Skip to main content

Thermodynamics of the Interaction of Proteins with Lipid Membranes

  • Chapter
Biological Membranes

Abstract

Peripheral proteins associated at the lipid surface are one of the major components of biological membranes. They may function in situ as electron carriers (e.g., cytochrome c), as enzymes (e.g., protein kinase C), as signal transduction proteins (e.g., G-proteins), or primarily as structural elements (e.g., spectrin and myelin basic protein). The protein density at the membrane surface can be relatively high, and the peripheral proteins may also interact with the exposed portions of integral proteins embedded within the membrane (e.g., with redox enzymes of the respiratory chain, or with receptors such as those to which G-proteins are coupled). The association with the membrane is most frequently of electrostatic origin but may also include surface adsorption and hydrophobic components. The interactions of the isolated peripheral proteins with lipid bi-layer membranes, therefore, are of direct relevance to the structure and function of biological membranes, and the determination of binding isotherms has proved to be particularly useful in the study of such interactions. Analysis of the latter constitutes the first and an important part of this chapter that is directly relevant to the thermodynamics of binding.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Albon N, Sturtevant JM (1978): Nature of the gel to liquid crystal transition of synthetic phosphatidylcholines. Proc Natl Acad Sci USA 75:2258–2260

    Article  PubMed  CAS  Google Scholar 

  • Apitz-Castro R, Jain MK, de Haas GH (1982): Origin of the latency phase during the action of phospholipase A2 on unmodified phosphatidylcholine vesicles. Biochim Biophys Acta 688:349–356

    Article  PubMed  CAS  Google Scholar 

  • Aveyard R, Haydon DA (1973): An Introduction to the Principles of Surface Chemistry. Cambridge: Cambridge University Press

    Google Scholar 

  • Bennett JP, Smith GA, Houslay MD, Hesketh TR, Metcalfe JC, Warren GB (1978): The phospholipid headgroup specificity of an ATP-dependent calcium pump. Biochim Biophys Acta 513:310–320

    Article  PubMed  CAS  Google Scholar 

  • Biltonen RL (1990): A statistical-thermodynamic view of cooperative structural changes in phospholipid bilayer membranes: Their potential role in biological function.J Chem Thermody 22:1–19

    Article  CAS  Google Scholar 

  • Blok MC, van der Neut-Kok ECM, van Deenen LLM, de Gier J (1975): The effect of chainlength and lipid phase transitions on the selective permeability properties of liposomes. Biochim Biophys Acta 406:187–196

    Article  PubMed  CAS  Google Scholar 

  • Boggs JM, Clement IR, Moscarello MA (1980): Similar effect of proteolipid apoproteins from human myelin (lipophilin) and bovine white matter on the lipid phase transition. Biochim Biophys Acta 601:134–151

    Article  PubMed  CAS  Google Scholar 

  • Boggs JM, Rangaraj G, Kostry KM (1988): Photolabeling of myelin basic protein in lipid vesicles with the hydrophobic reagent 3-(trifluoromethyl)-3-(m-[125I]iodophenyl) diazirine. Biochim Biophys Acta 937:1–9

    Article  PubMed  CAS  Google Scholar 

  • Boheim G, Hanke W, Eibl H (1980): Lipid phase transition in a planar bilayer and its effect on carrier- and pore-mediated transport. Proc Natl Acad Sci USA 77:3403–3407

    Article  PubMed  CAS  Google Scholar 

  • Burack WR, Yuan Q, Biltonen RL (1993): Role of lateral phase separation in the modulation of phospholipase A2 activity. Biochemistry 31:583–589

    Article  Google Scholar 

  • Cantor CR, Schimmel PR (1980): Biophysical Chemistry, Vol. J. New York: Freeman

    Google Scholar 

  • Carruthers A, Melchior DL (1984): Human erythrocyte hexose transporter activity is governed by bilayer lipid composition in reconstituted vesicles. Biochemistry 23:6901–6911

    Article  PubMed  CAS  Google Scholar 

  • Cevc G, Marsh D (1987): Phospholipid Bilayers. Physical Principles and Models. New York: Wiley-Interscience

