Abstract
Specific molecular interactions that determine many of the functions of a biomembrane have a high probability of occurring at the surface of that membrane. However, unlike their hydrophobic core, the polar-apolar interface of biomembranes has been somewhat neglected experimentally. Reasons for this are that the chemical heterogeneity encountered makes a simple description difficult and that probing the membrane surface often involves a perturbation of those very interactions being studied. Classical methods for obtaining structural information about biomolecules, including X-ray diffraction, electron microscopy, and more recently high-resolution 2D nuclear magnetic resonance techniques are inappropriate for all but the simplest of membrane problems. In an effort to throw light on how membrane surfaces are organized, both architecturally and dynamically, protons in lipids and proteins have been selectively replaced by deuterons and the resultant deuterium NMR spectrum analyzed to give structural and dynamic information about the molecular associations between a range of membrane components. In principle, lipids, proteins, and oligosaccharides can be studied by this method and the information gained related to biochemical integrity and function. With one or two notable exceptions, the majority of the studies reported so far have been on model systems. A comprehensive review of the literature will not be presented here. However, protein-lipid molecular specificity in membranes, peptide-induced lateral separation, and the ionization behavior of deuterated phospholipids and peripheral proteins will all be demonstrated predominantly using deuterium NMR methods. Some suggestions for future work are also presented.
Similar content being viewed by others
Abbreviations
- csa:
-
chemical shift anisotropy (ppm)
- ΔνQ :
-
quadrupolar splitting (Hz)
- NMR:
-
nuclear magnetic resonance
- ESR:
-
electron spin resonance
- νex :
-
exchange rate (s−1)
- τc :
-
correlation time (s)
- DMPC:
-
1,2-dimyristoyl-sn-glycerol(3)phosphocholine
- PE:
-
1,2-diacyl-sn-glycerol(3)phosphoethanolamine
- PS:
-
1,2-diacyl-sn-glycerol(3)phosphoserine
- PG:
-
1,2-diacyl-sn-glycerol(3)phosphoglycerol
References
Abney, J. R., and Owicki, J. C. (1985).Progress in Protein-Lipid Interactions (Watts, A., and de Pont, J. J. H. H. M., eds.), Elsevier, Amsterdam, Vol. 1, Chapter 1.
Akutsu, H., and Seelig, J. (1981).Biochemistry 20, 7366–7373.
Allegrini, P. R., Plushke, G., and Seelig, J. (1984).Biochemistry 23, 6452–6458.
Allegrini, P. R., van Scharrenburg, G. J. M., Slotboom, A. J., de Haas, G. H., and Seelig, J. (1985).Biochemistry 24, 3268–3273.
Bloom, M. (1979).Can. J. Phys. 57, 2227–2230.
Bloom, M., and Smith, I. C. P. (1985). InProgress in Protein-Lipid Interactions (Watts, A., and De Pont, J. J. H. H. M., eds.), Elsevier, Amsterdam, Vol. 1, Chapter 2.
Boggs, J. M., and Moscarello, M. A. (1978).J. Membr. Biol. 39, 75–96.
Boggs, J. M., Moscarello, M. A., and Papahadjopoulos, D. (1982). InLipid-Protein Interactions (Jost, P. C., and Griffith, O. H., eds.), Wiley-Interscience, New York, Vol. 2, Chapter 1.
Bowers, J. L., Smith, R. L., Coretsopoulos, C., Kunwar, A. C., Keniry, M., Shan, X., Gutowsky, H. S., and Oldfield, E. (1986). InProgress in Protein-Lipid Interactions (Watts, A., and De Pont, J. J. H. H. M., eds.), Elsevier, Amsterdam, Vol. 2, Chapter 3.
Brown, L. R., and Wüthrich, K. (1977).Biochim. Biophys. Acta 468, 389–410.
Brown, M. F., Seelig, J., and Häberlen, U. (1979).J. Chem. Phys. 70, 5045–5053.
Burnell, E. E., Cullis, P. R., and de Kruijff, B. (1980).Biochim. Biophys. Acta 603, 63–69.
Cevc, G., Watts, A., and Marsh, D. (1980).FEBS Lett. 120, 267–270.
Cross, T. A., and Opella, S. J. (1985).J. Mol. Biol. 182, 367–387.
Cullis, P. R., Verkleij, A. J., and Ververgaert, P. H. J. T. (1978).Biochim. Biophys. Acta 513, 11–20.
