Advertisement

Water and Lipid Bilayers

  • Jonathan D. NickelsEmail author
  • John KatsarasEmail author
Part of the Subcellular Biochemistry book series (SCBI, volume 71)

Abstract

Water is crucial to the structure and function of biological membranes. In fact, the membrane’s basic structural unit, i.e. the lipid bilayer, is self-assembled and stabilized by the so-called hydrophobic effect, whereby lipid molecules unable to hydrogen bond with water aggregate in order to prevent their hydrophobic portions from being exposed to water. However, this is just the beginning of the lipid-bilayer-water relationship. This mutual interaction defines vesicle stability in solution, controls small molecule permeation, and defines the spacing between lamella in multi-lamellar systems, to name a few examples. This chapter will describe the structural and dynamical properties central to these, and other water- lipid bilayer interactions.

Keywords

Permeation Water distribution Dynamics 

Notes

Acknowledgments

Support for the authors was received from the Department of Energy (DOE), Scientific User Facilities Division, Office of Basic Energy Sciences (BES) through Oak Ridge National Laboratory (ORNL), which is managed by UT-Battelle, LLC, for the U.S. DOE under contract no. DE-AC05-00OR2275. JDN was partially supported through EPSCoR grant no. DEFG02-08ER46528.

References

  1. Ackerman DG, Heberle FA, Feigenson GW (2013) Limited perturbation of a DPPC bilayer by fluorescent lipid probes: a molecular dynamics study. J Phys Chem B 117(17):4844–4852PubMedCentralPubMedCrossRefGoogle Scholar
  2. Al-Awqati Q (1999) One hundred years of membrane permeability: does Overton still rule? Nat Cell Biol 1(8):E201–E202PubMedCrossRefGoogle Scholar
  3. Almeida PF, Vaz WL, Thompson T (1992) Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry 31(29):6739–6747PubMedCrossRefGoogle Scholar
  4. Åman K, Lindahl E, Edholm O et al (2003) Structure and dynamics of interfacial water in an L α phase lipid bilayer from molecular dynamics simulations. Biophys J 84(1):102–115PubMedCentralPubMedCrossRefGoogle Scholar
  5. Armstrong BD, Han S (2009) Overhauser dynamic nuclear polarization to study local water dynamics. J Am Chem Soc 131(13):4641–4647PubMedCrossRefGoogle Scholar
  6. Auer B, Kumar R, Schmidt J et al (2007) Hydrogen bonding and Raman, IR, and 2D-IR spectroscopy of dilute HOD in liquid D2O. Proc Natl Acad Sci 104(36):14215–14220PubMedCentralPubMedCrossRefGoogle Scholar
  7. Balasubramanian S, Pal S, Bagchi B (2002) Hydrogen-bond dynamics near a micellar surface: origin of the universal slow relaxation at complex aqueous interfaces. Phys Rev Lett 89(11):115505PubMedCrossRefGoogle Scholar
  8. Bee M (1988) Quasielastic neutron scattering: principles and applications in solid state chemistry, biology, and materials science. Adam Hilger, BristolGoogle Scholar
  9. Bemporad D, Essex JW, Luttmann C (2004) Permeation of small molecules through a lipid bilayer: a computer simulation study. J Phys Chem B 108(15):4875–4884CrossRefGoogle Scholar
  10. Bernal J, Fowler R (1933) A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions. J Chem Phys 1(8):515–548CrossRefGoogle Scholar
  11. Binder H (2007) Water near lipid membranes as seen by infrared spectroscopy. Eur Biophys J 36(4–5):265–279PubMedCrossRefGoogle Scholar
  12. Böckmann RA, Hac A, Heimburg T et al (2003) Effect of sodium chloride on a lipid bilayer. Biophys J 85(3):1647–1655PubMedCentralPubMedCrossRefGoogle Scholar
  13. Büldt G, Gally H, Seelig A et al (1978) Neutron diffraction studies on selectively deuterated phospholipid bilayers. Nature 271(5641):182–184PubMedCrossRefGoogle Scholar
