Advertisement

Cell Biochemistry and Biophysics

, Volume 75, Issue 3–4, pp 369–385 | Cite as

High Cholesterol/Low Cholesterol: Effects in Biological Membranes: A Review

  • Witold K. SubczynskiEmail author
  • Marta Pasenkiewicz-Gierula
  • Justyna Widomska
  • Laxman Mainali
  • Marija Raguz
Original Paper

Abstract

Lipid composition determines membrane properties, and cholesterol plays a major role in this determination as it regulates membrane fluidity and permeability, as well as induces the formation of coexisting phases and domains in the membrane. Biological membranes display a very diverse lipid composition, the lateral organization of which plays a crucial role in regulating a variety of membrane functions. We hypothesize that, during biological evolution, membranes with a particular cholesterol content were selected to perform certain functions in the cells of eukaryotic organisms. In this review, we discuss the major membrane properties induced by cholesterol, and their relationship to certain membrane functions.

Keyword

EPR Oximetry Lipid spin label Membrane domains Cholesterol 

Notes

Acknowledgements

This work was supported by grants EY015526, EB001980, and EY001931 from the National Institutes of Health, USA. Faculty of Biochemistry, Biophysics, and Biotechnology of Jagiellonian University is a partner of the Leading National Research Center (KNOW) supported by the Ministry of Science and Higher Education, Poland.

