Skip to main content
SpringerLink
Log in

Interdigitation of Lipids Induced by Membrane–Active Proteins

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

The membrane–active protein Nogo-66 is found to induce interdigitation in dimyristoylphosphocholine membranes. Extensive molecular dynamics simulations have been employed to probe the interactions of Nogo-66 with these model membranes. This phase change happens when the temperature is close to the main transition temperature of the membrane (Tm) and only in the presence of the protein. No similar interdigitation of the membrane lipids was observed temperatures well above Tm in the presence of the protein. In addition, in protein-free simulations, no interdigitation of the membrane lipids was found both at temperatures near or well above Tm indicating that the observed effect is caused by the interactions of Nogo-66 with the membrane. Analysis of the simulations suggest protein–membrane interactions, even if transient, alter the lifetimes of lipid head defects and can potentially alter the effective Tm and cause interdigitation. This study emphasize the importance of membrane–active proteins and their interactions with membranes leading to phase transitions which would affect other membrane-related processes such as domain formation.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Akabori K, Nagle JF (2015) Structure of the DMPC lipid bilayer ripple phase. Soft Matter 11(5):918–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida C, Lamazière A, Filleau A, Corvis Y, Espeau P, Ayala-Sanmartin J (2016) Membrane re-arrangements and rippled phase stabilisation by the cell penetrating peptide penetratin. Biochim Biophys Acta 1858(11):2584–2591

    Article  CAS  PubMed  Google Scholar 

  • Aoun B, Pellegrini E, Trapp M, Natali F, Cantú L, Brocca P, Gerelli Y, Demé B, Koza MM, Johnson M et al (2016) Direct comparison of elastic incoherent neutron scattering experiments with molecular dynamics simulations of dmpc phase transitions. Eur Phys J E 39(4):48

    Article  PubMed  CAS  Google Scholar 

  • Baoukina S, Tielemanm DP (2015) Computer simulations of phase separation in lipid bilayers and monolayers. Methods in membrane lipids. Springer, New York, pp 307–322

    Google Scholar 

  • Baul U, Vemparala S (2015) Membrane-bound conformations of antimicrobial agents and their modes of action, vol 22. Advances in planar lipid bilayers and liposomes. Elsevier, Amsterdam, pp 97–128

    Google Scholar 

  • Baul U, Vemparala S (2017) Influence of lipid composition of model membranes on methacrylate antimicrobial polymer–membrane interactions. Soft Matter 13(41):7665–7676

    Article  CAS  PubMed  Google Scholar 

  • Best RB, Zhu X, Shim J, Lopes PEM, Mittal J, Feig M, MacKerell AD Jr (2012) Optimization of the additive charmm all-atom protein force field targeting improved sampling of the backbone \(\phi\), \(\psi\) and side-chain \(\chi\)1 and \(\chi\)2 dihedral angles. J Chem Theory Comput 8(9):3257–3273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bigay J, Casella J-F, Drin G, Mesmin B, Antonny B (2005) Arfgap1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J 24(13):2244–2253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cevc G, Marsh D (1987) Phospholipid bilayers: physical principles and models. Wiley, Hoboken

    Google Scholar 

  • Chen C-M, Lubensky TC, MacKintosh FC (1995) Phase transitions and modulated phases in lipid bilayers. Phys Rev E 51(1):504

    Article  CAS  Google Scholar 

  • Chen W, Duša F, Witos J, Ruokonen S-K, Wiedmer SK (2018) Determination of the main phase transition temperature of phospholipids by nanoplasmonic sensing. Sci Rep 8(1):14815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choubey A, Nomura K, Kalia RK, Nakano A, Vashishta P (2014) Small interfering ribonucleic acid induces liquid-to-ripple phase transformation in a phospholipid membrane. Appl Phys Lett 105(11):113702

    Article  CAS  Google Scholar 

  • Cui H, Lyman E, Voth GA (2011) Mechanism of membrane curvature sensing by amphipathic helix containing proteins. Biophys J 100(5):1271–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darden T, York D, Pedersen L (1993) Particle mesh ewald: an n log (n) method for ewald sums in large systems. J Chem Phys 98(12):10089–10092

