Skip to main content
SpringerLink
Log in

Orientation and conformation of lipids in crystals of transmembrane proteins

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

Orientational order parameters and individual dihedral torsion angles are evaluated for phospholipid and glycolipid molecules that are resolved in X-ray structures of integral transmembrane proteins in crystals. The order parameters of the lipid chains and glycerol backbones in protein crystals are characterised by a much wider distribution of orientational order than is found in fluid lipid bilayers and reconstituted lipid–protein membranes. This indicates that the lipids that are resolved in crystals of membrane proteins are mostly not representative of the entire lipid–protein interface. Much of the chain configurational disorder of the membrane-bound lipids in crystals arises from C–C bonds in energetically disallowed skew conformations. This suggests configurational heterogeneity of the lipids at a single binding site: eclipsed conformations occur also in the glycerol backbone torsion angles and the C–C torsion angles of the lipid head groups. Conformations of the lipid glycerol backbone in protein crystals are not restricted to the gauche C1–C2 rotamers found invariably in phospholipid bilayer crystals. Lipid head-group conformations in the protein crystals also do not conform solely to the bent-down conformation, with gauche–gauche configuration of the phosphodiester, that is characteristic of phospholipid bilayer membranes. Stereochemical violations in the protein-bound lipids are evidenced by ester carboxyl groups in non-planar configurations, and even in the cis configuration. Some lipids have the incorrect enantiomeric configuration of the glycerol backbone, and many of the branched methyl groups in the phytanyl chains associated with bacteriorhodopsin have the incorrect S configuration.

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
Fig. 9

Similar content being viewed by others

References

  • Abe A, Mark JE (1976) Conformational energies and the random-coil dimensions and dipole-moments of the polyoxides CH3O[(CH2) y O] x CH3. J Am Chem Soc 98:6468–6476

    Article  CAS  Google Scholar 

  • Abe A, Jernigan RL, Flory PJ (1966) Conformational energies of n-alkanes and the random configuration of higher homologs including polymethylene. J Am Chem Soc 88:631–650

    Article  CAS  Google Scholar 

  • Allinger NL, Zhu Z, Chen K (1992) Molecular mechanics (MM3) studies of carboxylic acids and esters. J Am Chem Soc 114:6120–6133

    Article  CAS  Google Scholar 

  • Belrhali H, Nollert P, Royant A, Menzel C, Rosenbusch JP, Landau EM, Pebay-Peyroula E (1999) Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution. Structure 7:909–917

    Article  PubMed  CAS  Google Scholar 

  • Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH, Strynadka NCJ (2003) Insights into the respiratory electron transfer pathway from the structure of nitrate reductase. Nat Struct Biol 10:681–687

    Article  PubMed  CAS  Google Scholar 

  • Bienvenue A, Bloom M, Davis JH, Devaux PF (1982) Evidence for protein-associated lipids from deuterium nuclear magnetic resonance studies of rhodopsin-dimyristoylphosphatidylcholine recombinants. J Biol Chem 257:3032–3038

    PubMed  CAS  Google Scholar 

  • Bloom M, Smith ICP (1985) Manifestations of lipid–protein interactions in deuterium NMR. In: Watts A, de Pont JJHHM (eds) Progress in protein–lipid interactions, vol 1. Elsevier, Amsterdam, pp 61–88

    Google Scholar 

  • Borisova NP, Vol’kenshtein MV (1961) Internal rotation in propane and n-butane. Zh Strukt Khim 2:437–442

    Google Scholar 

  • Camara-Artigas A, Brune D, Allen JP (2002) Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc Natl Acad Sci USA 99:11055–11060

    Article  PubMed  CAS  Google Scholar 

  • Cevc G, Marsh D (1987) Phospholipid bilayers. Physical principles and models. Wiley–Interscience, New York

    Google Scholar 

  • Chandrasekhar I, Kastenholz M, Lins RD, Oostenbrink C, Schuler LD, Tieleman DP, van Gunsteren WF (2003) A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field. Eur Biophys J 32:67–77

    PubMed  CAS  Google Scholar 

  • de Planque MRR, Greathouse DV, Koeppe RE II, Schäfer H, Marsh D, Killian JA (1998) Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A. Biochemistry 37:9333–9345

    Article  PubMed  Google Scholar 

  • DePristo MA, de Bakker PIW, Blundell TL (2004) Heterogeneity and inaccuracy in protein structures solved by x-ray crystallography. Structure 12:831–838

