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. 2001 May;80(5):2327–2337. doi: 10.1016/S0006-3495(01)76203-0

Membrane properties of D-erythro-N-acyl sphingomyelins and their corresponding dihydro species.

M Kuikka 1, B Ramstedt 1, H Ohvo-Rekilä 1, J Tuuf 1, J P Slotte 1
PMCID: PMC1301422  PMID: 11325733

Abstract

We have prepared acyl chain-defined D-erythro-sphingomyelins and D-erythro-dihydrosphingomyelins and compared their properties in monolayer and bilayer membranes. Surface pressure/molecular area isotherms of D-erythro-N-16:0-sphingomyelin (16:0-SM) and D-erythro-N-16:0-dihydrosphingomyelin (16:0-DHSM) show very similar packing properties, except that the expanded-to-condensed phase transition (crystallization) occurs at a lower surface pressure for 16:0-DHSM. The measured surface potential was generally about 100 mV less for 16:0-DHSM monolayers compared to 16:0-SM monolayers. The condensed domains (crystals) that formed in 16:0-SM monolayers as a function of compression displayed star-shaped morphology when viewed under an epifluorescence microscope. 16:0-DHSM monolayers did not form similar crystals upon compression. 16:0-DHSM was degraded much faster by sphingomyelinase from Staphylococcus aureus than 16:0-SM (10-fold difference in enzyme activity needed for comparable hydrolytic rate). Cholesterol desorption from 16:0-DHSM to cyclodextrin was slightly slower (approximately 20%) than the rate measured from 16:0-SM monolayers (at 60 mol % cholesterol). The bilayer melting temperature of 16:0-DHSM was 47.7 degrees C (DeltaH 8.3 kcal/mol) whereas it was 41.2 degrees C for 16:0-SM (DeltaH 8.1 kcal/mol). Cholesterol/16:0-DHSM bilayers (15 mol % sterol) had more condensed domains than comparable 16:0-SM bilayers, as evidenced from the quenching resistance of DPH in DHSM membranes. We conclude that cholesterol interacts more favorably with 16:0-DHSM and that the membranes are more condensed than comparable 16:0-SM-containing membranes.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahmed S. N., Brown D. A., London E. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry. 1997 Sep 9;36(36):10944–10953. doi: 10.1021/bi971167g. [DOI] [PubMed] [Google Scholar]
  2. Barenholz Y., Suurkuusk J., Mountcastle D., Thompson T. E., Biltonen R. L. A calorimetric study of the thermotropic behavior of aqueous dispersions of natural and synthetic sphingomyelins. Biochemistry. 1976 Jun 1;15(11):2441–2447. doi: 10.1021/bi00656a030. [DOI] [PubMed] [Google Scholar]
  3. Borchman D., Byrdwell W. C., Yappert M. C. Thermodynamic phase transition parameters of human lens dihydrosphingomyelin. Ophthalmic Res. 1996;28 (Suppl 1):81–85. doi: 10.1159/000267977. [DOI] [PubMed] [Google Scholar]
  4. Brown R. E. Sphingolipid organization in biomembranes: what physical studies of model membranes reveal. J Cell Sci. 1998 Jan;111(Pt 1):1–9. doi: 10.1242/jcs.111.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Byrdwell W. C., Borchman D. Liquid chromatography/mass-spectrometric characterization of sphingomyelin and dihydrosphingomyelin of human lens membranes. Ophthalmic Res. 1997;29(4):191–206. doi: 10.1159/000268014. [DOI] [PubMed] [Google Scholar]
  6. Grainger D. W., Reichert A., Ringsdorf H., Salesse C. Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: direct observation of enzyme domain formation using fluorescence microscopy. Biochim Biophys Acta. 1990 Apr 30;1023(3):365–379. doi: 10.1016/0005-2736(90)90128-b. [DOI] [PubMed] [Google Scholar]