    Article  CAS  Google Scholar 

  • de Vries AH, Serge Y, Mark AE, Marrink SJ (2005) Molecular structure of the lecithin ripple phase. Proc Natl Acad Sci 102(15):5392–5396

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Debnath A, Thakkar FM, Maiti PK, Kumaran V, Ayappa KG (2014) Laterally structured ripple and square phases with one and two dimensional thickness modulations in a model bilayer system. Soft Matter 10(38):7630–7637

    Article  CAS  PubMed  Google Scholar 

  • Destainville N, Schmidt TH, Lang T (2016) Where biology meets physics: a converging view on membrane microdomain dynamics, vol 77. Current topics in membranes. Elsevier, Amsterdam, pp 27–65

    Google Scholar 

  • Di Pisa M, Chassaing G, Swiecicki J-M (2014) Translocation mechanism (s) of cell-penetrating peptides: biophysical studies using artificial membrane bilayers. Biochemistry 54(2):194–207

    Article  PubMed  CAS  Google Scholar 

  • Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) Pdb2pqr: an automated pipeline for the setup of poisson-boltzmann electrostatics calculations. Nucl Acids Res 32(suppl 2):W665–W667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584(9):1840–1847

    Article  CAS  PubMed  Google Scholar 

  • Edidin M (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32(1):257–283

    Article  CAS  PubMed  Google Scholar 

  • Epand RM, Walker C, Epand RF, Magarvey NA (2016) Molecular mechanisms of membrane targeting antibiotics. Biochim Biophys Acta 1858(5):980–987

    Article  CAS  PubMed  Google Scholar 

  • Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh ewald method. J Chem Phys 103(19):8577–8593

    Article  CAS  Google Scholar 

  • Feller FSE, Zhang Y, Pastor RW, Brooks BR (1995) Constant pressure molecular dynamics simulation: the langevin piston method. J Chem Phys 103(11):4613–4621

    Article  CAS  Google Scholar 

  • Feng ZV, Granick S, Gewirth AA (2004) Modification of a supported lipid bilayer by polyelectrolyte adsorption. Langmuir 20(20):8796–8804

    Article  CAS  PubMed  Google Scholar 

  • Fusco G, Sanz-Hernandez M, De Simone A (2018) Order and disorder in the physiological membrane binding of α-synuclein. Curr Opin Struct Biol 48:49–57

    Article  CAS  PubMed  Google Scholar 

  • Gautier R, Bacle A, Tiberti ML, Fuchs PF, Vanni S, Antonny B (2018) Packmem: a versatile tool to compute and visualize interfacial packing defects in lipid bilayers. Biophys J 115(3):436–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giorgino T (2014) Computing 1-d atomic densities in macromolecular simulations: the density profile tool for vmd. Comput Phys Commun 185(1):317–322

    Article  CAS  Google Scholar 

  • Gray E, Karslake J, Machta BB, Veatch SL (2013) Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophys J 105(12):2751–2759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffn KL, Cheng C-Y, Smith EA, Dea PK (2010) Effects of pentanol isomers on the phase behavior of phospholipid bilayer membranes. Biophys Chem 152(1–3):178–183

    Article  CAS  Google Scholar 

  • Guixa-González R, Rodriguez-Espigares I, Ramírez-Anguita JM, Carrió-Gaspar P, Martinez-Seara H, Giorgino T, Selent J (2014) Membplugin: studying membrane complexity in vmd. Bioinformatics 30(10):1478–1480

    Article  PubMed  CAS  Google Scholar 

  • Harrison PL, Heath GR, Johnson BRG, Abdel-Rahman MA, Strong PN, Evans SD, Miller K (2016) Phospholipid dependent mechanism of smp24, an α-helical antimicrobial peptide from scorpion venom. Biochim Biophys Acta 1858(11):2737–2744