    Google Scholar 

  • Cevc G, Watts A, Marsh D (1981): Titration of the phase transition of phosphatidylserine bilayer membranes. Effects of pH, surface electrostatics, ion binding and head-group hydration. Biochemistry 20:4955–4965

    Article  PubMed  CAS  Google Scholar 

  • Cevc G, Watts A, Marsh D (1980): Non-electrostatic contribution to the titration of the ordered-fluid phase transition of phosphatidylglycerol bilayers. FEBS Lett 120:267–270

    Article  PubMed  CAS  Google Scholar 

  • Cheddar G, Tollin G (1994): Comparison of electron transfer kinetics between redox proteins free in solution and electrostatically complexed to a lipid bilayer membrane. Arch Biochem Biophys 310:392–396

    Article  PubMed  CAS  Google Scholar 

  • Chen YS, Hubbell WL (1973): Temperature- and light-dependent structural changes in rhodopsin-lipid membranes. Exp Eye Res 17:517–532

    Article  PubMed  CAS  Google Scholar 

  • Cortese JD, Fleischer S (1987): Noncooperative vs. cooperative reactivation of D-β-hydroxybutyrate dehydrogenase: Multiple equilibria for lecithin binding are determined by the physical state (soluble vs. bilayer) and composition of the phospholipids. Biochemistry 26:5283–5293

    Article  PubMed  CAS  Google Scholar 

  • Cutsforth GA, Whitaker RN, Hermans J, Lentz BR (1989): A new model to describe extrinsic protein binding to phospholipid membranes of varying composition: Application to human coagulation proteins. Biochemistry 28:7453–7461

    Article  PubMed  CAS  Google Scholar 

  • Daum G (1985): Lipids of mitochondria. Biochim Biophys Acta 822:1–42

    PubMed  CAS  Google Scholar 

  • Dickerson RE, Takano T, Eisenberg D, Kallai OB, Samson L, Cooper A, Margoliash EJ (1971): Ferricytochrome c 1. General features of the horse and bonito proteins at 2.8 Ă… resolution.J Biol Chem 246:1511–1535

    PubMed  CAS  Google Scholar 

  • Evans EA, Kwok R (1982): Mechanical calorimetry of large dimyristoyl phosphatidylcholine vesicles in the phase transition region. Biochemistry 21:4874–4879

    Article  PubMed  CAS  Google Scholar 

  • Fajer P, Knowles PFK, Marsh D (1989): Rotational motion of yeast cytochrome oxidase in phosphatidylcholine complexes studied by saturation-transfer electron spin resonance. Biochemistry 28:5634–5643

    Article  PubMed  CAS  Google Scholar 

  • Ferrenberg AM, Swendsen RH (1988): New Monte Carlo technique for studying phase transitions. Phys Rev Lett 61:2635–2638

    Article  PubMed  CAS  Google Scholar 

  • Fox RO, Jr., Richards FM (1982): A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1.5-A resolution. Nature 30:325–330

    Article  Google Scholar 

  • Freire E, Markello T, Rigell C, Holloway PW (1983): Calorimetric and fluorescence characterization of interactions between cytochrome b 5 and phosphatidylcholine bilayers. Biochemistry 22:1675–1680

    Article  PubMed  CAS  Google Scholar 

  • Görrisen H, Marsh D, Rietveld A, de Kruijff B (1986): Apocytochrome c binding to negatively charged lipid dispersions studied by spin-label electron spin resonance. Biochemistry 25:2904–2910

    Article  Google Scholar 

  • Grainger DW, Reichert A, Ringsdorf H, Salesse C (1990): Hydrolytic action of phospholipase A2 in monolayers in the phase transition region: Direct observation of enzyme domain formation using fluorescence microscopy. Biochim Biophys Acta 1023:365–379

    Article  PubMed  CAS  Google Scholar 

  • Grant CWM, McConnell HM (1974): Glycophorin in lipid bilayers. Proc Natl Acad Sci USA 71:4653–4657

