

ANESTHETICS, INHALATION; BIOPHYSICAL PROCESSES; CALORIMETRY, DIFFERENTIAL SCANNING; HOT TEMPERATURE; LIPID BILAYERS; LIPOSOMES; MEMBRANE FLUIDITY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PHASE TRANSITION; PHOSPHATIDYLCHOLINES; PHOSPHOLIPIDS; PRESSURE; THERMODYNAMICS; XENON;

EID: 84875156290     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.01.016     Document Type: Article

References (100)

1. B. Urban Modern Anesthetics J. Schüttler, H. Schwilden, 2008 Spinger-Verlag Berlin
2. The Joint Commission Preventing, and managing the impact of, anesthesia awareness Sentinel Event Alert 32 2004 1 3
3. H. Meyer Zur theorie der alkoholnarkose Naunyn-Schmiedebergs Arch. Pharmakol. 42 1899 109 118
4. C. Overton Studien über die Narkose: Zugleich ein Beitrag zur Allgemeinen Pharmakologie 1901 Verlag von Gustav Fischer Jena
5. N.P. Franks, and W.R. Lieb Do general anaesthetics act by competitive binding to specific receptors? Nature 310 1984 599 601
6. P. Barash, B. Cullen, R. Stoelting, and M. Stock Handbook of Clinical Anesthesia 2009 Lippincott, Williams, & Wilkins Philadelphia
7. B. Urban, M. Bleckwenn, and M. Barann Interactions of anesthetics with their targets: non-specific, specific or both? Pharmacol. Ther. 111 2006 729 770
8. N. Franks Molecular targets underlying general anaesthesia Br. J. Pharmacol. 147 2006 S72 S81
9. A. Lugli, C. Yost, and C. Kindler Anaesthetic mechanisms: update on the challenge of unravelling the mystery of anaesthesia Eur. J. Anaesthesiol. 26 2009 807 820
10. S. Cullen, and E. Gross The anesthetic properties of xenon in animals and human beings, with additional observations on krypton Science 113 1951 580 582
11. R. Sanders, N. Franks, and M. Maze Xenon: no stranger to anaesthesia Br. J. Anaesth. 91 2003 709 717
12. 2O): the dominant ozone-depleting substance emitted in the 21st century Science 326 2009 123 125
13. T. Goto, K. Suwa, S. Uezono, F. Ichinose, M. Uchiyama, and S. Morita The blood-gas partition coefficient of xenon may be lower than generally accepted Br. J. Anaesth. 80 1998 255 256
14. S. Wilhelm, D. Ma, M. Maze, and N.P. Franks Effects of xenon on in vitro and in vivo models of neuronal injury Anesthesiology 96 2002 1485 1491
15. D. Ma, S. Wilhelm, M. Maze, and N.P. Franks Neuroprotective and neurotoxic properties of the 'inert' gas, xenon Br. J. Anaesth. 89 2002 739 746
16. B. Lachmann, S. Armbruster, W. Schairer, M. Landstra, A. Trouwborst, G.J.V. Daal, A. Kusuma, and W. Erdmann Safety and efficacy of xenon in routine use as an inhalational anaesthetic Lancet 335 1990 1413 1415
17. P. Harris, and R. Barnes The uses of helium and xenon in current clinical practice Anesthesia 63 2008 284 293
18. A. Brücken, M. Coburn, S. Rex, R. Rossaint, and M. Fries Current developments in xenon research. Importance for anesthesia and intensive care medicine Anaesthesist 59 2010 883 895
19. N. Franks, R. Dickinson, S. de Sousa, A. Hall, and W. Lieb How does xenon produce anaesthesia? Nature 396 1998 324
20. S.L. de Sousa, R. Dickinson, W.R. Lieb, and N.P. Franks Contrasting synaptic actions of the inhalational general anesthetics isoflurane and xenon Anesthesiology 92 2000 1055 1066
21. E. Salmi, R. Laitio, S. Aalto, A. Maksimow, J. Långsjö, K. Kaisti, R. Aantaa, V. Oikonen, L. Metsähonkala, K. Någren, E. Korpi, and H. Scheinin Xenon does not affect gamma-aminobutyric acid type A receptor binding in humans Anesth. Analg. 106 2008 129 134
