Summary
Recent studies on the interactions of soluble proteins, membrane proteins and enzymes with phospholipid model membranes are reviewed. Similarities between the properties of such systems and the behavior of biomembranes, such as alterations in the redox potential of cytochromec after binding to membranes and effects of phospholipid fluidity on (Na + K) ATPase activity, are emphasized. The degree of correspondence between the behavior of model systems and natural membranes encourages the continuing use of model membranes in studies on protein-lipid interactions. However, some of the data on the increase of surface pressure of phospholipid monolayers by proteins and increases in the permeability of liposomes indicate that many soluble proteins also have a capability to interact hydrophobically with phospholipids. Thus a sharp distinction between both peripheral and integral membrane proteins and non-membrane proteins are not seen by these techniques. Cautious use of such studies, however, should lead to greater understanding of the molecular basis of cell membrane structure and function in normal and pathological states. Studies implicating protein-lipid interactions and (Na + K) ATPase activity in membrane alterations in disease states are also briefly discussed.
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References
Davson, H. and Danielli, J. F., The Permeability of Natural Membranes, 1952 edition, reprinted 1970 by Hofner Publishing Company, Darien, Conn.
Claude, A., J. Exp. Med. 84, 51–89 (1946).
Keilin, D., Proc. Roy. Soc. B. 106, 418–444 (1930).
Keilin, D. and Hartree, E. F., Proc. Roy. Soc. B. 122, 298–308 (1937).
Singer, S. J. and Nicolson, G. L., Science 175, 720–731 (1972).
Smith, L. and Stotz, E., J. Biol. Chem. 209, 819–828 (1954).
Vanderkooi, S. G., Biochim. Biophys. Acta 344, 307–345 (1974).
Jurtshuk, P. Jr., Sekuzu, I. and Green, D. E., Biochem. and Biophys. Res. Commun. 6, 76–80 (1961).
Coleman, R., Biochim. Biophys. Acta 300, 1–30 (1973).
Skou, J. C., Physiol. Rev. 45, 596–617 (1965).
Winzler, R. J., in: Red Cell Membrane Structure and Function, p. 157 (Jamieson, F. A. and Greenawalt, T. J., editors). J. B. Lippincott, Philadelphia, Penn. (1969).
Dahl, J. L. and Hokin, L. E., Ann. Rev. of Biochem. 43, 327–356 (1974).
Marchesi, V. T., Jackson, R. L., Segrest, J. P. and Kahane, I., Fed. Proc. 32, 1833–1837 (1973).
Kaplan, D. M. and Criddle, R. S., Physiol. Rev. 51, 249–272 (1971).
Singer, S. J., Ann. Rev. Biochem. 43, 805–833 (1974).
Makino, S., Reynolds, J. A. and Tanford, C., J. Biol. Chem. 248, 4926–4932 (1973).
Rouser, G., Nelson, G. J., Fleischer, S. and Simon, G., in: Biological Membrane Physical Fact and Function, pp. 5–69, (Chapman, D., editor) Academic Press, New York and London (1968).
Bangham, A. D., Standish, M. M. and Watkins, J. C., J. Mol. Biol. 13, 238–252 (1965).
Small, D. M., J. Lipid Res. 8, 551–557 (1967).
Papahadjopoulos, D. and Miller, N., Biochim. Biophys. Acta 135, 624–638 (1967).
Bangham, A. D., Hill, M. W. and Miller, N. G. A., in: Methods in Membrane Biology, 1, pp. 1–68, (Korn, E. D., editor) Plenum Press, New York and London (1974).
Mueller, P., Rudin, D. O., Tien, H. T. and Westcott, W. C., Nature 194, 979–980 (1962).
Steinemann, A. and Läuger, P., J. Membrane Biol. 4, 74–81 (1971).
Montal, M., J. Membrane Biol. 7, 245–266 (1972).
Steim, J. M., Tourtellotte, M. E., Reinert, J. C., McElhaney, R. N. and Rader, J. C., Proc. Nat. Acad. Sci. (U.S.A.) 63, 104–109 (1969).
Blazyk, J. F. and Steim, J. M., Biochim. Biophys. Acta 266, 737–741 (1972).
Shipley, G. G., in: Biological Membranes, (Chapman, D. and Wallach, D. F. H., editors) 2, pp. 1–89, Academic Press, London and New York (1973).