    Article  PubMed  CAS  Google Scholar 

  • Harlos K, Vaz WLC, Kovatchev S (1977): Effect of desoxylysolecithins on dimyristoyl-lecithin vesicles. Influence of the lipid phase transition. FEBS Lett 77:7–10

    Article  PubMed  CAS  Google Scholar 

  • Haydon DA, Taylor FH (1960): On adsorption at the oil/water interface and the calculation of electrical potentials in the aqueous surface phase. I. Neutral molecules and a simplified treatment for ions. Phil Trans Roy Soc A 252:225–248

    Article  Google Scholar 

  • Heimburg T, Biltonen RL (1996): A Monte-Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. Biophys J 70:84–96

    Article  PubMed  CAS  Google Scholar 

  • Heimburg T, Biltonen RL (1994): Thermotropic behavior of dimyristoylphosphatidyl-glycerol and its interaction with cytochrome c. Biochemistry 33:9477–9488

    Article  PubMed  CAS  Google Scholar 

  • Heimburg T, Marsh D (1995): Protein surface-distribution and protein-protein interactions in the binding of peripheral proteins to charged lipid membranes. Biophys J 68:536–546

    Article  PubMed  CAS  Google Scholar 

  • Heimburg T, Marsh D (1993): Investigation of secondary and tertiary structural changes of cytochrome c in complexes with anionic lipids using amide hydrogen exchange measurements: An FTIR study. Biophys J 65:2408–2417

    Article  PubMed  CAS  Google Scholar 

  • Heimburg T, Hildebrandt P, Marsh D (1991): Cytochrome c-lipid interactions studied by resonance Raman and 31P-NMR spectroscopy. Correlation between the conformational changes of the protein and the lipid bilayer. Biochemistry 30:9084–9089

    Article  PubMed  CAS  Google Scholar 

  • Hesketh TR, Smith GA, Houslay MD, McGill KA, Birdsall, NJM, Metcalfe JC, Warren GB (1976): Annular lipids determine the ATPase activity of a calcium transport protein complexed with dipalmitoyllecithin. Biochemistry 15:4145–4151

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo C, Thomas DD, Ikemoto N (1978): Effect of the lipid environment on protein motion and enzymatic activity of the sarcoplasmic reticulum calcium ATPase. J Biol Chem 253:6879–6887

    PubMed  CAS  Google Scholar 

  • Hildebrandt P, Stockburger M (1989a): Cytochrome c at charged interfaces. 1. Conformational and redox equilibria at the electrode/electrolyte interface probed by surface-enhanced Raman spectroscopy. Biochemistry 28:6710–6721

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt P, Stockburger M (1989b): Cytochrome c at charged interfaces. 2. Complexes with negatively charged macromolecular systems studied by resonance Raman spectroscopy. Biochemistry 28:6722–6728

    Article  PubMed  CAS  Google Scholar 

  • Hildebrandt P, Heimburg T, Marsh D (1990): Quantitative conformational analysis of cytochrome c bound to phospholipid vesicles studied by resonance Raman spectroscopy. Eur Biophys J 18:193–201

    Article  PubMed  CAS  Google Scholar 

  • Hill TL (1960): An Introduction to Statistical Thermodynamics. New York: Dover

    Google Scholar 

  • Hill TL (1946): Statistical mechanics of multimolecular absorption. II. Localized and mobile adsorption and absorption. J Chem Phys 14:441–453

    Article  CAS  Google Scholar 

  • Huang J, Swanson JE, Dibble ARG, Hinderliter AK, Feigenson GW (1993): Nonideal mixing of phosphatidylserine and phosphatidylcholine in the fluid lamellar phase. Biophys J 64:413–425

    Article  PubMed  CAS  Google Scholar 

  • Jacobson K, Papahadjopoulos D (1976): Effect of phase transition on the binding of 1-anilino-8-naphthalenesulfonate to phospholipid membranes. Biophys J 16:549–560

    Article  PubMed  CAS  Google Scholar 

  • Jähnig F (1976): Electrostatic free energy and shift of the phase transition for charged lipid membranes. Biophys Chem 4:309–318