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. 1.
    Roux, B., Berneche, S., Egwolf, B., Lev, B., Noskov, S. Y., Rowley, C. N., et al. (2011). Ion selectivity in channels and transporters. The Journal of General Physiology, 137, 415–426.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Hille, B. (2001). Ion Channels of Excitable Membranes. (3rd Edition). Sinauer Associates Inc, Sunderland, MA.Google Scholar
  3. 3.
    Luckey, M. (2008). Membrane Structural Biology: with Biochemical and Biophysical Foundations. Cambridge University Press, New York, NY.Google Scholar
  4. 4.
    Diamond, J. M., & Katz, Y. (1974). Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water. Journal of Membrane Biology, 17, 121–154.CrossRefPubMedGoogle Scholar
  5. 5.
    Viola, A. (2001). The amplification of TCR signaling by dynamic membrane microdomains. Trends in Immunology, 22, 322–327.CrossRefPubMedGoogle Scholar
  6. 6.
    Simons, K., & Toomre, D. (2000). Lipid rafts and signal transduction. Nature Reviews. Molecular Cell Biology, 1, 31–39.CrossRefPubMedGoogle Scholar
  7. 7.
    Kusumi, A., Fujiwara, T. K., Morone, N., Yoshida, K. J., Chadda, R., Xie, M., et al. (2012). Membrane mechanisms for signal transduction: the coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes. Seminars in Cell and Developmental Biology, 23, 126–144.CrossRefPubMedGoogle Scholar
  8. 8.
    Nelson, D. L., & Cox, M. M. (2008). Lehninger Principles of Biochemistry. 5th edition. W. H. Freeman and Company, New York, NY.Google Scholar
  9. 9.
    Borchman, D., & Yappert, M. C. (2010). Lipids and the ocular lens. Journal of Lipid Research, 51, 2473–2488.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Subczynski, W. K., Raguz, M., Widomska, J., Mainali, L., & Konovalov, A. (2012). Functions of cholesterol and the cholesterol bilayer domain specific to the fiber-cell plasma membrane of the eye lens. Journal of Membrane Biology, 245, 51–68.CrossRefPubMedGoogle Scholar
  11. 11.
    Epand, R. M. (2005). Role of membrane lipids in modulating the activity of membrane-bound enzymes. In P. L. Yeagle (Ed.), The Structure of Biological Membrane (pp. 499–509). Boca Raton: CRC Press.Google Scholar
  12. 12.
    Reichow, S. L., & Gonen, T. (2009). Lipid-protein interactions probed by electron crystallography. Current Opinion in Structural Biology, 19, 560–565.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Tong, J., Briggs, M. M., & McIntosh, T. J. (2012). Water permeability of aquaporin-4 channel depends on bilayer composition, thickness, and elasticity. Biophysical Journal, 103, 1899–1908.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Tong, J., Canty, J. T., Briggs, M. M., & McIntosh, T. J. (2013). The water permeability of lens aquaporin-0 depends on its lipid bilayer environment. Experimental Eye Research, 113, 32–40.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bloch, K. E. (1983). Sterol structure and membrane function. CRC Critical Reviews in Biochemistry, 14, 47–92.CrossRefPubMedGoogle Scholar
  16. 16.
    Bloom, M., & Mouritsen, O. G. (1995). The evolution of membrane. In R. Lipowsky, E. Sackmann (eds.). Structure and Dynamics of Membrane (pp. 65–95). Amsterdam: Elsevier.Google Scholar
  17. 17.
    Miao, L., Nielsen, M., Thewalt, J., Ipsen, J. H., Bloom, M., Zuckermann, M. J., et al. (2002). From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers. Biophysical Journal, 82, 1429–1444.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rog, T., Pasenkiewicz-Gierula, M., Vattulainen, I., & Karttunen, M. (2007). What happens if cholesterol is made smoother: importance of methyl substituents in cholesterol ring structure on phosphatidylcholine-sterol interaction. Biophysical Journal, 92, 3346–3357.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hannich, J. T., Umebayashi, K., & Riezman, H. (2011). Distribution and functions of sterols and sphingolipids. Cold Spring Harbor Perspectives in Biology, 3, 1–14.CrossRefGoogle Scholar