22. T. Yamakura, and R.A. Harris Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels. comparison with isoflurane and ethanol Anesthesiology 93 2000 1095 1101
23. J. Ogata, M. Shiraishi, T. Namba, C. Smothers, J. Woodward, and R. Harris Effects of anesthetics on mutant N-methyl-d-aspartate receptors expressed in Xenopus oocytes J. Pharmacol. Exp. Ther. 318 2006 434 443
24. R. Dickinson, B. Peterson, P. Banks, C. Simillis, J. Martin, C. Valenzuela, M. Maze, and N. Franks Competitive inhibition at the glycine site of the N-methyl-d-aspartate receptor by the anesthetics xenon and isoflurane: evidence from molecular modeling and electrophysiology Anesthesiology 107 2007 756 767
25. L. Liu, Y. Xu, and P. Tang Mechanistic insights into xenon inhibition of NMDA receptors from MD simulations J. Phys. Chem. B 114 2010 9010 9016
26. P. Nagele, L. Metz, and M. Crowder Xenon acts by inhibition of non-N-methyl-d-aspartate receptor-mediated glutamatergic neurotransmission in Caenorhabditis elegans Anesthesiology 103 2005 508 513
27. E. Eger, D. Raines, S. Shafer, H. Hemmings, and J. Sonner Is a new paradigm needed to explain how inhaled anesthetics produce immobility? Anesth. Analg. 107 2008 832 848
28. S. Rex, W. Schaefer, P. Meyer, R. Rossaint, C. Boy, K. Setani, U. Büll, and J. Baumert Positron emission tomography study of regional cerebral metabolism during general anesthesia with xenon in humans Anesthesiology 105 2006 936 943
29. R. Laitio, J. Långsjö, S. Aalto, K. Kaisti, E. Salmi, A. Maksimow, R. Aantaa, V. Oikonen, T. Viljanen, R. Parkkola, and H. Scheinin The effects of xenon anesthesia on the relationship between cerebral glucose metabolism and blood flow in healthy subjects: a positron emission tomography study Anesth. Analg. 108 2009 593 600
30. M. Gruss, T.J. Bushell, D.P. Bright, W.R. Lieb, A. Mathie, and N.P. Franks Two-pore-domain K + channels are a novel target for the anesthetic gases xenon, nitrous oxide, and cyclopropane Mol. Pharmacol. 65 2004 443 452
31. D. Pang, C. Robledo, D. Carr, T. Gent, A. Vyssotski, A. Caley, A.W.W. Zecharia, S. Brickley, and N. Franks An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action Proc. Natl. Acad. Sci. U.S.A. 106 2009 17546 17551
32. R. Lazarenko, S. Willcox, S. Shu, A. Berg, J. Vesna, E. Talley, X. Chen, and D. Bayliss Motoneuronal task channels contribute to immobilizing effects of inhalational general anesthetics J. Neurosci. 30 2010 7691 7704
33. M. Jensen, and O. Mouritsen Lipids do influence protein function - the hydrophobic matching hypothesis revisited Biochim. Biophys. Acta 1666 2004 205 226
34. O. Andersen, and R. Koeppe Bilayer thickness and membrane protein function: an energetic perspective Annu. Rev. Biophys. Bioeng. 36 2007 107 130
35. D. Marsh Protein modulation of lipids, and vice-versa, in membranes Biochim. Biophys. Acta 1778 2008 1545 1575
36. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
37. D. Schmidt, and R. MacKinnon Voltage-dependent K + channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane Proc. Natl. Acad. Sci. U.S.A. 105 2008 19276 19281
38. B. Martinac, and O. Hamill Gramicidin A channels switch between stretch activation and stretch inactivation depending on bilayer thickness Proc. Natl. Acad. Sci. U.S.A. 99 2002 4308 4312