  7. Jungner M., Ohvo H., Slotte J. P. Interfacial regulation of bacterial sphingomyelinase activity. Biochim Biophys Acta. 1997 Feb 18;1344(3):230–240. doi: 10.1016/s0005-2760(96)00147-6. [DOI] [PubMed] [Google Scholar]
  8. Koval M., Pagano R. E. Intracellular transport and metabolism of sphingomyelin. Biochim Biophys Acta. 1991 Mar 12;1082(2):113–125. doi: 10.1016/0005-2760(91)90184-j. [DOI] [PubMed] [Google Scholar]
  9. Lange Y., Ramos B. V. Analysis of the distribution of cholesterol in the intact cell. J Biol Chem. 1983 Dec 25;258(24):15130–15134. [PubMed] [Google Scholar]
  10. Lange Y., Swaisgood M. H., Ramos B. V., Steck T. L. Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J Biol Chem. 1989 Mar 5;264(7):3786–3793. [PubMed] [Google Scholar]
  11. Li L. K., So L., Spector A. Membrane cholesterol and phospholipid in consecutive concentric sections of human lenses. J Lipid Res. 1985 May;26(5):600–609. [PubMed] [Google Scholar]
  12. Mattjus P., Slotte J. P. Does cholesterol discriminate between sphingomyelin and phosphatidylcholine in mixed monolayers containing both phospholipids? Chem Phys Lipids. 1996 Jun 17;81(1):69–80. doi: 10.1016/0009-3084(96)02535-2. [DOI] [PubMed] [Google Scholar]
  13. Ohvo H., Olsio C., Slotte J. P. Effects of sphingomyelin and phosphatidylcholine degradation on cyclodextrin-mediated cholesterol efflux in cultured fibroblasts. Biochim Biophys Acta. 1997 Nov 15;1349(2):131–141. doi: 10.1016/s0005-2760(97)00126-4. [DOI] [PubMed] [Google Scholar]
  14. Ohvo H., Slotte J. P. Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate. Biochemistry. 1996 Jun 18;35(24):8018–8024. doi: 10.1021/bi9528816. [DOI] [PubMed] [Google Scholar]
  15. Patton S. Correlative relationship of cholesterol and sphingomyelin in cell membranes. J Theor Biol. 1970 Dec;29(3):489–491. doi: 10.1016/0022-5193(70)90111-6. [DOI] [PubMed] [Google Scholar]
  16. Phillips M. C., Johnson W. J., Rothblat G. H. Mechanisms and consequences of cellular cholesterol exchange and transfer. Biochim Biophys Acta. 1987 Jun 24;906(2):223–276. doi: 10.1016/0304-4157(87)90013-x. [DOI] [PubMed] [Google Scholar]
  17. Pörn M. I., Ares M. P., Slotte J. P. Degradation of plasma membrane phosphatidylcholine appears not to affect the cellular cholesterol distribution. J Lipid Res. 1993 Aug;34(8):1385–1392. [PubMed] [Google Scholar]
  18. Ramstedt B., Leppimäki P., Axberg M., Slotte J. P. Analysis of natural and synthetic sphingomyelins using high-performance thin-layer chromatography. Eur J Biochem. 1999 Dec;266(3):997–1002. doi: 10.1046/j.1432-1327.1999.00938.x. [DOI] [PubMed] [Google Scholar]
  19. Ramstedt B., Slotte J. P. Comparison of the biophysical properties of racemic and d-erythro-N-acyl sphingomyelins. Biophys J. 1999 Sep;77(3):1498–1506. doi: 10.1016/S0006-3495(99)76997-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ramstedt B., Slotte J. P. Interaction of cholesterol with sphingomyelins and acyl-chain-matched phosphatidylcholines: a comparative study of the effect of the chain length. Biophys J. 1999 Feb;76(2):908–915. doi: 10.1016/S0006-3495(99)77254-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sarmientos F., Schwarzmann G., Sandhoff K. Direct evidence by carbon-13 NMR spectroscopy for the erythro configuration of the sphingoid moiety in Gaucher cerebroside and other natural sphingolipids. Eur J Biochem. 1985 Jan 2;146(1):59–64. doi: 10.1111/j.1432-1033.1985.tb08619.x. [DOI] [PubMed] [Google Scholar]