    Article  PubMed  Google Scholar 

  • Jain MK, Vaz WLC (1987): Dehydration of the lipid-protein microinterface on binding phospholipase A2 to lipid bilayers. Biochim Biophys Acta 905:1–8

    Article  PubMed  CAS  Google Scholar 

  • Jain MK, Egmond MR, Verheij H, Apitz-Castro R, Dijkman R, de Haas GH (1982): Interaction of phospholipase A2 and phospholipid bilayers. Biochim Biophys Acta 688:341–348

    Article  PubMed  CAS  Google Scholar 

  • Jain MK, Yu B-Z, Kozubek A (1989): Binding of phospholipase A2 to zwitterionic bilayers is promoted by lateral segregation of anionic amphiphiles. Biochim Biophys Acta 980:23–32

    Article  PubMed  CAS  Google Scholar 

  • Kimelberg HK, Papahadjopoulos D (1974): Effects of phospholipid acyl chain fluidity, phase transitions and cholesterol on (Na+ + K+)-stimulated adenosine triphosphatase. J Biol Chem 249:1071–1080

    PubMed  CAS  Google Scholar 

  • Kleeman W, McConnell HM (1976): Interactions of proteins and cholesterol with lipids in bilayer membranes. Biochim Biophys Acta 419:206–222

    Article  Google Scholar 

  • Kleeman W, McConnell HM (1974): Lateral phase separations in Escherichia coli membranes. Biochim Biophys Acta 345:220–230

    Article  Google Scholar 

  • Lee J, Kosterlitz JM (1991): Finite-size scaling and Monte Carlo simulations of first-order phase transitions. Phys Rev B 43:3265–3277

    Article  Google Scholar 

  • Lichtenberg D, Romero G, Menashe M, Biltonen RL (1986): Hydrolysis of dipalmitoyl phosphatidylcholine large unilamellar vesicles by porcine pancreatic phospholipase A2. J Biol Chem 261:5334–5340

    PubMed  CAS  Google Scholar 

  • Linden C, Wright K, McConnell HM, Fox CF (1973): Phase separations and glucoside uptake in E. coli fatty acid auxotrophs. Proc Natl Acad Sci USA 70:2271–2275

    Article  PubMed  CAS  Google Scholar 

  • Liu NI, Kay RL (1977): Redetermination of the pressure dependence of the lipid bilayer phase transition. Biochemistry 16:3484–3486

    Article  PubMed  CAS  Google Scholar 

  • London Y, Demel RA, Guerts van Kessel WSM, Vossenberg FGA, van Deenen LLM (1979): The protection of A1 myelin basic protein against the action of proteolytic enzymes after injection of the protein with lipids at the air-water interface. Biochim Biophys Acta 311:520–530

    Google Scholar 

  • Marsh D (1996): Lateral pressure in membranes. Biochim Biophys Acta: in press

    Google Scholar 

  • Marsh D (1995a): Specificity of lipid-protein interactions. In: Biomembranes, Vol. 1, Lee AG, ed. Greenwich, CT: JAI Press

    Google Scholar 

  • Marsh D (1995b): Lipid-protein interactions and heterogeneous lipid distribution in membranes. Mol Memb Biol 12:59–64

    Article  CAS  Google Scholar 

  • Marsh D (1990): Handbook of Lipid Bilayers. Boca Raton, FL: CRC Press

    Google Scholar 

  • Marsh D (1985): ESR spin label studies of lipid-protein interactions. In: Progress in Protein-Lipid Interactions, Vol. 1, Watts A, de Pont JJHHM, eds. Amsterdam: Elsevier

    Google Scholar 

  • Marsh D, Watts A (1981): ESR spin label studies. In: Liposomes: from Physical Structure to Therapeutic Applications, Knight CG, ed. Amsterdam: Elsevier/North-Holland Biomedical Press

    Google Scholar 

  • Marsh D, Watts A, Knowles PF (1977): Cooperativity of the phase transition in single-and multibilayer lipid vesicles. Biochim Biophys Acta 465:500–514