    Article  PubMed  CAS  Google Scholar 

  • East JM, Lee AG (1982) Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid. Biochemistry 21:4144–4151

    Article  PubMed  CAS  Google Scholar 

  • Elder M, Hitchcock P, Mason R, Shipley GG (1977) A refinement analysis of the crystallography of the phospholipid, 1,2-dilauroyl-dl-phosphatidylethanolamine, and some remarks on lipid–lipid and lipid–protein interactions. Proc R Soc Lond A 354:157–170

    Article  CAS  Google Scholar 

  • Esmann M, Powell GL, Marsh D (1988) Spin label studies on the selectivity of lipid–protein interaction of cardiolipin analogues with the Na+/K+-ATPase. Biochim Biophys Acta 941:287–292

    Article  PubMed  CAS  Google Scholar 

  • Essen L-O, Siegert R, Lehmann WD, Oesterhelt D (1998) Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin–lipid complex. Proc Natl Acad Sci USA 95:11673–11678

    Article  PubMed  CAS  Google Scholar 

  • Ferguson AD, Welte W, Hofmann E, Lindner B, Holst O, Coulton JW, Diederichs K (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Struct Fold Des 8:585–592

    Article  CAS  Google Scholar 

  • Flory PJ (1969) Statistical mechanics of chain molecules. Wiley, London

    Google Scholar 

  • Fyfe PK, Ridge JP, McAuley KE, Cogdell RJ, Isaacs NW, Jones MR (2000) Structural consequences of the replacement of glycine M203 with aspartic acid in the reaction center from Rhodobacter sphaeroides. Biochemistry 39:5953–5960

    Article  PubMed  CAS  Google Scholar 

  • Fyfe PK, McAuley KE, Rothmann M, Isaacs NW, Cogdell RJ, Jones MR (2001) Probing the interface between membrane proteins and membrane lipids by x-ray crystallography. Trends Biochem Sci 26:106–112

    Article  PubMed  CAS  Google Scholar 

  • Gally HU, Niederberger W, Seelig J (1975) Conformation and motion of the choline head group in bilayers of dipalmitoyl-3-sn-phosphatidylcholine. Biochemistry 14:3647–3652

    Article  PubMed  CAS  Google Scholar 

  • Gorenstein DG, Kar D (1977) Effect of bond angle distortion on torsional potentials. Ab initio and CNDO/2 calculations on dimethoxymethane and dimethyl phosphate. J Am Chem Soc 99:672–677

    Article  CAS  Google Scholar 

  • Gorenstein DG, Kar D, Luxon BA, Momii RK (1976) Conformational study of cyclic and acyclic phosphate esters. CNDO/2 calculations of angle strain and torsional strain. J Am Chem Soc 98:1668–1673

    Article  PubMed  CAS  Google Scholar 

  • Harlos K, Eibl H, Pascher I, Sundell S (1984) Conformation and packing properties of phosphatidic acid—the crystal structure of monosodium dimyristoylphosphatidate. Chem Phys Lipids 34:115–126

    Article  Google Scholar 

  • Harrenga A, Michel H (1999) The cytochrome c oxidase from Paracoccus denitrificans does not change the metal center ligation upon reduction. J Biol Chem 274:33296–33299

    Article  PubMed  CAS  Google Scholar 

  • Hauser H, Pascher I, Pearson RH, Sundell S (1981) Preferred conformation and molecular packing of phosphatidylethanolamine and phosphatidylcholine. Biochim Biophys Acta 650:21–51

    Article  PubMed  CAS  Google Scholar 

  • Hong M, Schmidt-Rohr K, Zimmermann H (1996) Conformational constraints on the headgroup and sn-2 chain of bilayer DMPC from NMR dipolar couplings. Biochemistry 35:8335–8341

    Article  PubMed  CAS  Google Scholar 

  • Horváth LI, Brophy PJ, Marsh D (1988a) Exchange rates at the lipid–protein interface of myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry 27:46–52

    Article  PubMed  Google Scholar 

  • Horváth LI, Brophy PJ, Marsh D (1988b) 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 27:5296–5304

    Article  PubMed  Google Scholar 

  • Horváth LI, Brophy PJ, Marsh D (1990a) Influence of polar residue deletions on lipid–protein interactions with the myelin proteolipid protein. Spin-label ESR studies with DM-20/lipid recombinants. Biochemistry 29:2635–2638