    Article  CAS  PubMed  Google Scholar 

  • Heller WT, Waring AJ, Lehrer RI, Harroun TA, Weiss TM, Yang L, Huang HW (2000) Membrane thinning effect of the β-sheet antimicrobial protegrin. Biochemistry 39(1):139–145

    Article  CAS  PubMed  Google Scholar 

  • Humphrey W, Dalke A, Schulten K (1996) VMD—visual molecular dynamics. J Mol Graph 14:33–38

    Article  CAS  PubMed  Google Scholar 

  • Jain MK, White HB (1977) Long-range order in biomembranes, vol 15. Advances in lipid research. Elsevier, Amsterdam, pp 1–60

    Google Scholar 

  • Jain MK, Wu NM (1977) Effect of small molecules on the dipalmitoyl lecithin liposomal bilayer: III. Phase transition in lipid bilayer. J Membr Biol 34(1):157–201

    Article  CAS  Google Scholar 

  • Jo S, Kim T, Iyer VG, Im W (2008) Charmm-gui: a web-based graphical user interface for charmm. J Comput Chem 29(11):1859–1865

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein Michael L (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79(2):926–935

    Article  CAS  Google Scholar 

  • Kaiser H-J, Lingwood D, Levental I, Sampaio JL, Kalvodova L, Rajendran L, Simons K (2009) Order of lipid phases in model and plasma membranes. Proc Natl Acad Sci 106(39):16645–16650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khakbaz P, Klauda JB (2018) Investigation of phase transitions of saturated phosphocholine lipid bilayers via molecular dynamics simulations. Biochim Biophys Acta 180(8):1489–1501

    Article  CAS  Google Scholar 

  • Koukos PI, Glykos NM (2013) Grcarma: a fully automated task-oriented interface for the analysis of molecular dynamics trajectories. J Comput Chem 34(26):2310–2312

    Article  CAS  PubMed  Google Scholar 

  • Kranenburg M, Smit B (2005) Phase behavior of model lipid bilayers. J Phys Chem B 109(14):6553–6563

    Article  CAS  PubMed  Google Scholar 

  • Kranenburg M, Venturoli M, Smit B (2003) Phase behavior and induced interdigitation in bilayers studied with dissipative particle dynamics. J Phys Chem B 107(41):11491–11501

    Article  CAS  Google Scholar 

  • Kranenburg M, Vlaar M, Smit B (2004) Simulating induced interdigitation in membranes. Biophys J 87(3):1596–1605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kučerka N, Nieh M-P, Katsaras J (2011) Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim Biophys Acta 1808(11):2761–2771

    Article  PubMed  CAS  Google Scholar 

  • Lamaziére A, Wolf C, Lambert O, Chassaing G, Trugnan G, Ayala-Sanmartin J (2008) The homeodomain derived peptide penetratin induces curvature of fluid membrane domains. PLoS ONE 3(4):e1938

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lamaziére A, Chassaing G, Trugnan G, Ayala-Sanmartin J (2009) Tubular structures in heterogeneous membranes induced by the cell penetrating peptide penetratin. Commun Integr Biol 2(3):223–224

    Article  PubMed  PubMed Central  Google Scholar 

  • Laner M, Hünenberger PH (2015) Effect of methanol on the phase-transition properties of glycerol-monopalmitate lipid bilayers investigated using molecular dynamics simulations in quest of the biphasic effect. J Mol Graph Model 55:85–104

    Article  CAS  PubMed  Google Scholar 

  • Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612(1):1–40

    Article  CAS  PubMed  Google Scholar 

  • Lee M-T, Chen F-Y, Huang HW (2004) Energetics of pore formation induced by membrane active peptides. Biochemistry 43(12):3590–3599

    Article  CAS  PubMed  Google Scholar 

  • Lee M-T, Sun T-L, Hung W-C, Huang HW (2013) Process of inducing pores in membranes by melittin. Proc Natl Acad Sci 110(35):14243–14248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenz O, Schmid F (2007) Structure of symmetric and asymmetric “ripple” phases in lipid bilayers. Phys Rev Lett 98(5):058104