Cullis, P. R., De Kruijff, B., Hope, M. J., Nayar, R., Rietveld, A., and Verkleij, A. J. (1980).Biochim. Biophys. Acta 600, 625–635.
Dasseux, J.-L., Faucon, J.-F., Lafleur, M., Pezolet, M., and Dufourcq, J. (1984).Biochim. Biophys. Acta 510, 75–86.
Datema, K. P., Pauls, K. P., and Bloom, M. (1986).Biochemistry 25, 3796–3803.
Davis, J. H. (1983).Biochem. Biophys. Acta 737, 117–171.
Deese, A. J., and Dratz, E. A. (1986). InProgress in Protein-Lipid Interactions (Watts, A., and De Pont, J. J. H. H. M., eds.), Elsevier, Amsterdam, Vol. 2, Chapter 2.
De Kruijff, B., and Cullis, P. R. (1980).Biochim. Biophys. Acta 602, 477–490.
De Kruijff, B., Cullis, P. R., Verkleij, A. J., Hope, M. J., Van Echteld, C. J. A., Taraschi, T. F., Van Hoogevest, P., Killian, J. A., Rietveld, A., and Van der Steen, A. T. M. (1985a). InProgress in Protein-Lipid Interactions (Watts, A. and De Pont, J. J. H. H. M., eds.), Elsevier, Amsterdam, Vol. 1, Chapter 3.
De Kruijff, B., Cullis, P. R., Verkleij, A. H., Hope, M. J., Van Echteld, C. J. A., and Taraschi, T. F. (1985b). InThe Enzymes of Biological Membranes, 2nd edn, Vol. 1,Membrane Structure and Dynamics, Plenum Press, New York, pp. 131–204.
Dempsey, C. E., and Watts, A. (1987).Biochemistry 26, 5811–5816.
Dempsey, C. E., Ryba, N. J. P., and Watts, A. (1986).Biochemistry 25, 2180–2187.
Dempsey, C. E., Cryer, G., and Watts, A. (1987).FEBS Lett.,218, 173–177.
Devaux, P. F., and Seigneuret, M. (1985).Biochim. Biophys. Acta 822, 63–125.
Devaux, P. F., Hoatson, G. L., Favre, E., Fellmann, P., Farren, B., MacKay, A. L., and Bloom, M. (1986).Biochemistry 25, 3804–3812.
Diebler, G. E., Martenson, R. E., and Kles, M. W. (1972).Prep. Biochem. 2, 139–165.
Diebler, G. E., Martenson, R. E., and Kles, M. W. (1975).J. Neurochem. 24, 173–182.
Dufourc, E. J., Smith, I. C. P., and Dufourcq, J. (1986).Biochemistry 25, 6448–6455.
Dufourcq, J., Faucon, J-L., Fourche, G., Dasseux, J.-L., LeMaire, M., and Gulik-Krzywicki, T. (1986).Biochim. Biophys. Acta 859, 33–48.
El Mashak, E. M., and Tocanne, J. F. (1980).Biochim. Biophys. Acta 729, 44–52.
Engleman, D. M., and Zaccai, G. (1980).Proc. Natl. Acad. Sci. USA 77, 5894–5898.
Feingold, D. S., HsuChen, C. C., and Sud, I. J. (1974).Ann. N.Y. Acad. Sci. 235, 480–492.
Gally, H. U., Pluschke, G., Overath, P., and Seelig, J. (1979).Biochemistry 18, 5605–5610.
Gally, H. U., Pluschke, G., Overath, P., and Seelig, J. (1980).Biochemistry 19, 1638–1643.
Harbison, G. S., Smith, S. O., Pardoen, J. A., Courtin, J. M. L., Lugtenburg, J., Herzfield, J., Mathies, R. A., and Griffin, R. G. (1985).Biochemistry 24, 6955–6962.
Hartman, W., Galla, H. J., and Sackmann, E. (1978).Biochem. Biophys. Acta 510, 124–139.
Hauser, H., Pascher, I., Pearson, R. H., and Sundrell, S. (1981).Biochim. Biophys. Acta 650, 21–51.
Hippe, S., and Lüth, H. (1986).J. Theor. Biol. 121, 351–366.
HsuChen, C. C., and Feingold, D. S. (1973).Biochemistry 12, 2105–2111.
Hunt, M. J., and McKay, A. L. (1976).J. Magn. Reson. 22, 295–301.
Israelachivili, J. N., Marcelja, S., and Horn, R. G. (1980).Q. Rev. Biophys. 13, 121–200.
