Abstract
The comparative effect of cholesterol (CH) versus cholesterol sulfate (CS) on dimyristoylphosphatidylcholine (DMPC) membranes has been investigated by optical microscopy, freeze-fracture electron microscopy, x-ray diffraction, and solid state 2H and 31P nuclear magnetic resonance (NMR). The sulfate analogue extends the lamellar phase domain toward high water contents, and substitution of 30 mol % CH by CS in DMPC lamellae induces the trapping of 30 wt % additional water. The greater swelling of the CS-containing systems is evidenced by determination of lamellar repeat distances at maximal hydration: 147 +/- 4 A and 64 +/- 2 A in the presence of CS and CH, respectively. 2H-NMR of heavy water demonstrates that CS binds approximately 12 more water molecules at the interface than CH whereas NMR of deuterium-labeled DMPC chains reveals that 30 mol % CS orders the membrane as 15 mol % CH at high temperature and disorders much more than CH at low temperatures. The various effects of CS versus CH are discussed by taking into account attractive Van der Waals forces and repulsive steric/electrostatic interactions of the negatively charged sulfate group.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Almeida P. F., Vaz W. L., Thompson T. E. Lateral diffusion in the liquid phases of dimyristoylphosphatidylcholine/cholesterol lipid bilayers: a free volume analysis. Biochemistry. 1992 Jul 28;31(29):6739–6747. doi: 10.1021/bi00144a013. [DOI] [PubMed] [Google Scholar]
- Bleau G., Bodley F. H., Longpré J., Chapdelaine A., Roberts K. D. Cholesterol sulfate. I. Occurrence and possible biological function as an amphipathic lipid in the membrane of the human erythrocyte. Biochim Biophys Acta. 1974 May 30;352(1):1–9. doi: 10.1016/0005-2736(74)90174-6. [DOI] [PubMed] [Google Scholar]
- Bourgès M., Small D. M., Dervichian D. G. Biophysics of lipidic associations. II. The ternary systems: cholesterol-lecithin-water. Biochim Biophys Acta. 1967 Feb 14;137(1):157–167. doi: 10.1016/0005-2760(67)90019-7. [DOI] [PubMed] [Google Scholar]
- Cheetham J. J., Chen R. J., Epand R. M. Interaction of calcium and cholesterol sulphate induces membrane destabilization and fusion: implications for the acrosome reaction. Biochim Biophys Acta. 1990 May 24;1024(2):367–372. doi: 10.1016/0005-2736(90)90366-v. [DOI] [PubMed] [Google Scholar]
- Cheetham J. J., Epand R. M., Andrews M., Flanagan T. D. Cholesterol sulfate inhibits the fusion of Sendai virus to biological and model membranes. J Biol Chem. 1990 Jul 25;265(21):12404–12409. [PubMed] [Google Scholar]
- Chiou J. S., Krishna P. R., Kamaya H., Ueda I. Alcohols dehydrate lipid membranes: an infrared study on hydrogen bonding. Biochim Biophys Acta. 1992 Oct 5;1110(2):225–233. doi: 10.1016/0005-2736(92)90363-q. [DOI] [PubMed] [Google Scholar]
- Cullis P. R., de Kruijff B. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta. 1979 Dec 20;559(4):399–420. doi: 10.1016/0304-4157(79)90012-1. [DOI] [PubMed] [Google Scholar]
- Davis J. H. Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys J. 1979 Sep;27(3):339–358. doi: 10.1016/S0006-3495(79)85222-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis J. H. The description of membrane lipid conformation, order and dynamics by 2H-NMR. Biochim Biophys Acta. 1983 Mar 21;737(1):117–171. doi: 10.1016/0304-4157(83)90015-1. [DOI] [PubMed] [Google Scholar]
- Douliez J. P., Léonard A., Dufourc E. J. Restatement of order parameters in biomembranes: calculation of C-C bond order parameters from C-D quadrupolar splittings. Biophys J. 1995 May;68(5):1727–1739. doi: 10.1016/S0006-3495(95)80350-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Engel A. K., Cowburn D. The origin of multiple quadrupole couplings in the deuterium NMR spectra of the 2 chain of 1,2 dipalmitoyl-sn-glycero-3-phosphorylcholine. FEBS Lett. 1981 Apr 20;126(2):169–171. doi: 10.1016/0014-5793(81)80233-5. [DOI] [PubMed] [Google Scholar]
