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. 1987 Feb;169(2):830–838. doi: 10.1128/jb.169.2.830-838.1987

Lipid acyl chain-dependent effects of sterols in Acholeplasma laidlawii membranes.

L Rilfors, G Wikander, A Wieslander
PMCID: PMC211854  PMID: 3027049

Abstract

Acholeplasma laidlawii was grown with different fatty acids for membrane lipid synthesis (saturated straight- and branched-chain acids and mono- and di-unsaturated acids). The ability of 12 different sterols to affect cell growth, lipid head group composition, the order parameter of the acyl chains, and the phase equilibria of in vivo lipid mixtures was studied. The following two effects were observed with respect to cell growth: with a given acyl chain composition of the membrane lipids, growth was stimulated, unaffected, reduced, or completely inhibited (lysis), depending on the sterol structure; and the effect of a certain sterol depended on the acyl chain composition (most striking for epicoprostanol, cholest-4-en-3-one, and cholest-5-en-3-one, which stimulated growth with saturated acyl chains but caused lysis with unsaturated chains). The three lytic sterols were the only sterols that caused a marked decrease in the ratio between the major lipids monoglucosyldiglyceride and diglucosyldiglyceride and hence a decrease in bilayer stability when the membranes were enriched in saturated (palmitoyl) chains. With these chains correlations were found for several sterols between the glucolipid ratio and the order parameter of the acyl chains, as well as the lamellar-reversed hexagonal phase transition, in model systems. A shaft experiment revealed a marked decrease in the ratio of monoglucosyldiglyceride to diglucosyldiglyceride with the lytic sterols in unsaturated (oleoyl) membranes. The two cholestenes induced nonlamellar phases in in vivo mixtures of oleoyl A. laidlawii lipids. The order parameters of the oleoyl chains were almost unaffected by the sterols. Generally, the observed effects cannot be explained by an influence of the sterols on the gel-to-liquid crystalline phase transition.