Chapman, D., in: Biological Membranes, (Chapman, D. and Wallach, D. F. H., editors) 2, pp. 91–144, Academic Press, London and New York (1973).
Bretscher, M. S., Science 181, 622–629 (1973).
Gitler, C., Ann. Rev. Biophys. and Bioengineering 1, 51–92 (1972).
Sweet, C. and Zull, J. E., Biochim. Biophys. Acta 173, 94–103 (1969).
Kimelberg, H. K. and Papahadjopoulos, D., J. Biol. Chem. 246, 1142–1148 (1971).
Papahadjopoulos, D., Biochim. Biophys. Acta 241, 254–259 (1971).
Calissano, P., Alema, S. and Rusca, G., Biochim. Biophys. Acta 255, 1009–1013 (1972).
Kaplan, J. H., Biochim. Biophys. Acta 311, 1–5 (1973).
Kimelberg, H. K., Lee, C. P., Claude, A. and Mrena, E., J. Membrane Biol. 2, 235–251 (1970).
Kimelberg, H. K. and Papahadjopoulos, D., Biochim. Biophys. Acta 233, 805–809 (1971).
Gulik-Krzywicki, T., Schechter, E., Luzzati, V. and Faure, M., Nature 223, 1116–1121 (1969).
Kamat, V. B., Chapman, D., Zwaal, R. F. A. and Van Deenen, L. L. M., Chem. Phys. Lipids 4, 323–331 (1970).
Mukai, K., Land, C. M. and Chesnut, D. B., Chem. Phys. Lipids 9, 196–216 (1972).
Vanderkooi, J., Erecinska, M. and Chance, B., Arch. Biochem. and Biophys. 154, 219–229 (1973).
Papahadjopoulos, D., Jacobson, K., Nir, S. and Isac, T., Biochim. Biophys. Acta 311, 330–348 (1973).
De Gier, J., Mandersloot, J. G. and Van Deenen, L. L. M., Biochim. Biophys. Acta 150, 666–675 (1969).
Papahadjopoulos, D., Cowden, M. and Kimelberg, H. K., Biochim. Biophys. Acta 330, 8–26 (1973).
Tenenbaum, D. and Folch-Pi, J., Biochim. Biophys. Acta 115, 141–147 (1966).
Juliano, R. L., Kimelberg, H. K. and Papahadjopoulos, D., Biochim. Biophys. Acta 241, 894–905 (1971).
Dawson, R. M. C. and Quinn, P. J., in: Membrane-Bound Enzymes, (Porcellati, G. and di Jeso, F., editors) p. 1, Plenum Press, New York and London (1971).
Nicholls, P., Biochim. Biophys. Acta 346, 261–310 (1974).
Kimelberg, H. K., Ph.D. Dissertation, State University of New York at Buffalo, University Microfilms Ltd. Ann Arbor, Michigan (1968).
Kimelberg, H. K. and Lee, C. P., Biochim. Biophys. Res. Comm., 34, 784–790 (1969).
Dickerson, R. E., Takano, T., Eisenberg, D., Kallai, O. B., Samson, L., Cooper, A. and Margoliash, E., J. Biol. Chem. 246, 1511–1535 (1971).
Colacicco, G., Lipids 5, 636–649 (1970).
Bigelow, C. C., J. Theoret. Biol. 16, 187–211 (1967).
Helenius, A. and Simons, K., J. Biol. Chem. 247, 3656–3661 (1972).
Neer, E. J., J. Biol. Chem. 249, 6527–6531 (1974).
Hammes, G. G. and Schullery, S. E., Biochemistry 9, 2555–2563 (1970).
Letellier, L. and Schechter, E., Eur. J. Biochem. 40, 507–512 (1973).
Kimelberg, H. K. and Lee, C. P., J. Membrane Biol. 2, 252–262 (1970).
Dutton, P. L., Wilson, D. F. and Lee, C. P., Biochemistry 9, 5077–5082 (1970).
Dutton, P. L. and Wilson, D. F., Biochim. Biophys. Acta 346, 165–212 (1974).
Nicolson, G. L. and Painter, R. G., J. Cell Biol. 59, 395–406 (1973).
