Summary
The effect of myelin basic protein from normal human central nervous system on lipid organization has been investigated by studying model membranes containing the protein by differential scanning calorimetry or electron spin resonance spectroscopy. Basic protein was found to decrease the phase transition temperature of dipalmitoyl phosphatidyl-glycerol, phosphatidic acid, and phosphatidylserine. The protein had a greater effect on the freezing temperature, measured from the cooling scan, than on the melting temperature, measured from the heating scan. These results are consistent with partial penetration of parts of the protein into the hydrocarbon region of the bilayer in the liquid crystalline state and partial freezing out when the lipid has been cooled below its phase transition temperature.
The effect of the protein on fatty acid chain packing was investigated by using a series of fatty acid spin labels with the nitroxide group located at different positions along the chain. If the protein has not yet penetrated, it increases the order throughout the bilayer in the gel phase, probably by decreasing the repulsion between the lipid polar head groups. Above the phase transition temperature, when parts of it are able to penetrate, it decreases the motion of the lipid fatty acid chains greatly near the polar head group region, but has little or no effect near the interior of the bilayer. Upon cooling again the protein still decreases the motion near the polar head group region but increases it greatly in the interior. Thus, the protein penetrates partway into the bilayer, distorts the packing of the lipid fatty acid chains, and prevents recrystallization, thus decreasing the phase transition temperature.
The magnitude of the effect varied with the lipid and was greatest for phosphatidic acid and phosphatidylglycerol. It could be reversed upon cooling for phosphatidylglycerol but not phosphatidic acid. The protein was only observed to decrease the phase transition temperature of phosphatidylserine upon cooling. It had only a small effect on phosphatidylethanolamine and no effect on phosphatidylcholine. Thus, the protein may penetrate to a different extent into different lipids even if it binds to the polar head group region by electrostatic interactions.
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References
Akutsu, H., Kyogoku, Y. 1977. Conformational difference in the polar groups of phosphatidycholine and phosphatidylethanolamine in aqueous phase.Chem. Phys. Lipids 18:285
Bartlett, G.R. 1959. Phosphorus assay in column chromatography.J. Biol. Chem. 234:466
Boggs, J.M., Hsia, J.C. 1973. Structural characteristics of hydrated glycerol-and sphingolipids. A spin label study.Can. J. Biochem. 51:1451
Boggs, J.M., Vail, W.J., Moscarello, M.A. 1976. Preparation and properties of vesicles of a purified myelin hydrophobic protein and phospholipid. A spin label study.Biochim. Biophys. Acta 448:517
Dehlinger, P.J., Jost, P.C., Griffith, O.H. 1974. Lipid binding to the amphipathic membrane protein cytochromeb 5.Proc. Nat. Acad. Sci. USA 71:2280
Demel, R.A., London, Y., Geurts van Kessel, W.S.M., Vossenberg, F.G.A., Deenen, L.L.M. van 1973. The specific interaction of myelin basic protein with lipids at the air-water interface.Biochim. Biophys. Acta 311:507
Eletr, S., Keith, A.D. 1972. Spin label studies of dynamics of lipid alkyl chains in biological membranes: Role of unsaturated sites.Proc. Nat. Acad. Sci. USA 69:1353
Epand, R.M., Moscarello, M.A., Zirenberg, B., Vail, W.J. 1974. The folded conformation of the encephalitogenic protein of the human brain.Biochemistry 13:1264
Eylar, E.H. 1972. The structure and immunologic properties of basic proteins of myelin.Ann. N. Y. Acad. Sci. 195:481
Gally, H.-U., Niederberger, W., Seelig, J. 1975. Conformation and motion of the choline head group in bilayers of dipalmitoyl-3-sn-phosphatidylcholine.Biochemistry 14:3647
