Structure, dynamics and composition of the lipid-protein interface. Perspectives from spin-labelling

Biochimica et Biophysica Acta - Reviews on Biomembranes

Volumn 1376, Issue 3, 1998, Pages 267-296

  Marsh, Derek ^a   Horváth, László I ^b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

Electron paramagnetic resonance; Integral protein; Lipid selectivity; Lipid protein interaction; Protein insertion; Spin label; Transmembrane peptide

Indexed keywords

DYNAMICS; ELECTRON SPIN RESONANCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW; SPIN LABELING; STOICHIOMETRY;

AMINO ACID SEQUENCE; ANIMALS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; HYDROGEN-ION CONCENTRATION; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA;

EID: 0344589334     PISSN: 03044157     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-4157(98)00009-4     Document Type: Review

References (114)

1. Lange A., Marsh D., Wassmer K.-H., Meier P., Kothe G. Electron spin resonance study of phospholipid membranes employing a comprehensive line-shape model. Biochemistry. 24:1985;4383-4392.
2. Moser M., Marsh D., Meier P., Wassmer K.-H., Kothe G. Chain configuration and flexibility gradient in phospholipid membranes. Comparison between spin-label electron spin resonance and deuteron nuclear magnetic resonance, and identification of new conformations. Biophys. J. 55:1989;111-123.
3. D. Marsh, ESR spin label studies of lipid-protein interactions, in: A. Watts, J.J.H.H.M. de Pont (Eds.), Progress in Protein-Lipid Interactions, vol. 1, ch. 4, Elsevier, Amsterdam, 1985, pp. 143-172.
4. D. Marsh, A. Watts, Spin-labeling and lipid-protein interactions in membranes, in: P.C. Jost, O.H. Griffith (Eds.), Lipid-Protein Interactions, vol. 2, Wiley-Interscience, New York, 1982, pp. 53-126.
5. D. Marsh, The nature of the lipid-protein interface and the influence of protein structure on protein-lipid interactions, in: A. Watts (Ed.), New Comprehensive Biochemistry, vol. 25, Protein-Lipid Interactions, Elsevier, Amsterdam, 1993, pp. 41-66.
6. D. Marsh, Lipid selectivity and integral protein structure, in: G. Pifat-Mrzljak (Ed.), Supramolecular Structure and Function (Dubrovnik, Yugoslavia, Sept. 16-28, 1987), 1988, World Scientific, Singapore, pp. 82-108.
7. Marsh D. Selectivity of lipid-protein interactions. J. Bioenerg. Biomembr. 19:1987;677-689.
8. D. Marsh, Experimental methods in spin-label spectral analysis, in: L.J. Berliner, J. Reuben (Eds.), Biological Magnetic Resonance, vol. 8, Plenum, New York, 1989, pp. 255-303.
9. D. Marsh, L.I. Horváth, Spin-label studies of the structure and dynamics of lipids and proteins in membranes, in: A.J. Hoff (Ed.), Advanced EPR. Applications in Biology and Biochemistry, Elsevier, Amsterdam, 1989, pp. 707-752.
10. Pates R.D., Marsh D. Lipid mobility and order in bovine rod outer segment disk membranes. A spin-label study of lipid-protein interactions. Biochemistry. 26:1987;29-39.
11. Knowles P.F., Watts A., Marsh D. Spin label studies of lipid immobilization in dimyristoylphosphatidylcholine-substituted cytochrome oxidase. Biochemistry. 18:1979;4480-4487.
12. +)-ATPase membranes from rectal glands of Squalus acanthias. Biochemistry. 24:1985;1386-1393.
13. Marsh D., Barrantes F.J. Immobilized lipid in acetylcholine receptor-rich membranes from Torpedo marmorata. Proc. Natl. Acad. Sci. U.S.A. 75:1978;4329-4333.
14. Watts A., Volotovski I.D., Marsh D. Rhodopsin-lipid associations in bovine rod outer segment membranes. Identification of immobilized lipid by spin labels. Biochemistry. 18:1979;5006-5013.