O'Brien, J. S. and Sampson, E. L., J. Lipid Res. 6, 537–544 (1965).
London, Y., Demel, R. A., Van Kessel Geurts, W. S. M., Zahler, P. and Van Deenen, L. L. M., Biochim. Biophys. Acta 332, 69–84 (1974).
Demel, R. A., London, Y., Van Kessel Geurts, W. S. M., Vossenberg, F. G. A. and Van Deenen, L. L. M., Biochim. Biophys. Acta 311, 507–519 (1973).
London, Y., Demel, R. A., Van Kessel Guerts, W. S. M., Vossenberg, F. G. A. and Van Deenen, L. L. M., Biochim. Biophys. Acta 311, 520–530 (1973).
Wood, J. G., Dawson, R. M. C. and Hauser, H., J. of Neurochem. 22, 637–643 (1974).
Zwaal, R. F. A. and Van Deenen, L. L. M., Chem. Phys. Lipids 4, 311–322 (1970).
Tosteson, M. T., Lav, F. and Tosteson, D. C., Nature New Biology 243, 112 (1973).
Capaldi, R. A. and Vanderkooi, G., Proc. Nat. Acad. Sci. 69, 930–932 (1972).
Tanford, C., J. Mol. Biol. 67, 59–74 (1972).
Triggle, D. J., in: Recent Progress in Surface Science, (Danielli, J. F., Riddiford, A. C. and Rosenberg, M. D., editors) 3, pp. 273–290, Academic Press, New York (1970).
Kagawa, Y., Biochim. Biophys. Acta 265, 297–338 (1972).
Razin, S., Biochim. Biophys. Acta 265, 241–296 (1972).
Papahadjopoulos, D. and Kimelberg, H. K., in: Progress in Surface Science, (Davison, S. G., editor) 4, pp. 141–232, Pergamon Press, Oxford (1973).
Fourcans, B. and Jain, M. K., in: Advances in Lipid Research, (Paoletti, R. and Kritchevsky, D., editors) 12, pp. 147–226, Academic Press, New York and London (1974).
Katz, B., Muscle and Synapse, McGraw-Hill Inc., New York (1966).
Thomas, R. C., Physiological Reviews 52, 563–594 (1972).
Tosteson, D. C., in: The Cellular Functions of Membrane Transport, (Hoffman, J. E., editor) pp. 3–22, Prentice-Hall Inc., Englewood Cliffs (1963).
Quastel, M. R. and Kaplan, J. G., Exper. Cell Res. 63, 230–233 (1970).
Ohnishi, T. and Kawamura, H., J. of Biochem. 56, 377–378 (1964).
Kimelberg, H. K. and Papahadjopoulos, D., J. Biol. Chem. 249, 1071–1080 (1974).
Tanaka, R. and Strickland, K. P., Arch. Biochem. Biophys. 111, 583–592 (1965).
Fenster, L. J. and Copenhaver, J. H., Biochim. Biophys. Acta 137, 406–408 (1967).
Emmelot, P. and Bos, C. J., Biochim. Biophys. Acta 150, 341–353 (1968).
Noguchi, T. and Freed, S., Nature New Biol. 230, 148–150 (1971).
Jarnefelt, J., Biochim. Biophys. Acta 266, 91–96 (1972).
Roelofsen, B. and Van Deenen, L. L. M., Europ. J. of Biochem. 40, 245–257 (1973).
Goldman, S. S. and Albers, R. W., J. Biol. Chem. 243, 867–874 (1973).
De Pont, J. J. H. H. M., Van Prooijen-Van Eeden, A. and Bonting, S. L., Biochim. Biophys. Acta 323, 487–494 (1973).
Cook, A. M., Low, E. and Ishizimi, M., Nature New Biol. 239, 150–151 (1972).
Tanaka, R. and Sakamoto, T., Biochim. Biophys. Acta 193, 384–393 (1969).
Tanaka, R., Sakamoto, T. and Sakamoto, Y., J. Membrane Biol. 4, 42–51 (1971).
Sun, A. Y., Sun, G. Y. and Samorajski, T., J. of Neurochem. 18, 1711–1718 (1971).
Taniguchi, K. and Tonomura, Y., J. Biochem. 69, 543–557 (1971).
Kimelberg, H. K. and Papahadjopoulos, D., Biochim. Biophys. Acta 282, 277–292 (1972).