    Article  PubMed  CAS  Google Scholar 

  • Marsh D, Watts A, Knowles PF (1976): Permeability of Tempocholine into dimyristoyl phosphatidylcholine vesicles at the phase transition. Biochemistry 15:3570–3578

    Article  PubMed  CAS  Google Scholar 

  • Mitaku S, Ikegami A, Sakanishi A (1978): Ultrasonic studies of lipid bilayer. Phase transition in synthethic phosphatidylcholine liposomes. Biophys Chem 8:295–304

    Article  PubMed  CAS  Google Scholar 

  • Morrow MR, Davis JH, Sharom FJ, Lamb MP (1986): Studies of the interaction of human erythrocyte band 3 with membrane lipids using deuterium nuclear magnetic resonance and differential scanning calorimetry. Biochim Biophys Acta 858:13–20

    Article  PubMed  CAS  Google Scholar 

  • Mouritsen OG, Biltonen RL (1992): Protein-lipid interactions and membrane heterogeneity. In: Protein-Lipid Interactions. New Comprehensive Biochemistry, Vol. 25, Watts A, ed. Amsterdam: Elsevier

    Google Scholar 

  • Muga A, Mantsch HH, Surewicz WK (1991): Membrane binding induces destabilization of cytochrome c structure. Biochemistry 30:7219–7224

    Article  PubMed  CAS  Google Scholar 

  • MĂĽhlebach T, Cherry RJ (1985): Rotational diffusion and self-association of band 3 in reconstituted lipid vesicles. Biochemistry 24:975–983

    Article  PubMed  Google Scholar 

  • Newton AC (1993): Interaction of proteins with lipid headgroups: Lessons from protein kinase C. Annu Rev Biophys Biomol Struct 22:1–25

    Article  PubMed  CAS  Google Scholar 

  • Op den Kamp JAF, Kauerz MTh, van Deenen LLM (1975): Action of pancreatic phospho-lipase A2 on phosphatidylcholine bilayers in different physical states. Biochim Biophys Acta 406:169–177

    Article  Google Scholar 

  • Orr JW, Newton AC (1992a): Interaction of protein kinase C with phosphatidylserine 1. Cooperativity in lipid binding. Biochemistry 31:4661–4667

    Article  PubMed  CAS  Google Scholar 

  • Orr JW, Newton AC (1992b): Interaction of protein kinase C with phosphatidylserine. 2. Specificity and regulation. Biochemistry 31:4667–4673

    Article  PubMed  CAS  Google Scholar 

  • Overath P, Thilo L (1978): Structural and functional aspects of biological membranes revealed by lipid phase transitions. In: Biochemistry of Cell Walls and Membranes II, Metcalfe JC, ed. London: Butterworth and University Park Press

    Google Scholar 

  • Papahadjopoulos D, Jacobson K, Nir S, Isac T (1973): Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability experiments concerning the effects of temperature and cholesterol. Biochim Biophys Acta 311:330–348

    Article  PubMed  CAS  Google Scholar 

  • Ramsay G, Prabhu R, Freire E (1986): Direct measurement of the energetics of association between myelin basic protein and phosphatidylserine vesicles. Biochemistry 25:2265–2270

    Article  PubMed  CAS  Google Scholar 

  • Ryba NJP, Marsh D (1992): Protein rotational diffusion and lipid/protein interactions in recombinants of bovine rhodopsin with saturated diacyl-phosphatidylcholines of different chainlengths studied by conventional and saturation-transfer electron spin resonance. Biochemistry 31:7511–7518

    Article  PubMed  CAS  Google Scholar 

  • Sankaram MB, Marsh D (1993): Protein-lipid interactions with peripheral membrane proteins. In: Protein-Lipid Interactions. New Comprehensive Biochemistry, Vol. 25, Watts A, ed. Amsterdam: Elsevier