15. Sachse J.-H., King M.D., Marsh D. ESR determination of lipid diffusion coefficients at low spin-label concentrations in biological membranes, using exchange broadening, exchange narrowing, and dipole-dipole interactions. J. Magn. Reson. 71:1987;385-404.
16. King M.D., Sachse J.-H., Marsh D. Unconstrained optimization method for interpreting the concentration and temperature dependence of the linewidths of interacting nitroxide spin labels. Application to the measurement of translational diffusion coefficients of spin-labeled phospholipids in membranes. J. Magn. Reson. 72:1987;257-267.
17. Marsh D. Progressive saturation and saturation transfer ESR for measuring exchange processes of spin-labelled lipids and proteins in membranes. Chem. Soc. Rev. 22:1993;329-335.
18. Horváth L.I., Brophy P.J., Marsh D. Microwave frequency dependence of ESR spectra from spin labels undergoing two-site exchange in myelin proteolipid membranes. J. Magn. Reson. B 105:1994;120-128.
19. Brotherus J.R., Griffith O.H., Brotherus M.O., Jost P.C., Silvius J.R., Hokin L.E. Lipid-protein multiple binding equilibria in membranes. Biochemistry. 20:1981;5261-5267.
20. Powell G.L., Knowles P.F., Marsh D. Association of spin-labelled cardiolipin with dimyristoylphosphatidylcholine-substituted bovine heart cytochrome c oxidase. A generalized specificity increase rather than highly specific binding sites. Biochim. Biophys. Acta. 816:1985;191-194.
21. Knowles P.F., Marsh D. Magnetic resonance of membranes. Biochem. J. 274:1991;625-641.
22. Ellena J.F., Blazing M.A., McNamee M.G. Lipid-protein interactions in reconstituted membranes containing acetylcholine receptor. Biochemistry. 22:1983;5523-5535.
23. G.L. Powell, C.-A. Yu, D. Marsh, Stoichiometry and selectivity of lipid-protein interactions with bovine mitochondrial cytochrome c reductase, 1998, submitted.
24. +-Pump, Part A: Molecular Aspects. Progress in Clinical and Biological Research, vol. 268A, Alan Liss, New York, 1988, pp. 189-196.
25. 2+-ATPase. Biochemistry. 23:1984;538-547.
26. Thomas D.D., Bigelow D.J., Squier T.C., Hidalgo C.H. Rotational dynamics of protein and boundary lipid in sarcoplasmic reticulum membrane. Biophys. J. 37:1982;217-225.
27. Ryba N.J.P., Horváth L.I., Watts A., Marsh D. Molecular exchange at the lipid-rhodopsin interface: spin label electron spin resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. Biochemistry. 26:1987;3234-3240.
28. Pates R.D., Watts A., Uhl R., Marsh D. Lipid-protein interactions in frog rod outer segment disc membranes. Characterization by spin labels. Biochim. Biophys. Acta. 814:1985;389-397.
29. Horváth L.I., Drees M., Beyer K., Klingenberg M., Marsh D. Lipid-protein interactions in ADP-ATP carrier/egg phosphatidylcholine recombinants studied by spin-label ESR spectroscopy. Biochemistry. 29:1990;10664-10669.
30. Brophy P.J., Horváth L.I., Marsh D. Stoichiometry and specificity of lipid-protein interaction with myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry. 23:1984;860-865.
31. Páli T., Finbow M.E., Holzenburg A., Findlay J.B.C., Marsh D. Lipid-protein interactions and assembly of the 16-kDa channel polypeptide from Nephrops norvegicus. Studies with spin-label electron spin resonance spectroscopy and electron microscopy. Biochemistry. 34:1995;9211-9218.
32. Peelen S.J.C.J., Sanders J.C., Hemminga M.A., Marsh D. Stoichiometry, selectivity, and exchange dynamics of lipid-protein interaction with bacteriophage M13 coat protein studied by spin label electron spin resonance. Effects of protein secondary structure. Biochemistry. 31:1992;2670-2677.
33. Cornea R.L., Jones L.R., Autry J.M., Thomas D.D. Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers. Biochemistry. 36:1997;2960-2967.
