Fluorescence evidence for cholesterol regular distribution in phosphatidylcholine and in sphingomyelin lipid bilayers (original) (raw)

Abstract

Our previous studies indicated that sterols (including cholesterol and dehydroergosterol) can be regularly distributed into hexagonal superlattices in the plane of liquid-crystalline phosphatidylcholine bilayers. It was suggested that regular and irregular regions coexist in the membrane. In the present study, we report supporting evidence for our sterol regular distribution model. We have examined the fractional concentration dependencies of dehydroergosterol (a naturally occurring cholesterol analogue) fluorescence intensity and lifetime in various phosphatidylcholine and sphingomyelin bilayers. Fluorescence intensity and lifetime dips have been observed at specific sterol mole fractions. At those mole fractions, the acrylamide quenching rate constant of dehydroergosterol fluorescence reaches a local maximum. Those mole fractions match the critical sterol mole fractions at which sterol molecules are expected to be regularly distributed into hexagonal superlattices. The results support the idea that the sterols in the regular region are embedded in the bilayer less deep than those in the irregular regions. We have also examined the fractional cholesterol concentration dependencies of diphenylhexatriene (DPH) fluorescence intensity, lifetime, and polarization in DMPC vesicles. DPH fluorescence intensity and polarization also exhibit distinct dips and peaks, respectively, at critical sterol mole fractions for hexagonal superlattices. However, DPH lifetime changes little with sterol mole fraction. As a comparison, the fluorescence properties of DHE and DPH behave differently in response to the formation of sterol regular distribution. Furthermore, finding evidence for sterol regular distribution in both phosphatidylcholine and sphingomyelin membranes raises the possibility that sterol regular distribution may occur within phospholipid/cholesterol enriched domains of real biological membranes.