  14. Cevc G (1991) Hydration force and the interfacial structure of the polar surface. J Chem Soc Faraday Trans 87(17):2733–2739CrossRefGoogle Scholar
  15. Chen S, Liao C, Huang H et al (2001) Collective dynamics in fully hydrated phospholipid bilayers studied by inelastic X-ray scattering. Phys Rev Lett 86(4):740PubMedCrossRefGoogle Scholar
  16. De Groot BL, Grubmüller H (2001) Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science 294(5550):2353–2357PubMedCrossRefGoogle Scholar
  17. Deamer DW, Bramhall J (1986) Permeability of lipid bilayers to water and ionic solutes. Chem Phys Lipids 40(2–4):167–188PubMedCrossRefGoogle Scholar
  18. Debnath A, Ayappa KG, Maiti PK (2013) Simulation of influence of bilayer melting on dynamics and thermodynamics of interfacial water. Phys Rev Lett 110(1):018303PubMedCrossRefGoogle Scholar
  19. Debye P, Hückel E (1923) De la theorie des electrolytes. I. abaissement du point de congelation et phenomenes associes. Phys Z 24(9):185–206Google Scholar
  20. Devaux P, Mcconnell H (1972) Lateral diffusion in spin-labeled phosphatidylcholine multilayers. J Am Chem Soc 94(13):4475–4481PubMedCrossRefGoogle Scholar
  21. Disalvo E, Lairion F, Martini F et al (2008) Structural and functional properties of hydration and confined water in membrane interfaces. Biochim Biophys Acta Biomembr 1778(12):2655–2670CrossRefGoogle Scholar
  22. Doyle DA, Cabral JM, Pfuetzner RA et al (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280(5360):69–77PubMedCrossRefGoogle Scholar
  23. Fecko CJ, Eaves JD, Loparo JJ et al (2003) Ultrafast hydrogen-bond dynamics in the infrared spectroscopy of water. Science 301(5640):1698–1702PubMedCrossRefGoogle Scholar
  24. Fenimore PW, Frauenfelder H, Mcmahon BH et al (2002) Slaving: solvent fluctuations dominate protein dynamics and functions. Proc Natl Acad Sci 99(25):16047–16051PubMedCentralPubMedCrossRefGoogle Scholar
  25. Filippov A, Orädd G, Lindblom G (2003) Influence of cholesterol and water content on phospholipid lateral diffusion in bilayers. Langmuir 19(16):6397–6400CrossRefGoogle Scholar
  26. Finer EG, Darke A (1974) Phospholipid hydration studied by deuteron magnetic resonance spectroscopy. Chem Phys Lipids 12(1):1–16PubMedCrossRefGoogle Scholar
  27. Finkelstein A (1976) Water and nonelectrolyte permeability of lipid bilayer membranes. J Gen Physiol 68(2):127–135PubMedCrossRefGoogle Scholar
  28. Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes: theory and reality. Wiley, New YorkGoogle Scholar
  29. Fitter J, Lechner RE, Dencher NA (1999) Interactions of hydration water and biological membranes studied by neutron scattering. J Phys Chem B 103(38):8036–8050CrossRefGoogle Scholar
  30. Frank HS, Wen W-Y (1957) Ion-solvent interaction. Structural aspects of ion-solvent interaction in aqueous solutions: a suggested picture of water structure. Discuss Faraday Soc 24(0):133–140CrossRefGoogle Scholar
  31. Gaede HC, Gawrisch K (2003) Lateral diffusion rates of lipid, water, and a hydrophobic drug in a multilamellar liposome. Biophys J 85(3):1734–1740PubMedCentralPubMedCrossRefGoogle Scholar
  32. Gawrisch K, Ruston D, Zimmerberg J et al (1992) Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. Biophys J 61(5):1213–1223PubMedCentralPubMedCrossRefGoogle Scholar
  33. Ghosh A, Smits M, Bredenbeck J et al (2007) Membrane-bound water is energetically decoupled from nearby bulk water: an ultrafast surface-specific investigation. J Am Chem Soc 129(31):9608–9609PubMedCrossRefGoogle Scholar
  34. Griffith OH, Dehlinger PJ, Van SP (1974) Shape of the hydrophobic barrier of phospholipid bilayers (evidence for water penetration in biological membranes). J Membr Biol 15(1):159–192PubMedCrossRefGoogle Scholar