    Article  PubMed  CAS  Google Scholar 

  • Lewis BA, Engelman DM (1983) Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles. J Mol Biol 166(2):211–217

    Article  CAS  PubMed  Google Scholar 

  • Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):40–50

    Article  CAS  Google Scholar 

  • Lubensky TC, MacKintosh FC (1993) Theory of “ripple” phases of lipid bilayers. Phys Rev Lett 71(10):1565

    Article  CAS  PubMed  Google Scholar 

  • Lyman E, Hsieh CL, Eggeling C (2018) From dynamics to membrane organization: experimental breakthroughs occasion a “modeling manifesto”. Biophys J

  • Mabrey M, Sturtevant JM (1976) Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry. Proc Natl Acad Sci 73(11):3862–3866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacKerell AD Jr, Bashford D, Bellott MLDR, Dunbrack RL Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S et al (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102(18):3586–3616

    Article  CAS  PubMed  Google Scholar 

  • Marrink SJ, De Vries AH, Tieleman DP (2009) Lipids on the move: simulations of membrane pores, domains, stalks, and curves. Biochim Biophys Acta 1788(1):149–168

    Article  CAS  PubMed  Google Scholar 

  • Martyna GJ, Tobias DJ, Klein ML (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101(5):4177–4189

    Article  CAS  Google Scholar 

  • Mavromoustakos T, Chatzigeorgiou P, Koukoulitsa C, Durdagi S (2011) Partial interdigitation of lipid bilayers. Int J Quantum Chem 111(6):1172–1183

    Article  CAS  Google Scholar 

  • McIntosh TJ, McDaniel RV, Simon SA (1983) Induction of an interdigitated gel phase in fully hydrated phosphatidylcholine bilayers. Biochim Biophys Acta 731(1):109–114

    Article  CAS  Google Scholar 

  • McIntosh TJ, Lin H, Li S, Huang C (2001) The effect of ethanol on the phase transition temperature and the phase structure of monounsaturated phosphatidylcholines. Biochim Biophys Acta 1510(1):219–230

    Article  CAS  PubMed  Google Scholar 

  • McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590

    Article  CAS  PubMed  Google Scholar 

  • Meck A, Lee D-K, Ramamoorthy A, Orr BG (2005) Membrane thinning due to antimicrobial peptide binding: an atomic force microscopy study of msi-78 in lipid bilayers. Biophys J 89(6):4043–4050

    Article  CAS  Google Scholar 

  • Mizuno N, Varkey J, Kegulian NC, Hegde BG, Naiqian C, Ralf L, Steven Alasdair C (2012) Remodeling of lipid vesicles into cylindrical micelles by α-synuclein in an extended α-helical conformation. J Biol Chem 287(35):29301–29311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagle JF, Wilkinson DA (1978) Lecithin bilayers density measurement and molecular interactions. Biophys J 23(2):159–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicovich PR, Kwiatek JM, Ma Y, Benda A, Gaus K (2018) Fscs reveals the complexity of lipid domain dynamics in the plasma membrane of live cells. Biophys J 114(12):2855–2864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouberai MM, Wang J, Swann MJ, Galvagnion C, Guilliams T, Dobson CM, Welland ME (2013) α-Synuclein senses lipid packing defects and induces lateral expansion of lipids leading to membrane remodeling. J Biol Chem 288:20883–20895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Leary EI, Jiang Z, Strub MP, Lee JC (2018) Effects of phosphatidylcholine membrane fluidity on the conformation and aggregation of n-terminally acetylated \(\alpha\)-synuclein. J Biol Chem 293(28):11195–11205

    Article  PubMed  PubMed Central  Google Scholar 

  • Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K (2005) Scalable molecular dynamics with namd. J Comput Chem 26(16):1781–1802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian S, Heller WT (2011) Peptide-induced asymmetric distribution of charged lipids in a vesicle bilayer revealed by small-angle neutron scattering. J Phys Chem B 115(32):9831–9837