- Epstein E. H., Jr, Williams M. L., Elias P. M. Steroid sulfatase, X-linked ichthyosis, and stratum corneum cell cohesion. Arch Dermatol. 1981 Dec;117(12):761–763. [PubMed] [Google Scholar]
- Fayrer-Hosken R. A., Brackett B. G., Brown J. Reversible inhibition of rabbit sperm-fertilizing ability by cholesterol sulfate. Biol Reprod. 1987 May;36(4):878–883. doi: 10.1095/biolreprod36.4.878. [DOI] [PubMed] [Google Scholar]
- Finer E. G., Darke A. Phospholipid hydration studied by deuteron magnetic resonace spectroscopy. Chem Phys Lipids. 1974 Feb;12(1):1–16. doi: 10.1016/0009-3084(74)90064-4. [DOI] [PubMed] [Google Scholar]
- Hui S. W., He N. B. Molecular organization in cholesterol-lecithin bilayers by X-ray and electron diffraction measurements. Biochemistry. 1983 Mar 1;22(5):1159–1164. doi: 10.1021/bi00274a026. [DOI] [PubMed] [Google Scholar]
- Ipsen J. H., Karlström G., Mouritsen O. G., Wennerström H., Zuckermann M. J. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta. 1987 Nov 27;905(1):162–172. doi: 10.1016/0005-2736(87)90020-4. [DOI] [PubMed] [Google Scholar]
- Ipsen J. H., Mouritsen O. G., Bloom M. Relationships between lipid membrane area, hydrophobic thickness, and acyl-chain orientational order. The effects of cholesterol. Biophys J. 1990 Mar;57(3):405–412. doi: 10.1016/S0006-3495(90)82557-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Israelachvili J. N., Mitchell D. J., Ninham B. W. Theory of self-assembly of lipid bilayers and vesicles. Biochim Biophys Acta. 1977 Oct 17;470(2):185–201. doi: 10.1016/0005-2736(77)90099-2. [DOI] [PubMed] [Google Scholar]
- Kitson N., Monck M., Wong K., Thewalt J., Cullis P. The influence of cholesterol 3-sulphate on phase behaviour and hydrocarbon order in model membrane systems. Biochim Biophys Acta. 1992 Oct 19;1111(1):127–133. doi: 10.1016/0005-2736(92)90282-q. [DOI] [PubMed] [Google Scholar]
- Lampe M. A., Burlingame A. L., Whitney J., Williams M. L., Brown B. E., Roitman E., Elias P. M. Human stratum corneum lipids: characterization and regional variations. J Lipid Res. 1983 Feb;24(2):120–130. [PubMed] [Google Scholar]
- Lampe M. A., Williams M. L., Elias P. M. Human epidermal lipids: characterization and modulations during differentiation. J Lipid Res. 1983 Feb;24(2):131–140. [PubMed] [Google Scholar]
- Langlais J., Zollinger M., Plante L., Chapdelaine A., Bleau G., Roberts K. D. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7266–7270. doi: 10.1073/pnas.78.12.7266. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lindblom G., Rilfors L., Hauksson J. B., Brentel I., Sjölund M., Bergenståhl B. Effect of head-group structure and counterion condensation on phase equilibria in anionic phospholipid-water systems studied by 2H, 23Na, and 31P NMR and X-ray diffraction. Biochemistry. 1991 Nov 12;30(45):10938–10948. doi: 10.1021/bi00109a019. [DOI] [PubMed] [Google Scholar]
- Léonard A., Dufourc E. J. Interactions of cholesterol with the membrane lipid matrix. A solid state NMR approach. Biochimie. 1991 Oct;73(10):1295–1302. doi: 10.1016/0300-9084(91)90092-f. [DOI] [PubMed] [Google Scholar]
- Marassi F. M., Macdonald P. M. Response of the headgroup of phosphatidylglycerol to membrane surface charge as studied by deuterium and phosphorus-31 nuclear magnetic resonance. Biochemistry. 1991 Oct 29;30(43):10558–10566. doi: 10.1021/bi00107a027. [DOI] [PubMed] [Google Scholar]
- McMullen T. P., McElhaney R. N. New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry. Biochim Biophys Acta. 1995 Mar 8;1234(1):90–98. doi: 10.1016/0005-2736(94)00266-r. [DOI] [PubMed] [Google Scholar]