  35. Halle B (2004) Protein hydration dynamics in solution: a critical survey. Philos Trans R Soc Lond B Biol Sci 359(1448):1207–1224PubMedCentralPubMedCrossRefGoogle Scholar
  36. Hanai T, Haydon D (1966) The permeability to water of bimolecular lipid membranes. J Theor Biol 11(3):370–382PubMedCrossRefGoogle Scholar
  37. Heberle FA, Petruzielo RS, Pan J et al (2013) Bilayer thickness mismatch controls domain size in model membranes. J Am Chem Soc 135(18):6853–6859PubMedCrossRefGoogle Scholar
  38. Helfrich W, Servuss R-M (1984) Undulations, steric interaction and cohesion of fluid membranes. Il Nuovo Cimento D 3(1):137–151CrossRefGoogle Scholar
  39. Ishai PB, Mamontov E, Nickels JD et al (2013) Influence of ions on water diffusion—a neutron scattering study. J Phys Chem B 117(25):7725–7729Google Scholar
  40. Israelachvili JN (2011) Intermolecular and surface forces: revised third edition. Academic, LondonGoogle Scholar
  41. Jansen M, Blume A (1995) A comparative study of diffusive and osmotic water permeation across bilayers composed of phospholipids with different head groups and fatty acyl chains. Biophys J 68(3):997–1008PubMedCentralPubMedCrossRefGoogle Scholar
  42. Jorgensen WL, Chandrasekhar J, Madura JD et al (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79(2):926–935CrossRefGoogle Scholar
  43. Katsaras J (1995) Structure of the subgel (Lc′) and Gel (L. beta’.) phases of oriented dipalmitoylphosphatidylcholine multibilayers. J Phys Chem 99(12):4141–4147CrossRefGoogle Scholar
  44. Katsaras J (1997) Highly aligned lipid membrane systems in the physiologically relevant “excess water” condition. Biophys J 73(6):2924–2929PubMedCentralPubMedCrossRefGoogle Scholar
  45. Katsaras J, Tristram-Nagle S, Liu Y et al (2000) Clarification of the ripple phase of lecithin bilayers using fully hydrated, aligned samples. Phys Rev E 61(5):5668–5677CrossRefGoogle Scholar
  46. Kausik R, Han S (2011) Dynamics and state of lipid bilayer-internal water unraveled with solution state 1H dynamic nuclear polarization. Phys Chem Chem Phys 13(17):7732–7746PubMedCrossRefGoogle Scholar
  47. Kedem OT, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246PubMedCrossRefGoogle Scholar
  48. Kolano C, Helbing J, Kozinski M et al (2006) Watching hydrogen-bond dynamics in a beta-turn by transient two-dimensional infrared spectroscopy. Nature 444(7118):469–472PubMedCrossRefGoogle Scholar
  49. König S, Sackmann E, Richter D et al (1994) Molecular dynamics of water in oriented DPPC multilayers studied by quasielastic neutron scattering and deuterium‐nuclear magnetic resonance relaxation. J Chem Phys 100:3307CrossRefGoogle Scholar
  50. Kornyshev A, Leikin S (1989) Fluctuation theory of hydration forces: the dramatic effects of inhomogeneous boundary conditions. Phys Rev A 40(11):6431PubMedCrossRefGoogle Scholar
  51. Kučerka N, Nagle JF, Feller SE et al (2004) Models to analyze small-angle neutron scattering from unilamellar lipid vesicles. Phys Rev E 69(5):051903CrossRefGoogle Scholar
  52. Kučerka N, Tristram-Nagle S, Nagle J (2006) Structure of fully hydrated fluid phase lipid bilayers with monounsaturated chains. J Membr Biol 208(3):193–202CrossRefGoogle Scholar
  53. Kučerka N, Nagle JF, Sachs JN et al (2008a) Lipid bilayer structure determined by the simultaneous analysis of neutron and X-ray scattering data. Biophys J 95(5):2356–2367PubMedCentralPubMedCrossRefGoogle Scholar
  54. Kučerka N, Papp-Szabo E, Nieh M-P et al (2008b) Effect of cations on the structure of bilayers formed by lipopolysaccharides isolated from pseudomonas aeruginosa PAO1. J Phys Chem B 112(27):8057–8062PubMedCrossRefGoogle Scholar