  20. 20.
    Bretscher, M. S., & Munro, S. (1993). Cholesterol and the Golgi apparatus. Science (New York, N.Y.), 261, 1280–1281.CrossRefGoogle Scholar
  21. 21.
    Schroeder, F., Frolov, A. A., Murphy, E. J., Atshaves, B. P., Jefferson, J. R., Pu, L., et al. (1996). Recent advances in membrane cholesterol domain dynamics and intracellular cholesterol trafficking. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine, 213, 150–177.CrossRefGoogle Scholar
  22. 22.
    van Meer, G., Voelker, D. R., & Feigenson, G. W. (2008). Membrane lipids: where they are and how they behave. Nature reviews. Molecular Cell Biology, 9, 112–124.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Spector, A. A., & Yorek, M. A. (1985). Membrane lipid composition and cellular function. Journal of Lipid Research, 26, 1015–1035.PubMedGoogle Scholar
  24. 24.
    Shinitzky, M., & Barenholz, Y. (1978). Fluidity parameters of lipid regions determined by fluorescence polarization. Biochimica et Biophysica Acta, 515, 367–394.CrossRefPubMedGoogle Scholar
  25. 25.
    Mainali, L., Raguz, M., & Subczynski, W. K. (2013). Formation of cholesterol bilayer domains precedes formation of cholesterol crystals in cholesterol/dimyristoylphosphatidylcholine membranes: EPR and DSC studies. Journal of Physical Chemistry B, 117, 8994–9003.CrossRefGoogle Scholar
  26. 26.
    Raguz, M., Mainali, L., Widomska, J., & Subczynski, W. K. (2011). Using spin-label electron paramagnetic resonance (EPR) to discriminate and characterize the cholesterol bilayer domain. Chemistry and Physics of Lipids, 164, 819–829.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Li, L. K., So, L., & Spector, A. (1987). Age-dependent changes in the distribution and concentration of human lens cholesterol and phospholipids. Biochimica et Biophysica Acta, 917, 112–120.CrossRefPubMedGoogle Scholar
  28. 28.
    Truscott, R. J. (2000). Age-related nuclear cataract: a lens transport problem. Ophthalmic Research, 32, 185–194.CrossRefPubMedGoogle Scholar
  29. 29.
    Li, L. K., So, L., & Spector, A. (1985). Membrane cholesterol and phospholipid in consecutive concentric sections of human lenses. Journal of Lipid Research, 26, 600–609.PubMedGoogle Scholar
  30. 30.
    Mason, R. P., & Jacob, R. F. (2003). Membrane microdomains and vascular biology. Emerging role in atherogenesis. Circulation, 107, 2270–2273.CrossRefPubMedGoogle Scholar
  31. 31.
    Mason, R., Tulenko, T. N., & Jacob, R. F. (2003). Direct evidence for cholesterol crystalline domains in biological membranes: role in human pathobiology. Biochimica et Biophysica Acta, 1610, 198–207.CrossRefGoogle Scholar
  32. 32.
    Jacob, R. F., Cenedella, R. J., & Mason, R. P. (1999). Direct evidence for immiscible cholesterol domains in human ocular lens fiber cell plasma membranes. Journal of Biological Chemistry, 274, 31613–31618.CrossRefPubMedGoogle Scholar
  33. 33.
    Singer, S. J., & Nicolson, G. L. (1972). The fluid mosaic model of the structure of cell membranes. Science (New York, N.Y.), 175, 720–731.CrossRefGoogle Scholar
  34. 34.
    Kusumi, A., Suzuki, K. G., Kasai, R. S., Ritchie, K., & Fujiwara, T. K. (2011). Hierarchical mesoscale domain organization of the plasma membrane. Trends in Biochemical Sciences, 36, 604–615.CrossRefPubMedGoogle Scholar
  35. 35.
    Kusumi, A., Fujiwara, T. K., Chadda, R., Xie, M., Tsunoyama, T. A., Kalay, Z., et al. (2012). Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson’s fluid-mosaic model. Annual Review of Cell and Developmental Biology, 28, 215–250.CrossRefPubMedGoogle Scholar
  36. 36.
    Wisniewska, A., Draus, J., & Subczynski, W. K. (2003). Is a fluid-mosaic model of biological membranes fully relevant? Studies on lipid organization in model and biological membranes. Cellular and Molecular Biology Letters, 8, 147–159.PubMedGoogle Scholar
  37. 37.