    Article  CAS  PubMed  Google Scholar 

  • Ramalho JPP, Gkeka P, Sarkisov L (2011) Structure and phase transformations of dppc lipid bilayers in the presence of nanoparticles: insights from coarse-grained molecular dynamics simulations. Langmuir 27(7):3723–3730

    Article  CAS  Google Scholar 

  • Reddy ST, Shrivastava S, Chattopadhyay A (2018) Local anesthetics induce interdigitation and thermotropic changes in dipalmitoylphosphatidylcholine bilayers. Chem Phys Lipids 210:22–27

    Article  CAS  PubMed  Google Scholar 

  • Reynolds NP, Soragni A, Rabe M, Verdes D, Liverani E, Handschin S, Riek R, Seeger S (2011) Mechanism of membrane interaction and disruption by α-synuclein. J Am Chem Soc 133(48):19366–19375

    Article  CAS  PubMed  Google Scholar 

  • Rowe ES, Campion JM (1994) Alcohol induction of interdigitation in distearoylphosphatidylcholine: fluorescence studies of alcohol chain length requirements. Biophys J 67(5):1888–1895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid F (2017) Physical mechanisms of micro- and nanodomain formation in multicomponent lipid membranes. Biochim Biophys Acta 1859(4):509–528

    Article  CAS  Google Scholar 

  • Sevcsik E, Pabst G, Jilek A, Lohner K (2007) How lipids influence the mode of action of membrane–active peptides. Biochim Biophys Acta 1768(10):2586–2595

    Article  CAS  PubMed  Google Scholar 

  • Sharma VK, Qian S (2019) Effect of an antimicrobial peptide on lateral segregation of lipids, a structure and dynamics study by neutron scattering. Langmuir 35:4152–4160

    Article  CAS  PubMed  Google Scholar 

  • Sharma VK, Mamontov E, Tyagi M, Qian S, Rai DK, Urban VS (2016) Dynamical and phase behavior of a phospholipid membrane altered by an antimicrobial peptide at low concentration. J Phys Chem Lett 7(13):2394–2401

    Article  CAS  PubMed  Google Scholar 

  • Shigematsu T, Koshiyama K, Wada S (2018) Stretch-induced interdigitation of a phospholipid/cholesterol bilayer. J Phys Chem B 122(9):2556–2563

    Article  CAS  PubMed  Google Scholar 

  • Slater JL, Huang C-H (1988) Interdigitated bilayer membranes. Prog Lipid Res 27(4):325–359

    Article  CAS  PubMed  Google Scholar 

  • Smith EA, Dea PK (2013) Differential scanning calorimetry studies of phospholipid membranes: the interdigitated gel phase. In: Applications of calorimetry in a wide context-differential scanning calorimetry, isothermal titration calorimetry and microcalorimetry. InTech, London

  • Stone MB, Shelby SA, Núñez MF, Wisser K, Veatch SL (2017) Protein sorting by lipid phase-like domains supports emergent signaling function in b lymphocyte plasma membranes. Elife 6:e19891

    Article  PubMed  PubMed Central  Google Scholar 

  • Su C-J, Wu S-S, Jeng U-S, Lee M-T, Su A-C, Liao K-F, Lin W-Y, Huang Y-S, Chen C-Y (2013) Peptide-induced bilayer thinning structure of unilamellar vesicles and the related binding behavior as revealed by X-ray scattering. Biochim Biophys Acta 1828(2):528–534

    Article  CAS  PubMed  Google Scholar 

  • Sun WJ, Tristram-Nagle S, Suter RM, Nagle JF (1996) Structure of the ripple phase in lecithin bilayers. Proc Natl Acad Sci 93(14):7008–7012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tardieu A, Vittorio L, Reman FC (1973) Structure and polymorphism of the hydrocarbon chains of lipids: a study of lecithin-water phases. J Mol Biol 75(4):711–733