34. + channel-associated peptide in the β-conformation. Spin label ESR studies. Biophys. J. 73:1997;2588-2594.
35. + channel-associated peptide in a lipid bilayer: conformation, lipid-protein interactions, and rotational diffusion. Biochemistry. 34:1995;3893-3898.
36. Marsh D. Stoichiometry of lipid-protein interaction and integral membrane protein structure. Eur. Biophys. J. 26:1997;203-208.
37. M.S.P. Sansom, I.D. Kerr, Principles of membrane protein structure, in: A.G. Lee (Ed.), Biomembranes, vol. 1, JAI Press, Greenwich, CT, 1995, pp. 29-78.
38. D. Marsh, Handbook of Lipid Bilayers, CRC Press, Boca Raton, FL, 1990.
39. Ryba N.J.P., Marsh D. Protein rotational diffusion and lipid/protein interactions in recombinants of bovine rhodopsin with saturated diacylphosphatidylcholines of different chain lengths studied by conventional and saturation transfer electron spin resonance. Biochemistry. 31:1992;7511-7518.
40. Weimbs T., Stoffel W. Proteolipid protein (PLP) of CNS myelin: positions of free, disulfide-bonded, and fatty acid thioester-linked cysteine residues and implications for the membrane topology of PLP. Biochemistry. 31:1992;12289-12296.
41. Holzenburg A., Jones P.C., Franklin T., Páli T., Heimburg T., Marsh D., Findlay J.B.C., Finbow M.E. Evidence for a common structure for a class of membrane channels. Eur. J. Biochem. 213:1993;21-30.
42. Møller J.V., Juul B., LeMaire M. Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim. Biophys. Acta. 1286:1996;1-51.
43. 2+) ATPase from sarcoplasmic reticulum leads to a highly hydrophobic proteinaceous residue with a mainly α helical structure. Biochemistry. 33:1994;8247-8254.
44. +-ATPase and of its membrane-associated proteolytic peptides. J. Biol. Chem. 270:1995;17685-17696.
45. Heimburg T., Esmann M., Marsh D. Characterization of the secondary structure and assembly of the transmembrane domains of trypsinized Na,K-ATPase by Fourier transform infrared spectroscopy. J. Biol. Chem. 272:1997;25685-25692.
46. 1 complex. Biochim. Biophys. Acta. 1275:1996;47-53.
47. Unwin N. Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229:1993;1101-1124.
48. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh R., Nakashima R., Yaono R., Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å Science. 272:1996;1136-1144.
49. R.D.B. Fraser, T.P. MacRea, Conformation in Fibrous Proteins and Related Synthetic Peptides, Academic Press, New York, 1973.
50. Marsh D. Peptide models for membrane channels. Biochem. J. 315:1996;345-361.
51. Aggeli A., Boden N., Cheng Y.-L., Findlay J.B.C., Knowles P.F., Kovatchev P., Turnbull P.J.H., Horváth L.I., Marsh D. Peptides modelled on the transmembrane region of the slow-voltage-gated IsK potassium channel: structural characterization of peptide assemblies in the β-strand conformation. Biochemistry. 35:1996;16213-16221.
52. Marsh D. Dichroic ratios in polarized Fourier Transform Infrared for nonaxial symmetry of β-sheet structures. Biophys. J. 72:1997;2710-2718.
53. Meier P., Sachse J.-H., Brophy P.J., Marsh D., Kothe G. Integral membrane proteins significantly decrease the molecular motion in lipid bilayers: a deuteron NMR relaxation study of membranes containing myelin proteolipid apoprotein. Proc. Natl. Acad. Sci. U.S.A. 84:1987;3704-3708.
54. M. Bloom, I.C.P. Smith, Manifestations of lipid-protein interactions in deuterium NMR, in: A. Watts, J.J.H.H.M. de Pont (Eds.), Progress in Protein-Lipid Interactions, vol. 1, Elsevier, Amsterdam, 1985, pp. 61-88.