    Nicolson, G. L. (2014). The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochimica et Biophysica Acta, 1838, 1451–1466.CrossRefPubMedGoogle Scholar
  38. 38.
    Subczynski, W. K., Antholine, W. E., Hyde, J. S., & Kusumi, A. (1990). Microimmiscibility and three-dimensional dynamic structures of phosphatidylcholine-cholesterol membranes: translational diffusion of a copper complex in the membrane. Biochemistry, 29, 7936–7945.CrossRefPubMedGoogle Scholar
  39. 39.
    Subczynski, W. K., Wisniewska, A., Hyde, J. S., & Kusumi, A. (2007). Three-dimensional dynamic structure of the liquid-ordered domain in lipid membranes as examined by pulse-EPR oxygen probing. Biophysical Journal, 92, 1573–1584.CrossRefPubMedGoogle Scholar
  40. 40.
    Subczynski, W. K., Hyde, J. S., & Kusumi, A. (1991). Effect of alkyl chain unsaturation and cholesterol intercalation on oxygen transport in membranes: a pulse ESR spin labeling study. Biochemistry, 30, 8578–8590.CrossRefPubMedGoogle Scholar
  41. 41.
    Almeida, P. F., Pokorny, A., & Hinderliter, A. (2005). Thermodynamics of membrane domains. Biochimica et Biophysica Acta, 1720, 1–13.CrossRefPubMedGoogle Scholar
  42. 42.
    Heberle, F. A., & Feigenson, G. W. (2011). Phase separation in lipid membranes. Cold Spring Harbor. Perspectives in Biology, 3, 1–13.CrossRefGoogle Scholar
  43. 43.
    Simons, K., & Vaz, W. L. (2004). Model systems, lipid rafts, and cell membranes. Annual Review of Biophysics and Biomolecular Structure, 33, 269–295.CrossRefPubMedGoogle Scholar
  44. 44.
    Huang, J., Buboltz, J. T., & Feigenson, G. W. (1999). Maximum solubility of cholesterol in phosphatidylcholine and phosphatidylethanolamine bilayers. Biochimica et Biophysica Acta, 1417, 89–100.CrossRefPubMedGoogle Scholar
  45. 45.
    Marsh, D. (1981). Electron spin resonance: spin labels. In E. Grell (ed.), Membrane Spectroscopy (pp. 51–142). Berlin: Springer.CrossRefGoogle Scholar
  46. 46.
    Devaux, P. F. (1983). ESR and NMR studies of lipid-protein interactions in membranes. In L. J. Berliner, J. Reuben (eds.), Biological Magnetic Resonance (pp. 183–299). New York: Plenum Press.CrossRefGoogle Scholar
  47. 47.
    Schreier, S., Polnaszek, C. F., & Smith, I. C. (1978). Spin labels in membranes. Problems in practice. Biochimica et Biophysica Acta, 515, 395–436.CrossRefPubMedGoogle Scholar
  48. 48.
    Rog, T., & Pasenkiewicz-Gierula, M. (2001). Cholesterol effects on the phosphatidylcholine bilayer nonpolar region: a molecular simulation study. Biophysical Journal, 81, 2190–2202.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Mainali, L., Feix, J. B., Hyde, J. S., & Subczynski, W. K. (2011). Membrane fluidity profiles as deduced by saturation-recovery EPR measurements of spin-lattice relaxation times of spin labels. Journal of Magnetic Resonance, 212, 418–425.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Mainali, L., Hyde, J. S., & Subczynski, W. K. (2013). Using spin-label W-band EPR to study membrane fluidity profiles in samples of small volume. Journal of Magnetic Resonance, 226, 35–44.CrossRefPubMedGoogle Scholar
  51. 51.
    Robinson, B. H., Haas, D. A., & Mailer, C. (1994). Molecular dynamics in liquids: spin-lattice relaxation of nitroxide spin labels. Science (New York, N.Y.), 263, 490–493.CrossRefGoogle Scholar
  52. 52.
    Mailer, C., Nielsen, R. D., & Robinson, B. H. (2005). Explanation of spin-lattice relaxation rates of spin labels obtained with multifrequency saturation recovery EPR. The Journal of Physical Chemistry. A, 109, 4049–4061.CrossRefPubMedGoogle Scholar
  53. 53.
    Rog, T., & Pasenkiewicz-Gierula, M. (2004). Non-polar interactions between cholesterol and phospholipids: a molecular dynamics simulation study. Biophysical Chemistry, 107, 151–164.CrossRefPubMedGoogle Scholar
  54. 54.
    Rog, T., & Pasenkiewicz-Gierula, M. (2001). Cholesterol effects on the phospholipid condensation and packing in the bilayer: a molecular simulation study. FEBS Letters, 502, 68–71.CrossRefPubMedGoogle Scholar