  22. Schneider P. B., Kennedy E. P. Sphingomyelinase in normal human spleens and in spleens from subjects with Niemann-Pick disease. J Lipid Res. 1967 May;8(3):202–209. [PubMed] [Google Scholar]
  23. Shah D. O., Schulman J. H. Interaction of calcium ions with lecithin and sphingomyelin monolayers. Lipids. 1967 Jan;2(1):21–27. doi: 10.1007/BF02531995. [DOI] [PubMed] [Google Scholar]
  24. Shinitzky M., Barenholz Y. Dynamics of the hydrocarbon layer in liposomes of lecithin and sphingomyelin containing dicetylphosphate. J Biol Chem. 1974 Apr 25;249(8):2652–2657. [PubMed] [Google Scholar]
  25. Shinitzky M., Barenholz Y. Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta. 1978 Dec 15;515(4):367–394. doi: 10.1016/0304-4157(78)90010-2. [DOI] [PubMed] [Google Scholar]
  26. Slotte J. P., Bierman E. L. Depletion of plasma-membrane sphingomyelin rapidly alters the distribution of cholesterol between plasma membranes and intracellular cholesterol pools in cultured fibroblasts. Biochem J. 1988 Mar 15;250(3):653–658. doi: 10.1042/bj2500653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Slotte J. P. Direct observation of the action of cholesterol oxidase in monolayers. Biochim Biophys Acta. 1995 Nov 16;1259(2):180–186. doi: 10.1016/0005-2760(95)00161-5. [DOI] [PubMed] [Google Scholar]
  28. Slotte J. P. Effect of sterol structure on molecular interactions and lateral domain formation in monolayers containing dipalmitoyl phosphatidylcholine. Biochim Biophys Acta. 1995 Jul 26;1237(2):127–134. doi: 10.1016/0005-2736(95)00096-l. [DOI] [PubMed] [Google Scholar]
  29. Slotte J. P. Lateral domain formation in mixed monolayers containing cholesterol and dipalmitoylphosphatidylcholine or N-palmitoylsphingomyelin. Biochim Biophys Acta. 1995 May 4;1235(2):419–427. doi: 10.1016/0005-2736(95)80031-a. [DOI] [PubMed] [Google Scholar]
  30. Slotte J. P., Mattjus P. Visualization of lateral phases in cholesterol and phosphatidylcholine monolayers at the air/water interface--a comparative study with two different reporter molecules. Biochim Biophys Acta. 1995 Jan 3;1254(1):22–29. doi: 10.1016/0005-2760(94)00159-v. [DOI] [PubMed] [Google Scholar]
  31. Verger R., De Haas G. H. Enzyme reactions in a membrane model. 1. A new technique to study enzyme reactions in monolayers. Chem Phys Lipids. 1973 Feb;10(2):127–136. doi: 10.1016/0009-3084(73)90009-1. [DOI] [PubMed] [Google Scholar]
  32. Xu X., London E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry. 2000 Feb 8;39(5):843–849. doi: 10.1021/bi992543v. [DOI] [PubMed] [Google Scholar]
  33. Yedgar S., Cohen R., Gatt S., Barenholz Y. Hydrolysis of monomolecular layers of synthetic sphingomyelins by sphingomyelinase of Staphylococcus aureus. Biochem J. 1982 Mar 1;201(3):597–603. doi: 10.1042/bj2010597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. von Tscharner V., McConnell H. M. An alternative view of phospholipid phase behavior at the air-water interface. Microscope and film balance studies. Biophys J. 1981 Nov;36(2):409–419. doi: 10.1016/S0006-3495(81)84740-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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