55. Bretscher M.S., Munro S. Cholesterol and the Golgi apparatus. Science. 261:1993;1280-1281.
56. Pelham H.R.B., Munro S. Sorting of membrane proteins in the secretory pathway. Cell. 75:1993;603-605.
57. 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A, Biochemistry (1998) 9333-9345.
58. Killian J.A. Gramicidin and gramicidin-lipid interactions. Biochim. Biophys. Acta. 1113:1992;391-425.
59. Marsh D. Spin label answers to lipid-protein interactions. Trends Biochem. Sci. 8:1983;330-333.
60. Bienvenue A., Bloom M., Davis J.H., Devaux P.F. Evidence for protein-associated lipids from deuterium nuclear magnetic resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. J. Biol. Chem. 257:1982;3032-3038.
61. Marsh D. Lipid-protein interactions and heterogeneous lipid distribution in membranes. Mol. Membr. Biol. 12:1995;59-64.
62. Horváth L.I., Brophy P.J., Marsh D. Influence of polar residue deletions on lipid-protein interactions with the myelin proteolipid protein. Spin-label ESR studies with DM-20/lipid recombinants. Biochemistry. 29:1990;2635-2638.
63. Sankaram M.B., Brophy P.J., Marsh D. Lipid-protein and protein-protein interactions in double recombinants of myelin proteolipid apoprotein and myelin basic protein with dimyristoylphosphatidylglycerol. Biochemistry. 30:1991;5866-5873.
64. Knowles P.F., Watts A., Marsh D. Spin label studies of headgroup specificity in the interaction of phospholipids with yeast cytochrome oxidase. Biochemistry. 20:1981;5888-5894.
65. Raines D.E., Miller K.W. The role of charge in lipid selectivity for the nicotinic acetylcholine receptor. Biophys J. 64:1993;632-641.
66. Datema K.P., Wolfs C.J.A.M., Marsh D., Watts A., Hemminga M.A. Spin-label electron spin resonance study of bacteriophage M13 coat protein incorporation into mixed lipid bilayers. Biochemistry. 26:1987;7571-7574.
67. Marsh D., Watts A., Pates R.D., Uhl R., Knowles P.F., Esmann M. ESR spin label studies of lipid-protein interactions in membranes. Biophys. J. 37:1982;265-274.
68. Horváth L.I., Brophy P.J., Marsh D. Influence of lipid headgroup on the specificity and exchange dynamics in lipid-protein interactions. A spin label study of myelin proteolipid apoprotein-phospholipid complexes. Biochemistry. 27:1988;5296-5304.
69. +-ATPase membranes from Squalus acanthias. Biochemistry. 24:1985;3572-3578.
70. Powell G.L., Knowles P.F., Marsh D. Spin label studies on the specificity of interaction of cardiolipin with beef heart cytochrome oxidase. Biochemistry. 26:1987;8138-8145.
71. R.A. Robinson, R.H. Stokes, Electrolyte Solutions, Butterworths, London, 1955.
72. D. Marsh, Specificity of lipid-protein interactions, in: A.G. Lee (Ed.), Biomembranes, vol. 1, JAI Press, Greenwich, CT, 1995, pp. 137-186.
73. Cevc G., Watts A., Marsh D. Non-electrostatic contribution to the titration of the ordered-fluid phase transition of phosphatidylglycerol bilayers. FEBS Lett. 120:1980;267-270.
74. Cevc G., Watts A., Marsh D. Titration of the phase transition of phosphatidylserine bilayer membranes. Effects of pH, surface electrostatics, ion binding and headgroup hydration. Biochemistry. 20:1981;4955-4965.
75. G. Cevc, D. Marsh, Phospholipid Bilayers. Physical Principles and Models, Wiley-Interscience, New York, 1987.
76. 31P-NMR studies of the cubic and inverted hexagonal phases of dimyristoylphosphatidylcholine/myristic acid (1:2, mol/mol) mixtures. Biochim. Biophys. Acta. 1024:1990;89-94.
77. Miyazaki J., Hideg K., Marsh D. Interfacial ionization and partitioning of membrane-bound local anaesthetics. Biochim. Biophys. Acta. 1103:1992;62-68.