  55. 55.
    Murzyn, K., Rog, T., Jezierski, G., Takaoka, Y., & Pasenkiewicz-Gierula, M. (2001). Effects of phospholipid unsaturation on the membrane/water interface: a molecular simulation study. Biophysical Journal, 81, 170–183.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Plesnar, E., Subczynski, W. K., & Pasenkiewicz-Gierula, M. (2013). Comparative computer simulation study of cholesterol in hydrated unary and binary lipid bilayers and in an anhydrous crystal. The Journal of Physical Chemistry. B, 117, 8758–8769.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Griffith, O. H., Dehlinger, P. J., & Van, S. P. (1974). Shape of the hydrophobic barrier of phospholipid bilayers (evidence for water penetration in biological membranes). Journal of Membrane Biology, 15, 159–192.CrossRefPubMedGoogle Scholar
  58. 58.
    Griffith, O. H., & Jost, P. C. (1976). Lipid spin labels in biological membranes. In L. J. Berliner (ed.), Spin Labeling Theory and Applications (pp. 453–523). New York, San Francisco, London: Academic Press.CrossRefGoogle Scholar
  59. 59.
    Subczynski, W. K., Wisniewska, A., Yin, J.-J., Hyde, J. S., & Kusumi, A. (1994). Hydrophobic barriers of lipid bilayer membranes formed by reduction of water penetration by alkyl chain unsaturation and cholesterol. Biochemistry, 33, 7670–7681.CrossRefPubMedGoogle Scholar
  60. 60.
    Wisniewska, A., & Subczynski, W. K. (1998). Effects of polar carotenoids on the shape of the hydrophobic barrier of phospholipid bilayers. Biochimica et Biophysica Acta, 1368, 235–246.CrossRefPubMedGoogle Scholar
  61. 61.
    Kusumi, A., Subczynski, W. K., & Hyde, J. S. (1982). Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels. Proceedings of National Academic Sciences USA, 79, 1854–1858.CrossRefGoogle Scholar
  62. 62.
    Subczynski, W. K., Hyde, J. S., & Kusumi, A. (1989). Oxygen permeability of phosphatidylcholine-cholesterol membranes. Proceedings National Academic Sciences USA, 86, 4474–4478.CrossRefGoogle Scholar
  63. 63.
    Ashikawa, I., Yin, J.-J., Subczynski, W. K., Kouyama, T., Hyde, J. S., & Kusumi, A. (1994). Molecular organization and dynamics in bacteriorhodopsin-rich reconstituted membranes: discrimination of lipid environments by the oxygen transport parameter using a pulse ESR spin-labeling technique. Biochemistry, 33, 4947–4952.CrossRefPubMedGoogle Scholar
  64. 64.
    Subczynski, W. K., Widomska, J., Wisniewska, A., & Kusumi, A. (2007). Saturation-recovery electron paramagnetic resonance discrimination by oxygen transport (DOT) method for characterizing membrane domains. In T. J. McIntosh (Ed.) Methods in Molecular Biology, Lipid Rafts (pp. 143–157). Humana Press: Totowa.Google Scholar
  65. 65.
    Mainali, L., Raguz, M., & Subczynski, W. K. (2011). Phase-separation and domain-formation in cholesterol-sphingomyelin mixture: pulse-EPR oxygen probing. Biophysical Journal, 101, 837–846.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Subczynski, W. K., Raguz, M., & Widomska, J. (2010). Studying lipid organization in biological membranes using liposomes and EPR spin labeling. Methods in Molecular Biology, 606, 247–269.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Kawasaki, K., Yin, J.-J., Subczynski, W. K., Hyde, J. S., & Kusumi, A. (2001). Pulse EPR detection of lipid exchange between protein rich raft and bulk domains in the membrane: methodology development and its application to studies of influenza viral membrane. Biophysical Journal, 80, 738–748.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Raguz, M., Mainali, L., Widomska, J., & Subczynski, W. K. (2011). The immiscible cholesterol bilayer domain exists as an integral part of phospholipid bilayer membranes. Biochimica et Biophysica Acta, 1808, 1072–1080.CrossRefPubMedGoogle Scholar
  69. 69.
