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. 1991 Aug 15;88(16):6926–6930. doi: 10.1073/pnas.88.16.6926

Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers.

I Schuler 1, A Milon 1, Y Nakatani 1, G Ourisson 1, A M Albrecht 1, P Benveniste 1, M A Hartman 1
PMCID: PMC52206  PMID: 11607205

Abstract

To gain some insight into the structural and functional roles of sterols in higher plant cells, various plant sterols have been incorporated into soybean phosphatidylcholine (PtdCho) bilayers and tested for their ability to regulate water permeability and acyl chain ordering. Sitosterol was the most efficient sterol in reducing the water permeability of these vesicles and stigmasterol appeared to have no significant effect. Vesicles containing 24zeta-methylcholesterol exhibited an intermediate behavior, similar to that of vesicles containing cholesterol. Cycloartenol, the first cyclic biosynthetic precursor of plant sterols, reduced the water permeability in a very effective way. Of two unusual plant sterols, 24-methylpollinastanol and 14alpha,24zeta-dimethylcholest-8-en-3beta-ol, the former was found to be functionally equivalent to sitosterol and the latter was found to be relatively inefficient. 2H NMR experiments have been performed with oriented bilayers consisting of soybean PtdCho with sitosterol, stigmasterol, or 24-methylpollinastanol. The results provided clear evidence that sitosterol and 24zeta-methylpollinastanol exhibit a high efficiency to order PtdCho acyl chains that closely parallels their ability to reduce water permeability. By contrast, stigmasterol shows a low efficiency for both functions. These results show that sitosterol and stigmasterol, two major 24-ethylsterols differing only by the absence or presence of the Delta22 double bond in the side chain, probably play different roles in regulating plant membrane properties; they also may explain why 9beta,19-cyclopropylsterols behave as good surrogates of sitosterol.

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Selected References

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

  1. Bittman R., Blau L. The phospholipid-cholesterol interaction. Kinetics of water permeability in liposomes. Biochemistry. 1972 Dec 5;11(25):4831–4839. doi: 10.1021/bi00775a029. [DOI] [PubMed] [Google Scholar]
  2. Bladocha M., Benveniste P. Manipulation by tridemorph, a systemic fungicide, of the sterol composition of maize leaves and roots. Plant Physiol. 1983 Apr;71(4):756–762. doi: 10.1104/pp.71.4.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bloch K. E. Sterol structure and membrane function. CRC Crit Rev Biochem. 1983;14(1):47–92. doi: 10.3109/10409238309102790. [DOI] [PubMed] [Google Scholar]
  4. Butler K. W., Smith I. C., Schneider H. Sterol structure and ordering effects in spin-labelled phospholipid multibilayer structures. Biochim Biophys Acta. 1970 Dec 1;219(2):514–517. doi: 10.1016/0005-2736(70)90236-1. [DOI] [PubMed] [Google Scholar]
  5. Butler K. W., Smith I. C. Sterol ordering effects and permeability regulation in phosphatidylcholine bilayers. A comparison of ESR spin-probe data from oriented multilamellae and dispersions. Can J Biochem. 1978 Feb;56(2):117–122. doi: 10.1139/o78-019. [DOI] [PubMed] [Google Scholar]
  6. Chakrabarti P., Khorana G. A new approach to the study of phospholipid-protein interactions in biological membranes. Synthesis of fatty acids and phospholipids containing photosensitive groups. Biochemistry. 1975 Nov 18;14(23):5021–5033. doi: 10.1021/bi00694a001. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Demiel R. A., Guerts van Kessel W. S., van Deenen L. L. The properties of polyunsaturated lecithins in monolayers and liposomes and the interactions of these lecithins with cholesterol. Biochim Biophys Acta. 1972 Apr 14;266(1):26–40. doi: 10.1016/0005-2736(72)90116-2. [DOI] [PubMed] [Google Scholar]
  10. Grandmougin A., Bouvier-Navé P., Ullmann P., Benveniste P., Hartmann M. A. Cyclopropyl sterol and phospholipid composition of membrane fractions from maize roots treated with fenpropimorph. Plant Physiol. 1989 Jun;90(2):591–597. doi: 10.1104/pp.90.2.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Heyn M. P. Determination of lipid order parameters and rotational correlation times from fluorescence depolarization experiments. FEBS Lett. 1979 Dec 15;108(2):359–364. doi: 10.1016/0014-5793(79)80564-5. [DOI] [PubMed] [Google Scholar]
  12. Isaacson Y., Riehl T. E., Stenson W. F. Nonelectrolyte permeability of liposomes of hydroxyfatty acid-containing phosphatidylcholines. Biochim Biophys Acta. 1989 Nov 27;986(2):295–300. doi: 10.1016/0005-2736(89)90480-x. [DOI] [PubMed] [Google Scholar]
  13. Jarrell H. C., Jovall P. A., Giziewicz J. B., Turner L. A., Smith I. C. Determination of conformational properties of glycolipid head groups by 2H NMR of oriented multibilayers. Biochemistry. 1987 Apr 7;26(7):1805–1811. doi: 10.1021/bi00381a003. [DOI] [PubMed] [Google Scholar]
  14. Jähnig F. Structural order of lipids and proteins in membranes: evaluation of fluorescence anisotropy data. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6361–6365. doi: 10.1073/pnas.76.12.6361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Klein R. A. The detection of oxidation in liposome preparations. Biochim Biophys Acta. 1970 Sep 8;210(3):486–489. doi: 10.1016/0005-2760(70)90046-9. [DOI] [PubMed] [Google Scholar]
  16. Lazrak T., Milon A., Wolff G., Albrecht A. M., Miehé M., Ourisson G., Nakatani Y. Comparison of the effects of inserted C40- and C50-terminally dihydroxylated carotenoids on the mechanical properties of various phospholipid vesicles. Biochim Biophys Acta. 1987 Sep 18;903(1):132–141. doi: 10.1016/0005-2736(87)90163-5. [DOI] [PubMed] [Google Scholar]
  17. Ourisson G., Rohmer M., Poralla K. Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annu Rev Microbiol. 1987;41:301–333. doi: 10.1146/annurev.mi.41.100187.001505. [DOI] [PubMed] [Google Scholar]
  18. Pugh E. L., Bittman R., Fugler L., Kates M. Comparison of steady-state fluorescence polarization and urea permeability of phosphatidylcholine and phosphatidylsulfocholine liposomes as a function of sterol structure. Chem Phys Lipids. 1989 Apr;50(1):43–50. doi: 10.1016/0009-3084(89)90024-8. [DOI] [PubMed] [Google Scholar]
  19. Ranadive G. N., Lala A. K. Sterol-phospholipid interaction in model membranes: role of C5-C6 double bond in cholesterol. Biochemistry. 1987 May 5;26(9):2426–2431. doi: 10.1021/bi00383a005. [DOI] [PubMed] [Google Scholar]
  20. Schuler I., Duportail G., Glasser N., Benveniste P., Hartmann M. A. Soybean phosphatidylcholine vesicles containing plant sterols: a fluorescence anisotropy study. Biochim Biophys Acta. 1990 Sep 21;1028(1):82–88. doi: 10.1016/0005-2736(90)90268-s. [DOI] [PubMed] [Google Scholar]
  21. Seelig J. Deuterium magnetic resonance: theory and application to lipid membranes. Q Rev Biophys. 1977 Aug;10(3):353–418. doi: 10.1017/s0033583500002948. [DOI] [PubMed] [Google Scholar]
  22. Stillwell W., Cheng Y. F., Wassall S. R. Plant sterol inhibition of abscisic acid-induced perturbations in phospholipid bilayers. Biochim Biophys Acta. 1990 May 24;1024(2):345–351. doi: 10.1016/0005-2736(90)90364-t. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Szoka F., Jr, Papahadjopoulos D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4194–4198. doi: 10.1073/pnas.75.9.4194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tanfani F., Bertoli E. Permeability of oxidized phosphatidylcholine liposomes. Biochem Biophys Res Commun. 1989 Aug 30;163(1):241–246. doi: 10.1016/0006-291x(89)92127-x. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. 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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