78. McMillen D.A., Volwerk J.J., Ohishi J., Erion M., Keanna J.F.W., Jost P.C., Griffith O.H. Identifying regions of membrane proteins in contact with phospholipid head groups: covalent attachment of a new class of aldehyde lipid labels to cytochrome c oxidase. Biochemistry. 25:1986;182-193.
79. Kuppe A., Mrsny R.J., Shimizu M., Firsan S.J., Keana J.F.W., Griffith O.H. Labeling of bovine heart cytochrome c oxidase with analogues of phospholipids. Synthesis and reactivity of a new cardiolipin benzaldehyde probe. Biochemistry. 26:1987;7693-7701.
80. Lisanti M.P., Rodriguez-Boulan E. Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Biochem. Sci. 15:1990;113-118.
81. Simons K., Ikonen E. Functional rafts in cell membranes. Nature. 387:1997;569-572.
82. +)-ATPase membranes. Biochemistry. 27:1988;2398-2403.
83. Caffrey M., Feigenson G.W. Fluorescence quenching in model membranes 3. Relationship between calcium adenosinetriphosphatase enzyme activity and the affinity of the protein for phosphatidylcholines with different acyl chain characteristics . Biochemistry. 20:1981;1949-1961.
84. +-ATPase. Protein Eng. 5:1992;7-15.
85. Horváth L.I., Brophy P.J., Marsh D. Exchange rates at the lipid-protein interface of myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry. 27:1988;46-52.
86. Wolfs C.J.A.M., Horváth L.I., Marsh D., Watts A., Hemminga M.A. Spin-label ESR of bacteriophage M13 coat protein in mixed lipid bilayers. Characterization of molecular selectivity of charged phospholipids for the bacteriophage coat protein in lipid bilayers. Biochemistry. 28:1989;9995-10001.
87. East J.M., Melville D., Lee A.G. Exchange rates and numbers of annular lipids for the calcium and magnesium ion dependent adenosinetriphosphatase. Biochemistry. 24:1985;2615-2623.
88. Marsh D. Exchange and dipolar spin-spin interactions and rotational diffusion in saturation transfer EPR spectroscopy. Appl. Magn. Reson. 3:1992;53-65.
89. D. Marsh, T. Páli, L.I. Horváth, Progressive saturation and saturation transfer EPR for measuring exchange processes and proximity relations in membranes, in: L.J. Berliner (Ed.), Biological Magnetic Resonance, vol. 14, Spin Labeling: The Next Millenium, Plenum, New York, 1998, pp. 23-82.
90. Horváth L.I., Brophy P.J., Marsh D. Exchange rates at the lipid-protein interface of the myelin proteolipid protein determined by saturation transfer electron spin resonance and continuous wave saturation studies. Biophys. J. 64:1993;622-631.
91. M.B. Sankaram, D. Marsh, Protein-lipid interactions with peripheral membrane proteins, in: A. Watts (Ed.), New Comprehensive Biochemistry, vol. 25. Protein-Lipid Interactions, Elsevier, Amsterdam, 1993, pp. 127-162.
92. Görrissen H., Marsh D., Rietveld A., de Kruijff B. Apocytochrome c binding to negatively charged lipid dispersions studied by spin-label electron spin resonance. Biochemistry. 25:1986;2904-2910.
93. Sankaram M.B., Brophy P.J., Marsh D. Spin label ESR studies on the interaction of bovine spinal cord myelin basic protein with dimyristoylphosphatidylglycerol dispersions. Biochemistry. 28:1989;9685-9691.
94. Keller R.C.A., ten Berge D., Nouwen N., Snel M.M.E., Tommassen J., Marsh D., de Kruijff B. Mode of insertion of the signal sequence of a bacterial precursor protein into phospholipid bilayers as revealed by cysteine-based site-directed spectroscopy. Biochemistry. 35:1996;3063-3071.
95. Keller R.C.A., Snel M.M.E., de Kruijff B., Marsh D. SecA restricts, in a nucleotide-dependent manner, acyl chain mobility up to the center of a phospholipid bilayer. FEBS Lett. 358:1995;251-254.