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Selected References

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  1. Bruckdorfer K. R., Demel R. A., De Gier J., van Deenen L. L. The effect of partial replacements of membrane cholesterol by other steroids on the osmotic fragility and glycerol permeability of erythrocytes. Biochim Biophys Acta. 1969 Jul 15;183(2):334–345. doi: 10.1016/0005-2736(69)90089-3. [DOI] [PubMed] [Google Scholar]
  2. Buttke T. M., Jones S. D., Bloch K. Effect of sterol side chains on growth and membrane fatty acid composition of Saccharomyces cerevisiae. J Bacteriol. 1980 Oct;144(1):124–130. doi: 10.1128/jb.144.1.124-130.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Christiansson A., Eriksson L. E., Westman J., Demel R., Wieslander A. Involvement of surface potential in regulation of polar membrane lipids in Acholeplasma laidlawii. J Biol Chem. 1985 Apr 10;260(7):3984–3990. [PubMed] [Google Scholar]
  4. Christiansson A., Wieslander A. Control of membrane polar lipid composition in Acholeplasma laidlawii a by the extent of saturated fatty acid synthesis. Biochim Biophys Acta. 1980 Jan 25;595(2):189–199. doi: 10.1016/0005-2736(80)90083-8. [DOI] [PubMed] [Google Scholar]
  5. Christiansson A., Wieslander A. Membrane lipid metabolism in Acholeplasma laidlawii A EF 22. Influence of cholesterol and temperature shift-down on incorporation of fatty acids and synthesis of membrane lipid species. Eur J Biochem. 1978 Apr;85(1):65–76. doi: 10.1111/j.1432-1033.1978.tb12212.x. [DOI] [PubMed] [Google Scholar]
  6. Clementz T., Christiansson A., Wieslander A. Transmembrane electrical potential affects the lipid composition of Acholeplasma laidlawii. Biochemistry. 1986 Feb 25;25(4):823–830. doi: 10.1021/bi00352a014. [DOI] [PubMed] [Google Scholar]
  7. Dahl J. S., Dahl C. E., Bloch K. Sterols in membranes: growth characteristics and membrane properties of Mycoplasma capricolum cultured on cholesterol and lanosterol. Biochemistry. 1980 Apr 1;19(7):1467–1472. doi: 10.1021/bi00548a032. [DOI] [PubMed] [Google Scholar]
  8. Dahl J. S., Dahl C. E. Coordinate regulation of unsaturated phospholipid, RNA, and protein synthesis in Mycoplasma capricolum by cholesterol. Proc Natl Acad Sci U S A. 1983 Feb;80(3):692–696. doi: 10.1073/pnas.80.3.692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Demel R. A., Bruckdorfer K. R., van Deenen L. L. The effect of sterol structure on the permeability of lipomes to glucose, glycerol and Rb + . Biochim Biophys Acta. 1972 Jan 17;255(1):321–330. doi: 10.1016/0005-2736(72)90031-4. [DOI] [PubMed] [Google Scholar]
  10. Gallay J., De Kruijff B. Correlation between molecular shape and hexagonal HII phase promoting ability of sterols. FEBS Lett. 1982 Jun 21;143(1):133–136. doi: 10.1016/0014-5793(82)80289-5. [DOI] [PubMed] [Google Scholar]
  11. Hubbell W. L., McConnell H. M. Molecular motion in spin-labeled phospholipids and membranes. J Am Chem Soc. 1971 Jan 27;93(2):314–326. doi: 10.1021/ja00731a005. [DOI] [PubMed] [Google Scholar]
  12. Jacobs R., Oldfield E. Deuterium nuclear magnetic resonance investigation of dimyristoyllecithin--dipalmitoyllecithin and dimyristoyllecithin--cholesterol mixtures. Biochemistry. 1979 Jul 24;18(15):3280–3285. doi: 10.1021/bi00582a013. [DOI] [PubMed] [Google Scholar]
  13. Kawasaki S., Ramgopal M., Chin J., Bloch K. Sterol control of the phosphatidylethanolamine-phosphatidylcholine conversion in the yeast mutant GL7. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5715–5719. doi: 10.1073/pnas.82.17.5715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Khan A., Rilfors L., Wieslander A., Lindblom G. The effect of cholesterol on the phase structure of glucolipids from Acholeplasma laidlawii membranes. Eur J Biochem. 1981 May;116(2):215–220. doi: 10.1111/j.1432-1033.1981.tb05321.x. [DOI] [PubMed] [Google Scholar]
  15. Lindblom G., Brentel I., Sjölund M., Wikander G., Wieslander A. Phase equilibria of membrane lipids from Acholeplasma laidlawii: importance of a single lipid forming nonlamellar phases. Biochemistry. 1986 Nov 18;25(23):7502–7510. doi: 10.1021/bi00371a037. [DOI] [PubMed] [Google Scholar]
  16. Mabrey S., Mateo P. L., Sturtevant J. M. High-sensitivity scanning calorimetric study of mixtures of cholesterol with dimyristoyl- and dipalmitoylphosphatidylcholines. Biochemistry. 1978 Jun 13;17(12):2464–2468. doi: 10.1021/bi00605a034. [DOI] [PubMed] [Google Scholar]
  17. Mandersloot J. G., Reman F. C., Van Deenen L. L., De Gier J. Barrier properties of lecithin/lysolecithin mixtures. Biochim Biophys Acta. 1975 Feb 28;382(1):22–26. doi: 10.1016/0005-2736(75)90368-5. [DOI] [PubMed] [Google Scholar]
  18. McElhaney R. N. The effect of alterations in the physical state of the membrane lipids on the ability of Acholeplasma laidlawii B to grow at various temperatures. J Mol Biol. 1974 Mar 25;84(1):145–157. doi: 10.1016/0022-2836(74)90218-6. [DOI] [PubMed] [Google Scholar]
  19. Noordam P. C., van Echteld C. J., de Kruijff B., Verkleij A. J., de Gier J. Barrier characteristics of membrane model systems containing unsaturated phosphatidylethanolamines. Chem Phys Lipids. 1980 Oct;27(3):221–232. doi: 10.1016/0009-3084(80)90037-7. [DOI] [PubMed] [Google Scholar]
  20. Rodriguez R. J., Low C., Bottema C. D., Parks L. W. Multiple functions for sterols in Saccharomyces cerevisiae. Biochim Biophys Acta. 1985 Dec 4;837(3):336–343. doi: 10.1016/0005-2760(85)90057-8. [DOI] [PubMed] [Google Scholar]
  21. Rottem S., Pfendt E. A., Hayflick L. Sterol requirements of T-strain mycoplasmas. J Bacteriol. 1971 Jan;105(1):323–330. doi: 10.1128/jb.105.1.323-330.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Silvius J. R., McElhaney R. N. Lipid compositional manipulation in Acholeplasma laidlawii B. Effect of exogenous fatty acids on fatty acid composition and cell growth when endogenous fatty acid production is inhibited. Can J Biochem. 1978 Jun;56(6):462–469. doi: 10.1139/o78-072. [DOI] [PubMed] [Google Scholar]
  23. Smith R. L., Oldfield E. Dynamic structure of membranes by deuterium NMR. Science. 1984 Jul 20;225(4659):280–288. doi: 10.1126/science.6740310. [DOI] [PubMed] [Google Scholar]
  24. Vincent M., Gallay J. Steroid-lipid interactions in sonicated dipalmitoyl phosphatidyl choline vesicles: a steady-state and time-resolved fluorescence anisotropy study with all trans-1,6-diphenyl-1,3,5-hexatriene as probe. Biochem Biophys Res Commun. 1983 Jun 29;113(3):799–810. doi: 10.1016/0006-291x(83)91070-7. [DOI] [PubMed] [Google Scholar]
  25. Wieslander A., Christiansson A., Rilfors L., Lindblom G. Lipid bilayer stability in membranes. Regulation of lipid composition in Acholeplasma laidlawii as governed by molecular shape. Biochemistry. 1980 Aug 5;19(16):3650–3655. doi: 10.1021/bi00557a002. [DOI] [PubMed] [Google Scholar]
  26. Wieslander A., Rilfors L., Lindblom G. Metabolic changes of membrane lipid composition in Acholeplasma laidlawii by hydrocarbons, alcohols, and detergents: arguments for effects on lipid packing. Biochemistry. 1986 Nov 18;25(23):7511–7517. doi: 10.1021/bi00371a038. [DOI] [PubMed] [Google Scholar]
  27. Wieslander A., Rilfors L. Qualitative and quantitative variations of membrane lipid species in Acholeplasma laidlawii A. Biochim Biophys Acta. 1977 Apr 18;466(2):336–346. doi: 10.1016/0005-2736(77)90229-2. [DOI] [PubMed] [Google Scholar]
  28. Wieslander A., Ulmius J., Lindblom G., Fontell K. Water binding and phase structures for different Acholeplasma laidlawii membrane lipids studied by deuteron nuclear magnetic resonance and x-ray diffraction. Biochim Biophys Acta. 1978 Sep 22;512(2):241–253. doi: 10.1016/0005-2736(78)90250-x. [DOI] [PubMed] [Google Scholar]
  29. Yeagle P. L. Lanosterol and cholesterol have different effects on phospholipid acyl chain ordering. Biochim Biophys Acta. 1985 Apr 26;815(1):33–36. doi: 10.1016/0005-2736(85)90470-5. [DOI] [PubMed] [Google Scholar]
  30. Yeagle P. L., Martin R. B., Lala A. K., Lin H. K., Bloch K. Differential effects of cholesterol and lanosterol on artificial membranes. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4924–4926. doi: 10.1073/pnas.74.11.4924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. de Kruyff B., Demel R. A., van Deenen L. L. The effect of cholesterol and epicholesterol incorporation on the permeability and on the phase transition of intact Acholeplasma laidlawii cell membranes and derived liposomes. Biochim Biophys Acta. 1972 Jan 17;255(1):331–347. doi: 10.1016/0005-2736(72)90032-6. [DOI] [PubMed] [Google Scholar]
  32. de Kruyff B., de Greef W. J., van Eyk R. V., Demel R. A., van Deenen L. L. The effect of different fatty acid and sterol composition on the erythritol flux through the cell membrane of Acholeplasma laidlawii. Biochim Biophys Acta. 1973 Mar 16;298(2):479–499. doi: 10.1016/0005-2736(73)90375-1. [DOI] [PubMed] [Google Scholar]

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