Hokin, L. E. and Hexum, T. D., Arch. Biochem. Biophys. 151, 453–463 (1972).
Wheeler, K. P. and Whittam, R., J. Physiol. 207, 303–328 (1970).
Raison, J. K., Bioenergetics 4, 285–309 (1973).
Overath, P., Schairer, H. U. and Stoffel, W., Proc. Nat. Acad. Sci. (U.S.A.) 67, 606–612 (1970).
Wilson, G., Rose, S. P. and Fox, C. F., Biochem. Biophys. Res. Commun. 38, 617–623 (1970).
Esfahani, M., Limbrick, A. R., Knutton, S., Oka, T. and Wakil, S. J., Proc. Nat. Acad. Sci. 68, 3180–3184 (1971).
Mavis, R. D. and Vagelos, P. R., J. Biol. Chem. 247, 652–659 (1972).
Ladbrooke, B. D., Williams, R. M. and Chapman, D., Biochim. Biophys. Acta 150, 333–340 (1968).
Trauble, H. and Eibl, H., Proc. Nat. Acad. Sci. 71, 214–219 (1974).
Hazel, J. R. and Prosser, C. L., Physiol. Reviews 54, 620–677 (1974).
Grisham, C. M. and Barnett, R. E., Biochem. 12, 2635–2637 (1973).
Linden, C. D., Wright, K. L., McConnell, H. M. and Fox, C. F., Proc. Nat. Acad. Sci. (U.S.A.) 70, 2271–2275 (1973).
Devaux, P. and McConnell, H. M., J. Amer. Chem. Soc. 94, 4475–4481 (1972).
Frye, L. D. and Edidin, M., J. Cell. Sci. 7, 319–335 (1970).
Kleeman, W. and McConnell, H. M., Biochim. Biophys. Acta 345, 220–230 (1974).
De Kruyff, B., Van Dijck, P. W. M., Goldbach, R. W., Denez, R. A. and Van Deenen, L. L. M., Biochim. Biophys. Acta 330, 269–282 (1973).
Chapman, D., Owens, N. F., Phillips, M. C. and Walker, D. A., Biochim. Biophys. Acta 183, 458–465 (1969).
Green, D. E. and Fleischer, S., Biochim. Biophys. Acta 70, 554–582 (1963).
Papahadjopoulos, D., Nir, S. and Ohki, S., Biochim. Biophys. Acta 266, 561–583 (1971).
Slack, J. R., Anderson, B. H. and Day, W. A., Biochim. Biophys. Acta 323, 547–559 (1973).
Hinkle, P. C., Kim, J. J. and Racker, E., J. Biol. Chem. 247, 1338–1339 (1972).
Goldin, S. M. and Tong, S. W., J. Biol. Chem. 249, 5907–5915 (1974).
Hilden, S., Rhee, H. M. and Hokin, L. E., J. Biol. Chem. 249, 7432–7440 (1974).
Warren, G. B., Toon, P. A., Birdsall, N. J. M., Lee, A. G. and Metcalfe, J. C., Proc. Nat. Acad. Sci. (U.S.A.) 71, 622–626 (1974).
Inesi, G., Millman, M. and Eletr, S., J. Mol. Biol. 81, 483–504 (1973).
Gruener, N. and Avi-Dor, Y., J. Biochem. 100, 762–767 (1966).
Swanson, P. D., J. Neurochem. 13, 229–236 (1966).
Charnock, J. S., Doty, D. M. and Russell, J. C., Arch. Biochem. Biophys. 142, 633–637 (1971).
Bowler, K. and Duncan, C. J., Comp. Biochem. Physiol. 24, 1043–1054 (1968).
Taniguchi, K. and Iida, S., Biochim. Biophys. Acta 274, 536–541 (1972).
Smith, M. W., Biochem. J. 105, 65–71 (1967).
Kimzey, S. L. and Willis, J. S., J. of General Physiology 58, 634–649 (1971).
Kemp, A., Groot, G. S. P. and Reitsna, H. J., Biochim. Biophys. Acta 180, 28–34 (1969).
Lyons, J. M. and Raison, J. K., Comp. Biochem. Physiol. 37, 405–411 (1970).