96. Snel M.M.E., de Kroon A.I.P.M., Marsh D. Mitochondrial presequence inserts differently into membranes containing cardiolipin and phosphatidylglycerol. Biochemistry. 34:1995;3605-3613.
97. Montich G.G., Montecucco C., Papini E., Marsh D. Insertion of diphtheria toxin in lipid bilayers studied by spin label ESR. Biochemistry. 34:1995;11561-11567.
98. Montich G.G., Marsh D. Interaction of α-lactalbumin with phosphatidylglycerol. Influence of protein binding on the lipid phase transition and lipid acyl chain mobility. Biochemistry. 34:1995;13139-13145.
99. Snel M.M.E., Marsh D. Membrane location of apocytochrome c and cytochrome c determined from lipid-protein spin exchange interactions by continuous wave saturation electron spin resonance. Biophys. J. 67:1994;737-745.
100. Snel M.M.E., de Kruijff B., Marsh D. Membrane location of spin-labeled apocytochrome c and cytochrome c determined by paramagnetic relaxation agents. Biochemistry. 33:1994;11150-11157.
101. Sankaram M.B., Brophy P.J., Marsh D. Interaction of two complementary fragments of the bovine spinal cord myelin basic protein with phospholipid bilayers. An ESR spin-label study. Biochemistry. 28:1989;9692-9698.
102. Sankaram M.B., Brophy P.J., Marsh D. Selectivity of interaction of phospholipids with bovine spinal cord myelin basic protein studied by spin-label electron spin resonance. Biochemistry. 28:1989;9699-9707.
103. Choe S., Bennett M.J., Fuji G., Curmi P.M., Kantardijeff K.A., Collier R.J., Eisenberg D. The crystal structure of diphtheria toxin. Nature. 357:1992;216-222.
104. Demel R., Schiavo G., de Kruijff B., Montecucco C. Lipid interaction of diphtheria toxin and mutants. A study with phospholipid and protein monolayers. Eur. J. Biochem. 19:1991;481-486.
105. Papini E., Schiavo G., Tomasi M., Colombatti M., Rappuli R., Montecucco C. Lipid interaction of diphtheria toxin and mutants with altered fragment B. Hydrophobic photolabelling and cell intoxication. Eur. J. Biochem. 169:1987;637-644.
106. Bychkova V.E., Pain R.H., Ptitsyn O.B. The 'molten globule' state is involved in the translocation of proteins across membranes? FEBS Lett. 238:1988;231-234.
107. Parker M.W., Pattus F. Rendering a membrane protein soluble in water: a common packing motif in bacterial protein toxins. Trends Biochem. Sci. 18:1993;391-395.
108. Grigorieff N., Ceska T.A., Downing K.H., Baldwin J.M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259:1996;393-421.
109. Marsh D., Livshits V.A., Páli T. Non-linear, continuous-wave EPR spectroscopy and spin-lattice relaxation: spin-label EPR methods for structure and dynamics. J. Chem. Soc., Perkin Trans. 2:1997;2545-2548.
110. Ahmed K., Thomas B.S. The effects of long chain fatty acids on sodium plus potassium ion-stimulated adenosine triphosphatase of rat brain. J. Biol. Chem. 246:1971;103-109.
111. Horváth L.I., Arias H.R., Hankovszky H.O., Hideg K., Barrantes F.J., Marsh D. Association of spin-labeled local anaesthetics at the hydrophobic surface of acetylcholine receptor in native membranes from Torpedo marmorata. Biochemistry. 29:1990;8707-8713.
112. Marsh D., Powell G.L. Properties of cardiolipin and functional implications for cytochrome oxidase activity. Bioelectrochem. Bioenerg. 20:1988;73-82.
113. Abramovitch D.A., Marsh D., Powell G.L. Activation of beef heart cytochrome oxidase by cardiolipin and analogues of cardiolipin. Biochim. Biophys. Acta. 1020:1990;34-42.
114. Perez-Gil J., Casals C., Marsh D. Interactions of hydrophobic lung surfactant proteins SP-B and SP-C with dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers studied by electron spin resonance. Biochemistry. 34:1995;3964-3971.