39. J. Lundbæk, R. Koeppe, and O. Andersen Amphiphile regulation of ion channel function by changes in the bilayer spring constant Proc. Natl. Acad. Sci. U.S.A. 107 2010 15427 15430
40. J. Lundbæk Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs J. Gen. Physiol. 131 2008 421 429
41. R. Søgaard, T. Werge, C. Bertelsen, C. Lundbye, K. Madsen, C. Nielsen, and J. Lundbaek GABA(A) receptor function is regulated by lipid bilayer elasticity Biochemistry 45 2006 13118 13129
42. R.S. Cantor The lateral pressure profile in membranes: a physical mechanism of general anesthesia Biochemistry 36 1997 2339 2344
43. Y. Suezaki, A. Petrov, and I. Ueda Theoretical model of anesthetic action upon ion channels mediated by lipid membrane Int. Congr. Ser. 1283 2005 227 230
44. D. Marsh Lateral pressure profile, spontaneous curvature frustration, and the incorporation and conformation of proteins in membranes Biophys. J. 93 2007 3884 3899
45. E. Terama, O. Ollila, E. Salonen, A. Rowat, C. Trandum, P. Westh, M. Patra, M. Karttunen, and I. Vattulainen Influence of ethanol on lipid membranes: from lateral pressure profiles to dynamics and partitioning J. Phys. Chem. B 112 2008 4131 4139
46. B. Griepernau, and R. Böckmann The influence of 1-alkanols and external pressure on the lateral pressure profiles of lipid bilayers Biophys. J. 95 2008 5766 5778
47. T. Heimburg, and A. Jackson On soliton propagation in biomembranes and nerves Proc. Natl. Acad. Sci. U.S.A. 102 2005 9790 9795
48. T. Heimburg, and A. Jackson The thermodynamics of general anesthesia Biophys. J. 92 2007 3159 3165
49. T. Heimburg, and A. Jackson On the action potential as a propagating density pulse and the role of anesthetics Biophys. Rev. Lett. 2 2007 1 22
50. S. Singer, and G. Nicolson The fluid mosaic model of the structure of cell membranes Science 175 1972 720 731
51. R. Cherry Protein mobility in membranes FEBS Lett. 55 1975 1 7
52. R. Venable, Y. Zhang, B. Hardy, and R. Pastor Molecular dynamics simulations of a lipid bilayer and of hexadecane: an investigation of membrane fluidity Science 262 1993 223 226
53. S. Marrink, and H. Berendsen Permeation process of small molecules across lipid membranes studied by molecular dynamics simulations J. Phys. Chem. 100 1996 16729 16738
54. D. Bemporad, J. Essex, and C. Luttmann Permeation of small molecules through a lipid bilayer: a computer simulation study J. Phys. Chem. B 108 2004 4875 4884
55. J. MacCallum, and D. Tieleman Computer simulation of the distribution of hexane in a lipid bilayer: spatially resolved free energy, entropy, and enthalpy profiles J. Am. Chem. Soc. 128 2006 125 130
56. A. Sum, R. Faller, and J. Pablo Molecular simulation study of phospholipid bilayers and insights of the interactions with disaccharides Biophys. J. 85 2003 2830 2844
57. B. Lee, R. Faller, A. Sum, I. Vattulainen, M. Patra, and M. Karttunen Structural effects of small molecules on phospholipid bilayers investigated by molecular simulations Fluid Phase Equilib. 225 2004 63 68
58. C. Pereira, R. Lins, I. Chandrasekhar, L. Freitas, and P. Hünenberger Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study Biophys. J. 86 2004 2273 2285
59. S. Leekumjorn, and A. Sum Molecular dynamics study on the stabilization of dehydrated lipid bilayers with glucose and trehalose J. Phys. Chem. B 112 2008 10732 10740
60. S. Feller, C. Brown, D. Nizza, and K. Gawrisch Nuclear overhauser enhancement spectroscopy cross-relaxation rates and ethanol distribution across membranes Biophys. J. 82 2002 1396 1404
61. M. Patra, E. Salonen, E. Terama, I. Vattulainen, R. Faller, B. Lee, J. Holopainen, and M. Karttunen Under the influence of alcohol: the effect of ethanol and methanol on lipid bilayers Biophys. J. 90 2006 1121 1135
62. M. Kaye, K. Schmalzl, V.C. Nibali, M. Tarek, and M. Rheinstädter Ethanol enhances collective dynamics of lipid membranes Phys. Rev. E 83 2011 (05097-1-4)
63. T. Sirk, E. Brown, A. Sum, and M. Friedman Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes J. Agric. Food Chem. 56 2008 7750 7758
64. T. Sirk, E. Brown, M. Friedman, and A. Sum Molecular binding of catechins to biomembranes: relationship to biological activity J. Agric. Food Chem. 57 2009 6720 6728
65. M. Pickholz, L. Saiz, and M. Klein Concentration effects of volatile anesthetics on the properties of model membranes: a coarse-grain approach Biophys. J. 88 2005 1524 1534
66. L. Koubi, M. Tarek, M. Klein, and D. Scharf Distribution of halothane in a dipalmitoylphosphatidylcholine bilayer from molecular dynamics calculations Biophys. J. 78 2000 800 811
67. P. Tang, and Y. Xu Large-scale molecular dynamics simulations of general anesthetic effects on the ion channel in the fully hydrated membrane: the implication of molecular mechanisms of general anesthesia Proc. Natl. Acad. Sci. U.S.A. 99 2002 16035 16040
68. S. Vemparala, L. Saiz, R. Eckenhoff, and M. Klein Partitioning of anesthetics into a lipid bilayer and their interaction with membrane-bound peptide bundles Biophys. J. 91 2006 2815 2825
69. L. Stimson, I. Vattulainen, T. Róg, and M. Karttunen Exploring the effect of xenon on biomembranes Cell. Mol. Biol. Lett. 10 2005 563 569
70. E. Yamamoto, T. Akimoto, H. Shimizu, Y. Hirano, M. Yasui, and K. Yasuoka Diffusive nature of xenon anesthetic changes properties of a lipid bilayer: molecular dynamics simulations J. Phys. Chem. B 116 2012 8989 8995
71. K.M. Tu, N. Matubayasi, K.K. Liang, I.T. Todorov, S.L. Chan, and P.-L. Chau A possible molecular mechanism for the pressure reversal of general anaesthetics: aggregation of halothane in POPC bilayers at high pressure Chem. Phys. Lett. 543 2012 148 154
72. M. Darvas, P. Hoang, S. Picaud, M. Sega, and P. Jedlovszky Anesthetic molecules embedded in a lipid membrane: a computer simulation study Phys. Chem. Chem. Phys. 14 2012 12956 12969
73. S.C. Cullen, E.I. Eger, B.F. Cullen, and P. Gregory Observations on the anesthetic effect of the combination of xenon and halothane Anesthesiology 31 1969 305 309
74. O. Berger, O. Edholm, and F. Jähnig Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature Biophys. J. 72 1997 2002 2013
75. H. Berendsen, J. Postma, W. van Gunsteren, and J. Hermans Intermolecular Forces 1981 Reidel Dordrecht
76. J. Hirschfelder, C. Curtiss, and R. Bird Molecular Theory of Gases and Liquids 1954 John Wiley & Sons, Inc. New York
77. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
78. H. Berendsen, J. Postma, W. van Gunsteren, and J. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 3690
79. J. Silvius Thermotropic Phase Transitions of Pure Lipids in Model Membranes and Their Modifications by Membrane Proteins 1982 John Wiley & Sons, Inc. New York
80. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an nlog(n) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
81. U. Essmann, L. Perera, M. Berkowitz, T. Darden, H. Lee, and L. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
82. B. Hess, H. Bekker, H.J.C. Berendsen, and J.G.E.M. Fraaije LINCS: a linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
83. D.P. Tieleman, S.J. Marrink, and H.J. Berendsen A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems Biochim. Biophys. Acta 1331 1997 235 270
84. M. Alwarawrah, J. Dai, and J. Huang A molecular view of the cholesterol condensing effect in DOPC lipid bilayers J. Phys. Chem. B 114 2010 7516 7523
85. R. Booker, C. Koh, E. Sloan, A. Sum, E. Shalaev, and S. Singh Xenon hydrate dissociation measurements with model protein systems J. Phys. Chem. B 115 2011 10270 10276
86. O.H. Ollila, H.J. Risselada, M. Louhivuori, E. Lindahl, I. Vattulainen, and S.J. Marrink 3D pressure field in lipid membranes and membrane-protein complexes Phys. Rev. Lett. 102 2009 1 4
87. O.H. Ollila, M. Hyvonen, and I. Vattulainen Polyunsaturation in lipid membranes: dynamic properties and lateral pressure profiles J. Phys. Chem. B 111 2007 3139 3150
88. M. Jain, and N. Wu Effect of small molecules on the dipalmitoyl lecithin liposomal bilayer: III. Phase transition in lipid bilayer J. Membr. Biol. 34 1977 157 201
89. R. Batchelor, C.J. Windle, S. Buchoux, and M. Lorch Cholesterol and lipid phases influence the interactions between serotonin receptor agonists and lipid bilayers J. Biol. Chem. 285 2010 41402 41411
90. J.R. Trudell, D.G. Payan, J.H. Chin, and E.N. Cohen The antagonistic effect of an inhalation anesthetic and high pressure on the phase diagram of mixed dipalmitoyl-dimyristoylphosphatidylcholine bilayers Proc. Natl. Acad. Sci. U.S.A. 72 1975 210 213
91. D.B. Mountcastle, R.L. Biltonen, and M.J. Halsey Effect of anesthetics and pressure on the thermotropic behavior of multilamellar dipalmitoylphosphatidylcholine liposomes Proc. Natl. Acad. Sci. U.S.A. 75 1978 4906 4910
92. J. Nagle Theory of lipid monolayer and bilayer phase transitions: effect of headgroup interactions J. Membr. Biol. 27 1976 233 250
93. D. Marsh, A. Watts, and P.F. Knowles Cooperativity of the phase transition in single- and multibilayer lipid vesicles Biochim. Biophys. Acta 465 1977 500 514
94. B.R. Cater, D. Chapman, S.M. Hawes, and J. Saville Lipid phase transitions and drug interactions Biochim. Biophys. Acta 363 1974 54 69
95. J.H. Chin, J.R. Trudell, and E.N. Cohen The compression-ordering and solubility-disordering effects of high pressure gases on phospholipid bilayers Life Sci. 18 1976 489 497
96. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
97. R.S. Cantor Breaking the Meyer-Overton rule: predicted effects of varying stiffness and interfacial activity on the intrinsic potency of anesthetics Biophys. J. 80 2001 2284 2297
98. B. Harris, E. Moody, and P. Skolnick Isoflurane anesthesia is stereoselective Eur. J. Anaesthesiol. 217 1992 215 216
99. G.S. Lysko, J.L. Robinson, R. Castro, and R.A. Ferrone The stereospecific effects of isoflurane isomers in vivo Eur. J. Anaesthesiol. 263 1994 25 29
100. R. Dickinson, N.P. Franks, and W.R. Lieb Can the stereoselective effects of the anesthetic isoflurane be accounted for by lipid solubility? Biophys. J. 66 1994 2019 2023