    Article  PubMed  Google Scholar 

  • Horváth LI, Drees M, Beyer K, Klingenberg M, Marsh D (1990b) Lipid–protein interactions in ADP–ATP carrier/egg phosphatidylcholine recombinants studied by spin-label ESR spectroscopy. Biochemistry 29:10664–10669

    Article  PubMed  Google Scholar 

  • Horváth LI, Brophy PJ, Marsh D (1993) 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 64:622–631

    Article  PubMed  Google Scholar 

  • Horváth LI, Brophy PJ, Marsh D (1994) Microwave frequency dependence of ESR spectra from spin labels undergoing two-site exchange in myelin proteolipid membranes. J Magn Reson B105:120–128

    Google Scholar 

  • IUPAC Commission on Nomenclature of Organic Chemistry (1976) Rules for the nomenclature of organic chemistry. Section E: stereochemistry. Pure Appl Chem 45:11–30

    Article  Google Scholar 

  • IUPAC-IUB Commission on Biochemical Nomenclature (CBN) (1970) Abbreviations and symbols for the description of the conformation of polypeptide chains. Eur J Biochem 17:193–201

    Article  Google Scholar 

  • IUPAC-IUB Commission on Biochemical Nomenclature (CBN) (1977) The nomenclature of lipids. Eur J Biochem 79:11–21

    Article  Google Scholar 

  • Joo CN, Kates M (1969) Synthesis of the naturally occurring phytanyl diether analogs of phosphatidyl glycerophosphate and phosphatidyl glycerol. Biochim Biophys Acta 176:278–297

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917

    Article  PubMed  CAS  Google Scholar 

  • Jormakka M, Tornroth S, Byrne B, Iwata S (2002) Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295:1863–1868

    Article  PubMed  Google Scholar 

  • Kates M, Joo CN, Palameta B, Shier T (1967) Absolute stereochemical configuration of phytanyl (dihydrophytyl) groups in lipids of Halobacterium cutirubrum. Biochemistry 6:3329–3338

    Article  PubMed  CAS  Google Scholar 

  • Kates M, Moldoveanu N, Stewart LC (1993) On the revised structure of the major phospholipid of Halobacterium salinarum. Biochim Biophys Acta 1169:46–53

    Article  PubMed  CAS  Google Scholar 

  • King MD, Marsh D (1987) Headgroup and chain length dependence of phospholipid self-assembly studied by spin-label electron spin resonance. Biochemistry 26:1224–1231

    Article  PubMed  CAS  Google Scholar 

  • Kleywegt GJ, Henrick K, Dodson EJ, van Aalten DMF (2003) Pound-wise but penny-foolish: how well do micromolecules fare in macromolecular refinement? Structure 11:1051–1059

    Article  PubMed  CAS  Google Scholar 

  • Klyne W, Prelog V (1960) Description of steric relationships across single bonds. Experientia 16:521–523

    Article  CAS  Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    Article  PubMed  CAS  Google Scholar 

  • Lange C, Nett JH, Trumpower BL, Hunte C (2001) Specific roles of protein–phospholipid interactions in the yeast cytochrome bc 1 complex structure. EMBO J 20:6591–6600

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lee AG (2011) Biological membranes: the importance of molecular detail. Trends Biochem Sci 36:493–500

    Article  PubMed  CAS  Google Scholar 

  • Li S, Lin HN, Wang ZQ, Huang C (1994) Identification and characterization of kink motifs in 1-palmitoyl-2-oleoyl-phosphatidylcholines: a molecular mechanics study. Biophys J 66:2005–2018

    Article  PubMed  CAS  Google Scholar 

  • Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292

    Article  PubMed  CAS  Google Scholar 

  • London E, Feigenson GW (1981) Fluorescence quenching in model membranes. 2. Determination of the local lipid environment of the calcium adenosine triphosphatase from sarcoplasmic reticulum. Biochemistry 20:1939–1948

    Article  PubMed  CAS  Google Scholar 

  • Luecke H, Schobert B, Richter H-T, Cartailler J-P, Lanyi JK (1999) Structure of bacteriorhodopsin at 1.55 Å resolution. J Mol Biol 291:899–911

    Article  PubMed  CAS  Google Scholar 

  • Marius P, Alvis SJ, East JM, Lee AG (2005) The interfacial lipid binding site on the potassium channel KcsA is specific for anionic phospholipids. Biophys J 89:4081–4089

    Article  PubMed  CAS  Google Scholar 

  • Marius P, Zagnoni M, Sandison ME, East JM, Morgan H, Lee AG (2008) Binding of anionic lipids to at least three nonannular sites on the potassium channel KcsA is required for channel opening. Biophys J 94:1689–1698