  55. Laage D, Hynes JT (2006) A molecular jump mechanism of water reorientation. Science 311(5762):832–835PubMedCrossRefGoogle Scholar
  56. Laage D, Stirnemann G, Hynes JT (2009) Why water reorientation slows without iceberg formation around hydrophobic solutes. J Phys Chem B 113(8):2428–2435PubMedCrossRefGoogle Scholar
  57. Leikin S, Parsegian VA, Rau DC et al (1993) Hydration forces. Annu Rev Phys Chem 44(1):369–395PubMedCrossRefGoogle Scholar
  58. Lelkes P, Miller I (1980) Perturbations of membrane structure by optical probes: I. Location and structural sensitivity of merocyanine 540 bound to phospholipid membranes. J Membr Biol 52(1):1–15PubMedCrossRefGoogle Scholar
  59. Leontiadou H, Mark AE, Marrink SJ (2004) Molecular dynamics simulations of hydrophilic pores in lipid bilayers. Biophys J 86(4):2156–2164PubMedCentralPubMedCrossRefGoogle Scholar
  60. Marčelja S, Radić N (1976) Repulsion of interfaces due to boundary water. Chem Phys Lett 42(1):129–130CrossRefGoogle Scholar
  61. Marchi M, Sterpone F, Ceccarelli M (2002) Water rotational relaxation and diffusion in hydrated lysozyme. J Am Chem Soc 124(23):6787–6791PubMedCrossRefGoogle Scholar
  62. Marrink S-J, Berendsen HJ (1994) Simulation of water transport through a lipid membrane. J Phys Chem 98(15):4155–4168CrossRefGoogle Scholar
  63. Marsh D (2002) Membrane water-penetration profiles from spin labels. Eur Biophys J 31(7):559–562PubMedCrossRefGoogle Scholar
  64. Mathai JC, Tristram-Nagle S, Nagle JF et al (2008) Structural determinants of water permeability through the lipid membrane. J Gen Physiol 131(1):69–76PubMedCentralPubMedCrossRefGoogle Scholar
  65. Mazur K, Heisler IA, Meech SR (2010) Ultrafast dynamics and hydrogen-bond structure in aqueous solutions of model peptides. J Phys Chem B 114(32):10684–10691PubMedCrossRefGoogle Scholar
  66. Mcintosh TJ, Simon SA (1986) Area per molecule and distribution of water in fully hydrated dilauroylphosphatidylethanolamine bilayers. Biochemistry 25(17):4948–4952PubMedCrossRefGoogle Scholar
  67. Mcintosh TJ, Simon SA (1994) Hydration and steric pressures between phospholipid bilayers. Annu Rev Biophys Biomol Struct 23(1):27–51PubMedCrossRefGoogle Scholar
  68. Murata K, Mitsuoka K, Hirai T et al (2000) Structural determinants of water permeation through aquaporin-1. Nature 407(6804):599–605PubMedCrossRefGoogle Scholar
  69. Murzyn K, Zhao W, Karttunen M et al (2006) Dynamics of water at membrane surfaces: effect of headgroup structure. Biointerphases 1(3):98–105PubMedCrossRefGoogle Scholar
  70. Nagata Y, Mukamel S (2010) Vibrational Sum-frequency generation spectroscopy at the water/lipid interface: molecular dynamics simulation study. J Am Chem Soc 132(18):6434–6442PubMedCentralPubMedCrossRefGoogle Scholar
  71. Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta Rev Biomembr 1469(3):159–195CrossRefGoogle Scholar
  72. Nagle JF, Wiener MC (1988) Structure of fully hydrated bilayer dispersions. Biochim Biophys Acta Biomembr 942(1):1–10CrossRefGoogle Scholar
  73. Nagle JF, Zhang R, Tristram-Nagle S et al (1996) X-ray structure determination of fully hydrated L alpha phase dipalmitoylphosphatidylcholine bilayers. Biophys J 70(3):1419–1431PubMedCentralPubMedCrossRefGoogle Scholar
  74. Nagle JF, Mathai JC, Zeidel ML et al (2008) Theory of passive permeability through lipid bilayers. J Gen Physiol 131(1):77–85PubMedCentralPubMedCrossRefGoogle Scholar
  75. Nickels JD, O’Neill H, Hong L, et al (2012) Dynamics of protein and its hydration water: neutron scattering studies on fully deuterated GFP. Biophys J 103(7):1566–1575.Google Scholar
  76. Overton E (1899) Ueber die osmotischen Eigenshaften der Zelle in ihrer Bedeutung Fur die Toxikologie und Pharmakologie. Vierteljahrsschr Naturforsch Ges Zurich 44:88–135Google Scholar
  77. Parsegian VA, Rand RP (1991) On molecular protrusion as the source of hydration forces. Langmuir 7(6):1299–1301CrossRefGoogle Scholar
  78. Pasenkiewicz-Gierula M, Takaoka Y, Miyagawa H et al (1997) Hydrogen bonding of water to phosphatidylcholine in the membrane as studied by a molecular dynamics simulation: location, geometry, and lipid-lipid bridging via hydrogen-bonded water. J Phys Chem A 101(20):3677–3691CrossRefGoogle Scholar
  79. Paula S, Volkov AG, Van Hoek AN et al (1996) Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 70(1):339–348PubMedCentralPubMedCrossRefGoogle Scholar
  80. Perticaroli S, Comez L, Paolantoni M et al (2011) Extended frequency range depolarized light scattering study of N-acetyl-leucine-methylamide–water solutions. J Am Chem Soc 133(31):12063–12068PubMedCrossRefGoogle Scholar
  81. Perticaroli S, Nakanishi M, Pashkovski E et al (2013) Dynamics of hydration water in sugars and peptides solutions. J Phys Chem B 117(25):7729–7736PubMedCrossRefGoogle Scholar
  82. Petrache HI, Feller SE, Nagle JF (1997) Determination of component volumes of lipid bilayers from simulations. Biophys J 72(5):2237–2242PubMedCentralPubMedCrossRefGoogle Scholar
  83. Pfeiffer W, Henkel T, Sackmann E et al (1989) Local dynamics of lipid bilayers studied by incoherent quasi-elastic neutron scattering. EPL Europhys Lett 8(2):201CrossRefGoogle Scholar
  84. Raghunathan V, Katsaras J (1995) Structure of the Lc′ phase in a hydrated lipid multilamellar system. Phys Rev Lett 74(22):4456PubMedCrossRefGoogle Scholar
  85. Rand R, Parsegian V (1989) Hydration forces between phospholipid bilayers. Biochim Biophys Acta Rev Biomembr 988(3):351–376CrossRefGoogle Scholar
  86. Rheinstädter MC (2012) Lipid membrane dynamics. Dynamics of soft matter. Springer, New York, USA, pp 263–286Google Scholar
  87. Rheinstädter MC, Ollinger C, Fragneto G et al (2004) Collective dynamics of lipid membranes studied by inelastic neutron scattering. Phys Rev Lett 93(10):108107PubMedCrossRefGoogle Scholar
  88. Rheinstädter MC, Seydel T, Demmel F et al (2005) Molecular motions in lipid bilayers studied by the neutron backscattering technique. Phy Rev E 71(6):061908CrossRefGoogle Scholar
  89. Sears VF (1992) Neutron scattering lengths and cross sections. Neutron News 3(3):26–37CrossRefGoogle Scholar
  90. Seelig J (1977) Deuterium magnetic resonance: theory and application to lipid membranes. Q Rev Biophys 10(3):353–418PubMedCrossRefGoogle Scholar
  91. Settles M, Doster W (1996) Anomalous diffusion of adsorbed water: a neutron scattering study of hydrated myoglobin. Faraday Discuss 103:269–279CrossRefGoogle Scholar
  92. Sirota EB, Smith GS, Safinya CR et al (1988) X-ray scattering studies of aligned, stacked surfactant membranes. Science 242(4884):1406–1409PubMedCrossRefGoogle Scholar
  93. Subczynski WK, Wisniewska A, Yin J-J et al (1994) Hydrophobic barriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol. Biochemistry 33(24):7670–7681PubMedCrossRefGoogle Scholar
  94. Sui H, Han B-G, Lee JK et al (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414(6866):872–878PubMedCrossRefGoogle Scholar
  95. Swenson J, Kargl F, Berntsen P et al (2008) Solvent and lipid dynamics of hydrated lipid bilayers by incoherent quasielastic neutron scattering. J Chem Phys 129:045101PubMedCrossRefGoogle Scholar
  96. Taschin A, Bartolini P, Eramo R et al (2013) Evidence of two distinct local structures of water from ambient to supercooled conditions. Nat Commun 4Google Scholar
  97. Tepper HL, Voth GA (2005) Protons may leak through pure lipid bilayers via a concerted mechanism. Biophys J 88(5):3095–3108PubMedCentralPubMedCrossRefGoogle Scholar