Knowles, P. F., Watts, A., and Marsh, D. (1981).Biochemistry 20, 5888–5894.
Lavialle, F., Levin, I., and Molloy, C. (1980).Biochim. Biophys. Acta,600, 62–71.
Marsh, D., and Watts, A. (1982). InLipid-Protein Interactions (Jost, P. C., and Griffith, O. H., eds.), Wiley-Interscience, New York, Vol. 2, Chapter 2.
Marsh, D., and Watts, A. (1987). InAdvances in Membrane Fluidity (Aloia, R. C., ed.), Alan R. Liss Inc., New York, Vol. 2.
Marsh, D., Phillips, A. D., Watts, A., and Knowles, P. F. (1971).Biochim. Biophys. Res. Commun. 49, 641–648.
Meier, P., Ohmes, E., and Kothe, G. (1986).J. Chem. Phys. 85, 3598–3614.
Mühlebach, T., and Cherry, R. J. (1985).Biochemistry 24, 975–983.
Müller, K., Meier, P., and Kothe, G. (1985).Prog. Nucl. Magn. Reson. Spectrosc. 17, 211–239.
Oldfield, E., Gilmore, R., Glaser, M., Gutowsky, M. S., Hsung, J. C., Kang, S. Y., King, T. E., Meadows, M., and Rice, D. (1978).Proc. Natl. Acad. Sci. USA 75, 4657–4660.
Paddy, M. R., Dalquist, F. W., Davis, J. H., and Bloom, M. (1981).Biochemistry 20, 3152–3162.
Powell, G. L., Knowles, P. F., and Marsh, D. (1985).Biochim. Biophys. Acta 816, 191–194.
Quinn, P., and Dawson, R. M. C. (1969).Biochem. J. 115, 65–75.
Rand, R. P., and Sengupta (1972).Biochem. Biophys. Acta 255, 484–492.
Ryba, N. J. P., Dempsey, C. E., and Watts, A. (1986).Biochemistry 25, 4818–4825.
Seelig, J. (1977).Q. Rev. Biophys. 10, 353–418.
Seelig, J., and Seelig, A. (1980).Q. Rev. Biophys. 13, 9–61.
Seelig, J., and Seelig, A. (1985).Biochim. Biophys. Acta 815, 153–158.
Seelig, J., Seelig, A., and Tamm, L. (1982). InLipid-Protein Interactions (Jost, P. C., and Griffith, O. H., eds.), Wiley-Interscience, New York, Vol. 2, Chapter 3.
Sixl, F., and Galla, H. J. (1981).Biochim. Biophys. Acta 643, 626–635.
Sixl, F., and Watts, A. (1982).Biochemistry 21, 6446–6452.
Sixl, F., and Watts, A. (1983).Proc. Natl. Acad. Sci. USA 80, 1613–1615.
Sixl, F., and Watts, A. (1985).Biochemistry 24, 7906–7910.
Sixl, F., Brophy, P. J., and Watts, A. (1984).Biochemistry 23, 2032–2039.
Tamm, L., and Seelig, L. (1983).Biochemistry 22, 1474–1483.
Van, S. P., and Griffith, O. H. (1975).J. Membr. Biol. 20, 155–170.
Watts, A. (1986).Stud. Biophys. 110, 149–154.
Watts, A. (1987a). InMembrane Receptors, Dynamics and Energetics (Wirtz, K. A. W., ed.), Plenum Press, New York, pp. 329–339.
Watts, A. (1987b).Bull. Mag. Reson., in press.
Watts, A., and Poile, T. P. (1986).Biochim. Biophys. Acta 861, 368–372.
Watts, A., Harlos, K., Maschke, W., and Marsh, D. (1978).Biochim. Biophys. Acta 510, 63–74.
Watts, A., Sixl, F., Ryba, N. J. P., Dempsey, C. E., and Brophy, P. J. (1985). InMagnetic Resonance in Biology and Medicine (Govil, G., Khetrapal, C. L., and Saran, A., eds.), Tata-McGraw Hill, New Delhi.
Wohlegemuth, R., Waespe-Sarcevic, N., and Seelig, J. (1980).Biochemistry 19, 3315–3321.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Watts, A. Nuclear magnetic resonance methods to characterize lipid-protein interactions at membrane surfaces. J Bioenerg Biomembr 19, 625–653 (1987). https://doi.org/10.1007/BF00762300
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00762300