    Google Scholar 

  • Sankaram MB, Brophy PJ, Jordi W, Marsh D (1990): Fatty acid pH titration and the selectivity of interaction with extrinsic proteins in dimyristoylphosphatidylglycerol dispersions. Spin label ESR studies. Biochim Biophys Acta 1021:63–69

    Article  CAS  Google Scholar 

  • Sankaram MB, Brophy PJ, Marsh D (1989a): Spin-label ESR studies on the interaction of bovine spinal cord myelin basic protein with dimyristoylphosphatidylglycerol dispersions. Biochemistry 28:9685–9691

    Article  PubMed  CAS  Google Scholar 

  • Sankaram MB, de Kruijff B, Marsh D (1989b): Selectivity of interaction of spin-labelled lipids with peripheral proteins bound to dimyristoyl phosphatidylglycerol bilayers, as determined by ESR spectroscopy. Biochim Biophys Acta 986:315–320

    Article  CAS  Google Scholar 

  • Silvius JR, McElhaney RN (1991): Non-linear Arrhenius plots and the analysis of reaction and motional rates in membranes.J Theoret Biol 88:135–152

    Article  Google Scholar 

  • Starling AP, East JM, Lee AG (1995): Effects of gel phase phospholipid on Ca2+-ATPase. Biochemistry 34:3084–3091

    Article  PubMed  CAS  Google Scholar 

  • Sugar IP, Biltonen RL, Mitchard N (1994): Monte Carlo simulations of membranes: Phase transition of small unilamellar dipalmitoylphosphatidylcholine vesicles. Methods Enzymol 240:569–593

    Article  PubMed  CAS  Google Scholar 

  • Surewicz WA, Moscarello MA, Mantsch HH (1987): Fourier transform infrared spectroscopic investigation of the interaction between myelin basic protein and dimyris-toylphosphatidylglycerol bilayers. Biochemistry 26:3881–3886

    Article  PubMed  CAS  Google Scholar 

  • Tanford C (1955): The electrostatic free energy of globular protein ions in aqueous solution.J Phys Chem 59:788–793

    Article  CAS  Google Scholar 

  • Teft RC Jr, Carruthers A, Melchior DL (1986): Reconstituted human erythrocyte sugar transporter activity is determined by bilayer lipid headgroups. Biochemistry 25:3709–3718

    Article  Google Scholar 

  • Thilo L, Träuble H, Overath P (1977): Mechanistic interpretation of the influence of lipid phase transitions on transport functions. Biochemistry 16:1283–1290

    Article  PubMed  CAS  Google Scholar 

  • Tsong TY (1975): Effect of a phase transition on the kinetics of dye transport in phospholipid bilayer structures. Biochemistry 14:5409–5414

    Article  PubMed  CAS  Google Scholar 

  • Van Hoogevest P, de Gier J, de Kruijff B (1984): Determination of the size of the packing defects in dimyristoyl phosphatidylcholine bilayers, present at the phase transition temperature. FEBS Lett 171:160–164

    Article  Google Scholar 

  • Wickner W (1976): Asymmetric orientation of phage M13 coat protein in Escherichia coli cytoplasmic membranes and in synthetic lipid vesicles. Proc Natl Acad Sci USA 73:1159–1163

    Article  PubMed  CAS  Google Scholar 

  • Wu SH, McConnell HM (1973): Lateral phase separations and perpendicular transport in membranes. Biochem Biophys Res Commun 55:484–491

    Article  PubMed  CAS  Google Scholar 

  • Zimm BH, Bragg JK (1959): Theory of the phase transition between helix and random coil in polypeptide chains.J Chem Phys 31:526–535

    Article  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Birkhäuser Boston

About this chapter

Cite this chapter

Heimburg, T., Marsh, D. (1996). Thermodynamics of the Interaction of Proteins with Lipid Membranes. In: Merz, K.M., Roux, B. (eds) Biological Membranes. Birkhäuser Boston. https://doi.org/10.1007/978-1-4684-8580-6_13

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-8580-6_13

  • Publisher Name: Birkhäuser Boston

  • Print ISBN: 978-1-4684-8582-0

  • Online ISBN: 978-1-4684-8580-6

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics