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Structure and Fluctuations of Charged Phosphatidylserine Bilayers in the Absence of Salt

Horia I. Petrache ^*, Stephanie Tristram-Nagle , Klaus Gawrisch , Daniel Harries ^*, V. Adrian Parsegian ^* and John F. Nagle 

^* Laboratory of Physical and Structural Biology, The National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland; Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania; Laboratory of Membrane Biochemistry and Biophysics, The National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, Maryland; and Department of Physics, Carnegie Mellon University, Pittsburgh, Pennsylvania

Correspondence: Address reprint requests to Dr. Horia I. Petrache, National Institutes of Health, Bldg. 9, Rm. 1E116, Bethesda, MD 20892. Tel.: 301-402-7797; E-mail: horia{at}helix.nih.gov.

Using x-ray diffraction and NMR spectroscopy, we present structural and material properties of phosphatidylserine (PS) bilayers that may account for the well documented implications of PS headgroups in cell activity. At 30°C, the 18-carbon monounsaturated DOPS in the fluid state has a cross-sectional area of 65.3 Ų which is remarkably smaller than the area 72.5 Ų of the DOPC analog, despite the extra electrostatic repulsion expected for charged PS headgroups. Similarly, at 20°C, the 14-carbon disaturated DMPS in the gel phase has an area of 40.8 Ų vs. 48.1 Ų for DMPC. This condensation of area suggests an extra attractive interaction, perhaps hydrogen bonding, between PS headgroups. Unlike zwitterionic lipids, stacks of PS bilayers swell indefinitely as water is added. Data obtained for osmotic pressure versus interbilayer water spacing for fluid phase DOPS are well fit by electrostatic interactions calculated for the Gouy-Chapman regime. It is shown that the electrostatic interactions completely dominate the fluctuational pressure. Nevertheless, the x-ray data definitively exhibit the effects of fluctuations in fluid phase DOPS. From our measurements of fluctuations, we obtain the product of the bilayer bending modulus K_C and the smectic compression modulus B. At the same interbilayer separation, the interbilayer fluctuations are smaller in DOPS than for DOPC, showing that B and/or K_C are larger. Complementing the x-ray data, ³¹P-chemical shift anisotropy measured by NMR suggest that the DOPS headgroups are less sensitive to osmotic pressure than DOPC headgroups, which is consistent with a larger K_C in DOPS. Quadrupolar splittings for D₂O decay less rapidly with increasing water content for DOPS than for DOPC, indicating greater perturbation of interlamellar water and suggesting a greater interlamellar hydration force in DOPS. Our comparisons between bilayers of PS and PC lipids with the same chains and the same temperature enable us to focus on the effects of these headgroups on bilayer properties.

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