Lenaz, G., Sechi, A. M., Parenti-Castelli, G., Landi, L. and Bertoli, E., Biochem. Biophys. Res. Commun. 49, 536–542 (1972).
Watson, K., Bertoli, E. and Griffiths, D. E., FEBS Letters 30, 120–124 (1973).
Lee, M. P. and Gear, A. R. L., J. Biol. Chem. 249, 7541–7549 (1974).
Eletr, S., Zakin, D. and Vessey, D. A., J. Molec. Biol. 78, 351–362 (1973).
Kreiner, P. W., Keirns, J. J. and Bitensky, M. W., Proc. Nat. Acad. Sci. (U.S.A.) 70, 1785–1789 (1973).
Bar, H. P., Molec. Pharmacol. 10, 597–604 (1974).
Chapman, D. and Urbina, FEBS Letters 12, 169 (1971).
Papahadjopoulos, D. and Isac, T., Fed. Proc. 33, 1254 (1974).
Jost, P., Griffith, O. H., Capaldi, R. A. and Vanderkooi, G., Biochim. Biophys. Acta 311, 141–152 (1973).
Bergelson, L. D., Dyatlovitskaya, E. V., Torkovskaya, T. I., Sorokina, I. B. and Gorkova, N. P., Biochim. Biophys. Acta 210, 287–298 (1970).
Karlsson, K. A., Samuelsson, B. E., Schersten, T., Steen, G. O. and Wahlquist, L., Biochim. Biophys. Acta 337, 349–355 (1974).
Feo, F., Canuto, R. A., Bertone, G., Garcea, R. and Pani, P., FEBS Letters 33, 229–232 (1973).
Wallach, D. F. H., in: Biological Membranes, (Chapman, D. and Wallach, D. F. H., editors) 2, pp. 253–294, Academic Press, New York and London (1973).
Yanagihara, T. and Cummings, J. N., Brain 92, 59–70 (1969).
Suzuki, O. and Yagi, K., Experientia 30, 248 (1974).
Perdue, J. F., Kletzien, R., Miller, K., Pridmore, G. and Wray, V. L., Biochim. Biophys. Acta 249, 435–453 (1971).
Yau, T. M. and Weber, M. J., Biochem. Biophys. Res. Commun. 49, 114–120 (1972).
Sheinin, R. and Onoderce, K., Biochim. Biophys. Acta 274, 49–63 (1972).
Graham, J. M., Biochem. J. 130, 1113–1124 (1972).
Yoshikawada-Fukada, M. and Nojima, T., J. Cell. Physiol. 80, 421–430 (1972).
Patterson, M. K. Jr., J. of Nat. Cancer Inst. 53, 1493–1498 (1974).
Kasarov, L. B. and Briedman, H., Cancer Res. 34, 1862–1865 (1974).
Kimelberg, H. K. and Mayhew, E., J. Biol. Chem. 250, 100–104 (1975).
Verdouw, H. and Bertina, R. M., Biochim. Biophys. Acta 325, 385–396 (1973).
Weber, M. J., J. Biol. Chem. 248, 2978–2983 (1973).
Isselbacher, K. J., Proc. Nat. Acad. Sci. (U.S.A.) 69, 585–589 (1972).
Kimelberg, H. K., Fed. Proc. 34, 642 (1975).
Janicki, R. H. and Kinter, W. B., Nature New Biol. 233, 148–149 (1971).
Secchi, G., Alessio, L. and Cambiaghi, G., Arch. Environ. Health 27, 399–400 (1973).
Stastny, F., Antosova, E., Kostir, J. and Jilek, L., Brain Res. 33, 597–600 (1972).
Lim, R., De la Torre, J. C. and Mullan, S., Arch. Neurol. 27, 314–321 (1972).
Laws, E. R. and O'Connor, J. S., J. Neurosurg. 33, 167–171 (1970).
Bray, G. M., Biochim. Biophys. Acta 298, 239–245 (1973).
Palatini, P., Dabbeni-Sala, F. and Bruni, A., Biochim. Biophys. Acta 288, 413–422 (1972).
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Kimelberg, H.K. Protein-liposome interactions and their relevance to the structure and function of cell membranes. Mol Cell Biochem 10, 171–190 (1976). https://doi.org/10.1007/BF01731688
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DOI: https://doi.org/10.1007/BF01731688