  98. Tielrooij KJ, Paparo D, Piatkowski L et al (2009) Dielectric relaxation dynamics of water in model membranes probed by terahertz spectroscopy. Biophys J 97(9):2484–2492PubMedCentralPubMedCrossRefGoogle Scholar
  99. Tielrooij K, Garcia-Araez N, Bonn M et al (2010) Cooperativity in ion hydration. Science 328(5981):1006–1009PubMedCrossRefGoogle Scholar
  100. Torre R, Bartolini P, Righini R (2004) Structural relaxation in supercooled water by time-resolved spectroscopy. Nature 428(6980):296–299PubMedCrossRefGoogle Scholar
  101. Träuble H (1971) The movement of molecules across lipid membranes: a molecular theory. J Membr Biol 4(1):193–208PubMedCrossRefGoogle Scholar
  102. Tristram-Nagle S, Petrache HI, Nagle JF (1998) Structure and interactions of fully hydrated dioleoylphosphatidylcholine bilayers. Biophys J 75(2):917–925PubMedCentralPubMedCrossRefGoogle Scholar
  103. Ulrich AS, Watts A (1994) Molecular response of the lipid headgroup to bilayer hydration monitored by 2H-NMR. Biophys J 66(5):1441–1449PubMedCentralPubMedCrossRefGoogle Scholar
  104. Verwey EJW, Overbeek JTG, Van Nes K (1948) Theory of the stability of lyophobic colloids: the interaction of sol particles having an electric double layer. Elsevier, New YorkGoogle Scholar
  105. Victor KG, Korb J-P, Bryant RG (2013) Translational dynamics of water at the phospholipid interface. J Phys Chem B 117(41):12475–12478PubMedCrossRefGoogle Scholar
  106. Volke F, Eisenblätter S, Galle J et al (1994) Dynamic properties of water at phosphatidylcholine lipid-bilayer surfaces as seen by deuterium and pulsed field gradient proton NMR. Chem Phys Lipids 70(2):121–131PubMedCrossRefGoogle Scholar
  107. Volkov VV, Palmer DJ, Righini R (2007) Heterogeneity of water at the phospholipid membrane interface. J Phys Chem B 111(6):1377–1383PubMedCrossRefGoogle Scholar
  108. Wassall SR (1996) Pulsed field gradient-spin echo NMR studies of water diffusion in a phospholipid model membrane. Biophys J 71(5):2724–2732PubMedCentralPubMedCrossRefGoogle Scholar
  109. Watson MC, Brown FL (2010) Interpreting membrane scattering experiments at the mesoscale: the contribution of dissipation within the bilayer. Biophys J 98(6):L9–L11PubMedCentralPubMedCrossRefGoogle Scholar
  110. Wood K, Plazanet M, Gabel F et al (2007) Coupling of protein and hydration-water dynamics in biological membranes. Proc Natl Acad Sci 104(46):18049–18054PubMedCentralPubMedCrossRefGoogle Scholar
  111. Woodka AC, Butler PD, Porcar L et al (2012) Lipid bilayers and membrane dynamics: insight into thickness fluctuations. Phys Rev Lett 109(5):058102PubMedCrossRefGoogle Scholar
  112. Xiang T-X, Anderson BD (1998) Influence of chain ordering on the selectivity of dipalmitoylphosphatidylcholine bilayer membranes for permeant size and shape. Biophys J 75(6):2658–2671PubMedCentralPubMedCrossRefGoogle Scholar
  113. Yi Z, Nagao M, Bossev DP (2009) Bending elasticity of saturated and monounsaturated phospholipid membranes studied by the neutron spin echo technique. J Phys Condens Matter 21:155104PubMedCrossRefGoogle Scholar
  114. Zaccai G, Blasie J, Schoenborn B (1975) Neutron diffraction studies on the location of water in lecithin bilayer model membranes. Proc Natl Acad Sci 72(1):376–380PubMedCentralPubMedCrossRefGoogle Scholar
  115. Zhou F, Schulten K (1995) Molecular dynamics study of a membrane-water interface. J Phys Chem 99(7):2194–2207CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Joint Institute for Neutron SciencesOak Ridge National LaboratoryOak RidgeUSA
  2. 2.Biology & Soft Matter and Biosciences DivisionOak Ridge National LaboratoryOak RidgeUSA

Personalised recommendations