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References

  1. B. R. Lentz, D. A. Barrow, and M. Hoechli (1980)Biochemistry 19, 1943–1954.
    Google Scholar
  2. B. Snyder and E. Freire (1980)Proc. Natl. Acad. Sci. USA 77, 4055–4059.
    Google Scholar
  3. J. Rogers, A. G. Lee, and D. D. Wilton (1979)Biochim. Biophys. Acta 552, 23–37.
    Google Scholar
  4. P. A. Hyslop, B. Morel, and R. D. Sauerheber (1990)Biochemistry 29, 1025–1038.
    Google Scholar
  5. P. H. Von Dreele (1978)Biochemistry 17, 3939–3943.
    Google Scholar
  6. I. P. Sugar, J. Zeng, and P. L.-G. Chong (1991)J. Phys. Chem. 95, 7524–7534.
    Google Scholar
  7. S. Mabrey, P. L. Mateo, and J. M. Sturtevant (1978)Biochemistry 17, 2464–2468.
    Google Scholar
  8. P. L.-G. Chong (1994)Proc. Natl. Acad. Sci. USA 91, 10069–10073.
    Google Scholar
  9. J. A. Virtanen, P. Somerharju, and P. K. J. Kinnunen (1988)J. Mol. Electr. 4, 233–236.
    Google Scholar
  10. D. Tang and P. L.-G. Chong (1992)Biophys. J. 63, 903–910.
    Google Scholar
  11. P. L.-G. Chong, D. Tang, and I. P. Sugar (1994)Biophys. J. 66, 2029–2038.
    Google Scholar
  12. I. P. Sugar, D. Tang, and P. L.-G. Chong (1994)J. Phys. Chem. 98, 7201–7210.
    Google Scholar
  13. G. R. Bartlett (1959)J. Biol. Chem. 234, 466–468.
    Google Scholar
  14. P. L.-G. Chong (1996) in J. L. Markley, D. B. Northrop, and C. A. Royer (Eds.),High Pressure Effects in Molecular Biophysics and Enzymology, Proceedings of the 1994 Steenbock Symposium, Oxford University Press, New York, pp. 298–313.
    Google Scholar
  15. E. Alvarez, V. Ruiz-Gutierrez, C. S. Maria, and A. Machado (1993)Mech. Age. Dev. 71, 1–12.
    Google Scholar
  16. E. Quintao, S. M. Grundy, and E. H. Ahrens (1971)J. Lipid Res. 12, 233–247.
    Google Scholar
  17. F. Schroeder, Y. Barenholz, E. Gratton, and T. E. Thompson (1987)Biochemistry 26, 2441–2448.
    Google Scholar
  18. D. L. Melchior, F. J. Scavitto, and J. M. Steim (1980)Biochemistry 19, 4828–4834.
    Google Scholar
  19. T. Parasassi, A. M. Giusti, M. Raimondi, and E. Gratton (1995)Biophys. J. 68, 1895–1902.
    Google Scholar
  20. J. Virtanen, M. Ruonala, M. Vauhkonen, and P. Somerharju (1995)Biochemistry 34, 11568–11581.
    Google Scholar
  21. G. Puchwein, T. Pfeffer, and E. J. M. Helmreich (1974)J. Biol. Chem. 249, 3232–3240.
    Google Scholar
  22. H. M'Zali, and F. Giraud (1986)Biochem. J. 234, 13–20.
    Google Scholar
  23. P. L.-G. Chong and A. R. Cossins (1984)Biochim. Biophys. Acta 772, 197–201.
    Google Scholar
  24. A. Chabanel, M. Flamm, K. L. P. Sung, M. M. Lee, D. Schachter, and S. Chien (1983)Biophys. J. 44, 171–176.
    Google Scholar
  25. J. M. Smaby, V. S. Kulkarni, M. Momsen, and R. E. Brown (1996)Biophys. J. 70, 868–877.
    Google Scholar
  26. C. R. Matteo, A. U. Acuna, and J.-C. Bronchon (1995)Biophys. J. 68, 978–987.
    Google Scholar
  27. D. Toprygin and L. Brand (1995)J. Fluoresc. 5, 39–50.
    Google Scholar
  28. E. Gratton and T. Parasassi (1995)J. Fluoresc. 5, 51–57.
    Google Scholar
  29. L. R. De Young and K. A. Dill (1990)J. Phys. Chem. 94, 801–809.
    Google Scholar
  30. D. Tang, B. W. van der Meer, and S.-Y. S. Chen (1995)Biophys. J. 68, 1944–1951.
    Google Scholar
  31. T. P. W. McMullen and R. N. McElhaney (1995)Biochim. Biophys. Acta 1234, 90–98.
    Google Scholar
  32. J. M. Smaby, M. Momsen, V. S. Kulkami, and R. E. Brown (1996)Biochemistry 35, 5696–5704.
    Google Scholar
  33. P. L.-G. Chong, M. M. Wang, F. Liu, K. Truong, A. Golsorkhi, I. P. Sugar, and R. E. Brown (1996)Proc. Fluoresc. Detect. IV, SPIE 2705, 143–154.
    Google Scholar
  34. M. Straume and B. J. Litman (1987)Biochemistry 26, 5121–5126.
    Google Scholar
  35. C. Ho and D. Stubbs (1992)Biophys. J. 63, 897–902.
    Google Scholar

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Authors and Affiliations

  1. Department of Biochemistry, Temple University School of Medicine, 19140, Philadelphia, Pennsylvania
    Parkson Lee-Gau Chong, Fang Liu, Mei Mei Wang & Khanh Truong
  2. Departments of Biomathematical Sciences and Physiology & Biophysics, Mount Sinai Medical Center, 10029, New York, New York
    Istvan P. Sugar
  3. Hormel Institute, University of Minnesota, 55912, Austin, Minnesota
    Rhoderick E. Brown

Authors

  1. Parkson Lee-Gau Chong
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  2. Fang Liu
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  3. Mei Mei Wang
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  4. Khanh Truong
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  5. Istvan P. Sugar
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  6. Rhoderick E. Brown
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Chong, P.LG., Liu, F., Wang, M.M. et al. Fluorescence evidence for cholesterol regular distribution in phosphatidylcholine and in sphingomyelin lipid bilayers.J Fluoresc 6, 221–230 (1996). https://doi.org/10.1007/BF00732825

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