- Mortensen K., Pfeiffer W., Sackmann E., Knoll W. Structural properties of a phosphatidylcholine-cholesterol system as studied by small-angle neutron scattering: ripple structure and phase diagram. Biochim Biophys Acta. 1988 Nov 22;945(2):221–245. doi: 10.1016/0005-2736(88)90485-3. [DOI] [PubMed] [Google Scholar]
- Oldfield E., Meadows M., Rice D., Jacobs R. Spectroscopic studies of specifically deuterium labeled membrane systems. Nuclear magnetic resonance investigation of the effects of cholesterol in model systems. Biochemistry. 1978 Jul 11;17(14):2727–2740. doi: 10.1021/bi00607a006. [DOI] [PubMed] [Google Scholar]
- Pebay-Peyroula E., Dufourc E. J., Szabo A. G. Location of diphenyl-hexatriene and trimethylammonium-diphenyl-hexatriene in dipalmitoylphosphatidylcholine bilayers by neutron diffraction. Biophys Chem. 1994 Dec;53(1-2):45–56. doi: 10.1016/0301-4622(94)00075-1. [DOI] [PubMed] [Google Scholar]
- Recktenwald D. J., McConnell H. M. Phase equilibria in binary mixtures of phosphatidylcholine and cholesterol. Biochemistry. 1981 Jul 21;20(15):4505–4510. doi: 10.1021/bi00518a042. [DOI] [PubMed] [Google Scholar]
- Roberts K. D. Sterol sulfates in the epididymis; synthesis and possible function in the reproductive process. J Steroid Biochem. 1987;27(1-3):337–341. doi: 10.1016/0022-4731(87)90325-6. [DOI] [PubMed] [Google Scholar]
- Salsbury N. J., Darke A., Chapman D. Deuteron magnetic resonance studies of water associated with phospholipids. Chem Phys Lipids. 1972 Mar;8(2):142–151. doi: 10.1016/0009-3084(72)90026-6. [DOI] [PubMed] [Google Scholar]
- Sankaram M. B., Thompson T. E. Modulation of phospholipid acyl chain order by cholesterol. A solid-state 2H nuclear magnetic resonance study. Biochemistry. 1990 Nov 27;29(47):10676–10684. doi: 10.1021/bi00499a015. [DOI] [PubMed] [Google Scholar]
- Scherer P. G., Seelig J. Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles. Biochemistry. 1989 Sep 19;28(19):7720–7728. doi: 10.1021/bi00445a030. [DOI] [PubMed] [Google Scholar]
- Siegenthaler U., Laine A., Polak L. Studies on contact sensitivity to chromium in the guinea pig. The role of valence in the formation of the antigenic determinant. J Invest Dermatol. 1983 Jan;80(1):44–47. doi: 10.1111/1523-1747.ep12531034. [DOI] [PubMed] [Google Scholar]
- Stockton G. W., Smith I. C. A deuterium nuclear magnetic resonance study of the condensing effect of cholesterol on egg phosphatidylcholine bilayer membranes. I. Perdeuterated fatty acid probes. Chem Phys Lipids. 1976 Oct;17(2-3):251–263. doi: 10.1016/0009-3084(76)90070-0. [DOI] [PubMed] [Google Scholar]
- Ulmius J., Wennerström H., Lindblom G., Arvidson G. Deuteron nuclear magnetic resonance studies of phase equilibria in a lecithin-water system. Biochemistry. 1977 Dec 27;16(26):5742–5745. doi: 10.1021/bi00645a014. [DOI] [PubMed] [Google Scholar]
- Ulrich A. S., Watts A. Molecular response of the lipid headgroup to bilayer hydration monitored by 2H-NMR. Biophys J. 1994 May;66(5):1441–1449. doi: 10.1016/S0006-3495(94)80934-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vist M. R., Davis J. H. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 1990 Jan 16;29(2):451–464. doi: 10.1021/bi00454a021. [DOI] [PubMed] [Google Scholar]
- Webster D., France J. T., Shapiro L. J., Weiss R. X-linked ichthyosis due to steroid-sulphatase deficiency. Lancet. 1978 Jan 14;1(8055):70–72. doi: 10.1016/s0140-6736(78)90005-3. [DOI] [PubMed] [Google Scholar]
- Yeagle P. L. Cholesterol and the cell membrane. Biochim Biophys Acta. 1985 Dec 9;822(3-4):267–287. doi: 10.1016/0304-4157(85)90011-5. [DOI] [PubMed] [Google Scholar]
- Zaccai G., Büldt G., Seelig A., Seelig J. Neutron diffraction studies on phosphatidylcholine model membranes. II. Chain conformation and segmental disorder. J Mol Biol. 1979 Nov 15;134(4):693–706. doi: 10.1016/0022-2836(79)90480-7. [DOI] [PubMed] [Google Scholar]