    Mitchell, P. (1961). Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature, 191, 144–148.CrossRefPubMedGoogle Scholar
  70. 70.
    Mannella, C. A. (2006). Structure and dynamics of the mitochondrial inner membrane cristae. Biochimica et Biophysica Acta, 1763, 542–548.CrossRefPubMedGoogle Scholar
  71. 71.
    Schlame, M., Brody, S., & Hostetler, K. Y. (1993). Mitochondrial cardiolipin in diverse eukaryotes. Comparison of biosynthetic reactions and molecular acyl species. European Journal of Biochemistry, 212, 727–735.CrossRefPubMedGoogle Scholar
  72. 72.
    Schlame, M., Horvath, L., & Vigh, L. (1990). Relationship between lipid saturation and lipid-protein interaction in liver mitochondria modified by catalytic hydrogenation with reference to cardiolipin molecular species. The Biochemical Journal, 265, 79–85.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Simons, K., & Ikonen, E. (1997). Functional rafts in cell membranes. Nature, 387, 569–572.CrossRefPubMedGoogle Scholar
  74. 74.
    Zurzolo, C., van Meer, G., & Mayor, S. (2003). The order of rafts. Conference on microdomains, lipid rafts and caveolae. EMBO Reports, 4, 1117–1121.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Subczynski, W. K., & Kusumi, A. (2003). Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochimica et Biophysica Acta, 1610, 231–243.CrossRefPubMedGoogle Scholar
  76. 76.
    Mayor, S., & Rao, M. (2004). Rafts: scale-dependent, active lipid organization at the cell surface. Traffic (Copenhagen, Denmark), 5, 231–240.CrossRefGoogle Scholar
  77. 77.
    Mukherjee, S., & Maxfield, F. R. (2004). Membrane domains. Annual Review of Cell and Developmental Biology, 20, 839–866.CrossRefPubMedGoogle Scholar
  78. 78.
    Kusumi, A., Koyama-Honda, I., & Suzuki, K. (2004). Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic (Copenhagen, Denmark), 5, 213–230.CrossRefGoogle Scholar
  79. 79.
    Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., et al. (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annual Review of Biophysics and Biomolecular Structure, 34, 351–378.CrossRefPubMedGoogle Scholar
  80. 80.
    Kusumi, A., Ike, H., Nakada, C., Murase, K., & Fujiwara, T. (2005). Single-molecule tracking of membrane molecules: plasma membrane compartmentalization and dynamic assembly of raft-philic signaling molecules. Seminars in Immunology, 17, 3–21.CrossRefPubMedGoogle Scholar
  81. 81.
    Munro, S. (2003). Lipid rafts: elusive or illusive? Cell, 115, 377–388.CrossRefPubMedGoogle Scholar
  82. 82.
    Taner, S. B., Onfelt, B., Pirinen, N. J., McCann, F. E., Magee, A. I., & Davis, D. M. (2004). Control of immune responses by trafficking cell surface proteins, vesicles and lipid rafts to and from the immunological synapse. Traffic (Copenhagen, Denmark), 5, 651–661.CrossRefGoogle Scholar
  83. 83.
    van Meer, G., & Sprong, H. (2004). Membrane lipids and vesicular traffic. Current Opinion in Cell Biology, 16, 373–378.CrossRefPubMedGoogle Scholar
  84. 84.
    Plesnar, E., Subczynski, W. K., & Pasenkiewicz-Gierula, M. (2012). Saturation with cholesterol increases vertical order and smoothes the surface of the phosphatidylcholine bilayer: a molecular simulation study. Biochimica et Biophysica Acta, 1818, 520–529.CrossRefPubMedGoogle Scholar
  85. 85.
    Kusumi, A., & Pasenkiewicz-Gierula, M. (1988). Rotational diffusion of a steroid molecule in phosphatidylcholine membranes: effects of alkyl chain length, unsaturation, and cholesterol as studied by a spin-label method. Biochemistry, 27, 4407–4415.CrossRefPubMedGoogle Scholar
  86. 86.
    Subczynski, W. K., Hopwood, L. E., & Hyde, J. S. (1992). Is the mammalian cell plasma membrane a barrier to oxygen transport? Journal of General Physiology, 100, 69–87.CrossRefPubMedGoogle Scholar
  87. 87.
    Rog, T., & Pasenkiewicz-Gierula, M. (2006). Cholesterol-sphingomyelin interactions: a molecular dynamics simulation study. Biophysical Journal, 91, 3756–3767.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Harding, J. J. (1997). Biochemistry of the eye. In J. J. Harding (Ed.), Lens (pp. 94–135). London: Chapman and Hall.Google Scholar