    Article  CAS  PubMed  Google Scholar 

  • Vamparys L, Gautier R, Vanni S, Bennett WFD, Tieleman DP, Antonny B, Etchebest C, Fuchs PFJ (2013) Conical lipids in flat bilayers induce packing defects similar to that induced by positive curvature. Biophys J 104(3):585–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanni S, Vamparys L, Gautier R, Drin G, Etchebest C, Fuchs PFJ, Antonny B (2013) Amphipathic lipid packing sensor motifs: probing bilayer defects with hydrophobic residues. Biophys J 104(3):575–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanni S, Hirose H, Barelli H, Antonny B, Gautier R (2014) A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment. Nat Commun 5:4916

    Article  CAS  PubMed  Google Scholar 

  • Varkey J, Isas JM, Mizuno N, Jensen MB, Bhatia VK, Jao CC, Petrlova J, Voss JC, Stamou DG, Steven AC et al (2010) Membrane curvature induction and tubulation are common features of synucleins and apolipoproteins. J Biol Chem 285(42):32486–32493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasudevan SV, Schulz J, Zhou C, Cocco MJ (2010) Protein folding at the membrane interface, the structure of nogo-66 requires interactions with a phosphocholine surface. Proc Natl Acad Sci 107(15):6847–6851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verde AR, Sierra MB, Alarcón LM, Pedroni VI, Appignanesi GA, Morini MA (2018) Experimental and computational studies of the effects of free dha on a model phosphatidylcholine membrane. Chem Phys Lipids 217:12–18

    Article  CAS  PubMed  Google Scholar 

  • Wang D-C, Taraschi TF, Rubin E, Janes N (1993) Configurational entropy is the driving force of ethanol action on membrane architecture. Biochim Biophys Acta 1145(1):141–148

    Article  CAS  PubMed  Google Scholar 

  • Weikl TR (2018) Membrane-mediated cooperativity of proteins. Annu Rev Phys Chem 69:521–539

    Article  CAS  PubMed  Google Scholar 

  • Welker S, Rudolph B, Frenzel E, Hagn F, Liebisch G, Schmitz G, Scheuring J, Kerth A, Blume A, Weinkauf S et al (2010) Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol cell 39(4):507–520

    Article  CAS  PubMed  Google Scholar 

  • Wu EL, Cheng X, Jo S, Rui H, Song KC, Dávila-Contreras EM, Qi Y, Lee J, Monje-Galvan V, Venable RM et al (2014) Charmm-gui membrane builder toward realistic biological membrane simulations. J Comput Chem 35(27):1997–2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Fukuto M (2005) Modulated phase of phospholipids with a two-dimensional square lattice. Phys Rev E 72(1):010901

    Article  CAS  Google Scholar 

  • Yin H, Flynn AD (2016) Drugging membrane protein interactions. Annu Rev Biomed Eng 18:51–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zambrano F, Fleischer S, Fleischer B (1975) Lipid composition of the golgi apparatus of rat kidney and liver in comparison with other subcellular organelles. Biochim Biophys Acta 380(3):357–369

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The simulations were carried out on the supercomputing machines Annapurna and Nandadevi at the Institute of Mathematical Sciences.

Author information

Authors and Affiliations

  1. The Institute of Mathematical Sciences, C.I.T. Campus, Taramani, Chennai, 600113, India

    T. Devanand, Sankaran Krishnaswamy & Satyavani Vemparala

  2. Homi Bhabha National Institute, Training School Complex, Anushakti Nagar, Mumbai, 400094, India

    T. Devanand & Satyavani Vemparala

Authors
  1. T. Devanand
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sankaran Krishnaswamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Satyavani Vemparala
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Satyavani Vemparala.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (PDF 1099 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Devanand, T., Krishnaswamy, S. & Vemparala, S. Interdigitation of Lipids Induced by Membrane–Active Proteins. J Membrane Biol 252, 331–342 (2019). https://doi.org/10.1007/s00232-019-00072-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-019-00072-7

Keywords

Search

Navigation