Gould, R.M., London, Y. 1972. Specific interaction of central nervous system myelin basic protein with lipids. Effects of basic protein on glucose leakage from liposomes.Biochim. Biophys. Acta 290:200
Hubbell, W.T., McConnell, H.M. 1971. Molecular motion in spin-labelled phospholipids and membranes.J. Am. Chem. Soc. 93:314
Jost, P.C., Griffith, O.H., Capaldi, R.A., Vanderkooi, G. 1973. Identification and extent of fluid bilayer regions in membranous cytochrome oxidase.Biochim. Biophys. Acta 311:141
Levine, Y.K., Birdsall, N.J.M., Lee, A.G., Metcalfe, J.C. 1972. C13 nuclear magnetic resonance relaxation measurements of synthetic lecithins and the effect of spin-labelled lipids.Biochemistry 11:1416
London, Y., Demel, R.A., Geurts van Kessel, W.S.M., Vossenberg, F.G.A., Deenen, L.L.M. van 1973. The protection of A1 myelin basic protein against the action of proteolytic enzymes after interaction of the protein with lipids at the air-water interface.Biochim. Biophys. Acta 311:520
London, Y., Vossenberg, F.G.A. 1973. Specific interaction of central nervous system myelin basic protein with lipids. Specific regions of the protein sequence protected from the proteolytic action of trypsin.Biochim. Biophys. Acta 307:478
Lowden, J.A., Moscarello, M.A., Morecki, R. 1966. The isolation and characterization of an acid soluble protein from myelin.Can. J. Biochem. Physiol. 44:567
Marchalonis, J.J. 1969. An enzymic method for the trace iodination of immunoglobulins and other proteins.Biochem. J. 113:299
Michaelson, D.M., Horwitz, A.F., Klein, M.P. 1974. Head group modulation of membrane fluidity.Biochemistry 13:2605
Palmer, F.P., Dawson, R.M.C. 1969. Complex formation between triphosphoinositide and experimental allergic encephalitogenic protein.Biochem. J. 111:637
Papahadjopoulos, D., Miller, N. 1967. Phospholipid model membranes. I. Structural characteristics of hydrated liquid crystals.Biochim. Biophys. Acta 135:624
Papahadjopoulos, D., Moscarello, M.A., Eylar, E.H., Isac, T. 1975a. Effects of proteins on thermotropic phase transitions of phospholipid membranes.Biochim. Biophys. Acta 401:317
Papahadjopoulos, D., Vail, W.J., Moscarello, M. 1975b. Interaction of a purified hydrophobic protein from myelin with phospholipid membranes: Studies on ultrastructure, phase transitions and permeability.J. Membrane Biol. 22:143
Phillips, M.C., Finer, E.G., Hauser, H. 1972. Differences between conformations of lecithin and phosphatidylethanolamine polar groups and their effects on interactions of phospholipid bilayer membranes.Biochim. Biophys. Acta 290:397
Rand, R.P., Tinker, D.O., Fast, P.G. 1971. Polymorphism of phosphatidylethanolamines from two natural sources.Chem. Phys. Lipids 6:333
Seelig, J. 1970. Spin label studies of oriented smectic liquid crystals (a model system for bilayer membranes).J. Am. Chem. Soc. 92:3881
Seelig, J., Gally, H.-U. 1976. Investigation of phosphatidylethanolamine bilayers by deuterium and phosphorus-31 nuclear magnetic resonance.Biochemistry 15:5199
Steck, A.J., Siegrist, H.P., Zahler, P., Herschkowitz, N.N. 1976. Lipid-protein interactions with native and modified myelin basic protein.Biochim. Biophys. Acta 455:343
Stollery, J.G. 1977. The Ultrastructure of Phosphatidylethanolamine Vesicles. M.Sc. Thesis, University of Guelph, Guelph (Ontario)
Vail, W.J., Papahadjopoulos, D., Moscarello, M.A. 1974. Interaction of a hydrophobic protein with liposomes. Evidence for particles seen in freeze fracture as being proteins.Biochim. Biophys. Acta 345:463
Van, S.P., Griffith, O.H. 1975. Bilayer structure in phospholipid-cytochrome c model membranes.J. Membrane Biol. 20:155
Yu, K.Y., Baldassare, J.J., Ho, C. 1974. Physical-chemical studies of phospholipids and poly(amino acids) interactions.Biochemistry 13:4375
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Boggs, J.M., Moscarello, M.A. Effect of basic protein from human central nervous system myelin on lipid bilayer structure. J. Membrain Biol. 39, 75–96 (1978). https://doi.org/10.1007/BF01872756
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DOI: https://doi.org/10.1007/BF01872756