  89. 89.
    Lynnerup, N., Kjeldsen, H., Heegaard, S., Jacobsen, C., & Heinemeier, J. (2008). Radiocarbon dating of the human eye lens crystallines reveal proteins without carbon turnover throughout life. PloS One, 3, e1529.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Mainali, L., Raguz, M., O’Brien, W.J., & Subczynski, W.K. (2016). Changes in the properties and organization of human lens lipid membranes occurring with age. Current Eye Research, doi: 10.1080/02713683.02712016.01231325.
  91. 91.
    Yappert, M. C., Rujoi, M., Borchman, D., Vorobyov, I., & Estrada, R. (2003). Glycero- versus sphingo-phospholipids: correlations with human and non-human mammalian lens growth. Experimental Eye Research, 76, 725–734.CrossRefPubMedGoogle Scholar
  92. 92.
    Rujoi, M., Jin, J., Borchman, D., Tang, D., & Yappert, M. C. (2003). Isolation and lipid characterization of cholesterol-enriched fractions in cortical and nuclear human lens fibers. Investigative Ophthalmology and Visual Science, 44, 1634–1642.CrossRefPubMedGoogle Scholar
  93. 93.
    Mainali, L., Raguz, M., O’Brien, W. J., & Subczynski, W. K. (2015). Properties of membranes derived from the total lipids extracted from clear and cataractous lenses of 61-70-year-old human donors. European Biophysics Journal, 44, 91–102.CrossRefPubMedGoogle Scholar
  94. 94.
    Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., et al. (2010). NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature, 464, 1357–1361.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Jacob, R. F., Cenedella, R. J., & Mason, R. P. (2001). Evidence for distinct cholesterol domains in fiber cell membranes from cataractous human lenses. Journal of Biological Chemistry, 276, 13573–13578.CrossRefPubMedGoogle Scholar
  96. 96.
    Kusumi, A., Tsuda, M., Akino, T., Ohnishi, S., & Terayama, Y. (1983). Protein-phospholipid-cholesterol interaction in the photolysis of invertebrate rhodopsin. Biochemistry, 22, 1165–1170.CrossRefPubMedGoogle Scholar
  97. 97.
    Kusumi, A., Subczynski, W. K., Pasenkiewicz-Gierula, M., Hyde, J. S., & Merkle, H. (1986). Spin-label studies on phosphatidylcholine-cholesterol membranes: effects of alkyl chain length and unsaturation in the fluid phase. Biochimica et Biophysica Acta, 854, 307–317.CrossRefPubMedGoogle Scholar
  98. 98.
    Subczynski, W. K., & Wisniewska, A. (2000). Physical properties of lipid bilayer membranes: relevance to membrane biological functions. Acta Biochimica Polonica, 47, 613–625.PubMedGoogle Scholar
  99. 99.
    Rog, T., & Pasenkiewicz-Gierula, M. (2006). Cholesterol effects on a mixed-chain phosphatidylcholine bilayer: a molecular dynamics simulation study. Biochimie, 88, 449–460.CrossRefPubMedGoogle Scholar
  100. 100.
    Skulachev, V. P. (1990). Power transmission along biological membranes. Journal of Membrane Biology, 114, 97–112.CrossRefPubMedGoogle Scholar
  101. 101.
    Raguz, M., Widomska, J., Dillon, J., Gaillard, E. R., & Subczynski, W. K. (2009). Physical properties of the lipid bilayer membrane made of cortical and nuclear bovine lens lipids: EPR spin-labeling studies. Biochimica et Biophysica Acta, 1788, 2380–2388.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Loura, L. M., Fedorov, A., & Prieto, M. (2001). Fluid-fluid membrane microheterogeneity: a fluorescence resonance energy transfer study. Biophysical Journal, 80, 776–788.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of BiophysicsMedical College of WisconsinMilwaukeeUSA
  2. 2.Department of Computational Biophysics and BioinformaticsJagiellonian UniversityKrakowPoland
  3. 3.Department of BiophysicsMedical University of LublinLublinPoland
  4. 4.Department of Medical Physics and BiophysicsUniversity of SplitSplitCroatia

Personalised recommendations