    Article  PubMed  CAS  Google Scholar 

  • Marsh D (1974) Statistical mechanics of the fluidity of phospholipid bilayers and membranes. J Membrane Biol 18:145–162

    Article  CAS  Google Scholar 

  • Marsh D (2003) Lipid-binding proteins: structure of the phospholipid ligands. Protein Sci 12:2109–2117

    Article  PubMed  CAS  Google Scholar 

  • Marsh D (2008a) Electron spin resonance in membrane research: protein–lipid interactions. Methods 46:83–96

    Article  PubMed  CAS  Google Scholar 

  • Marsh D (2008b) Energetics of hydrophobic matching in lipid–protein interactions. Biophys J 94:3996–4013

    Article  PubMed  CAS  Google Scholar 

  • Marsh D, Horváth LI (1998) Structure, dynamics and composition of the lipid–protein interface. Perspectives from spin-labelling. Biochim Biophys Acta 1376:267–296

    Article  PubMed  CAS  Google Scholar 

  • Marsh D, Páli T (2006) Lipid conformation in crystalline bilayers and in crystals of transmembrane proteins. Chem Phys Lipids 141:48–65

    Article  PubMed  CAS  Google Scholar 

  • McAuley KE, Fyfe PK, Ridge JP, Isaacs NW, Cogdell RJ, Jones MR (1999) Structural details of an interaction between cardiolipin and an integral membrane protein. Proc Natl Acad Sci USA 96:14706–14711

    Article  PubMed  CAS  Google Scholar 

  • Meier P, Sachse J-H, Brophy PJ, Marsh D, Kothe G (1987) 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 USA 84:3704–3708

    Article  PubMed  CAS  Google Scholar 

  • Moser M, Marsh D, Meier P, Wassmer K-H, Kothe G (1989) 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 55:111–123

    Article  PubMed  CAS  Google Scholar 

  • Mouritsen OG, Bloom M (1984) Mattress model of lipid–protein interactions in membranes. Biophys J 46:141–153

    Article  PubMed  CAS  Google Scholar 

  • Nogi T, Fathir I, Kobayashi M, Nozawa T, Miki K (2000) Crystal structures of photosynthetic reaction center and high-potential iron-sulfur protein from Thermochromatium tepidum: thermostability and electron transfer. Proc Natl Acad Sci USA 97:13561–13566

    Article  PubMed  CAS  Google Scholar 

  • Oldfield E (1982) NMR of protein-lipid interactions in model and biological membrane systems. In: Martonosi EN (ed) Membranes and transport, vol 1. Plenum Press, New York, pp 115–123

    Chapter  Google Scholar 

  • Páli T, Marsh D (2001) Tilt, twist and coiling in β-barrel membrane proteins: relation to infrared dichroism. Biophys J 80:2789–2797

    Article  PubMed  Google Scholar 

  • Pascher I (1996) The different conformations of the glycerol region of crystalline acylglycerols. Curr Opin Struct Biol 6:439–448

    Article  PubMed  CAS  Google Scholar 

  • Pascher I, Sundell S (1986) Membrane lipids: preferred conformational states and their interplay. The crystal structure of dilauroylphosphatidyl-N,N-dimethylethanolamine. Biochim Biophys Acta 855:68–78

    Article  CAS  Google Scholar 

  • Pascher I, Sundell S, Harlos K, Eibl H (1987) Conformation and packing properties of membrane lipids: the crystal structure of sodium dimyristoylphosphatidylglycerol. Biochim Biophys Acta 896:77–88

    Article  PubMed  CAS  Google Scholar 

  • Pascher I, Lundmark M, Nyholm P-G, Sundell S (1992) Crystal structures of membrane lipids. Biochim Biophys Acta 1113:339–373

    Article  PubMed  CAS  Google Scholar 

  • Pearson RH, Pascher I (1979) The molecular structure of lecithin dihydrate. Nature (Lond) 281:499–501

    Article  CAS  Google Scholar 

  • Pebay-Peyroula E, Rosenbusch JP (2001) High-resolution structures and dynamics of membrane protein–lipid complexes: a critique. Curr Opin Struct Biol 11:427–432

    Article  PubMed  CAS  Google Scholar 

  • Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trézéguet V, Lauquin GJM, Brandolin G (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426:39–44

    Article  PubMed  CAS  Google Scholar 

  • Peelen SJCJ, Sanders JC, Hemminga MA, Marsh D (1992) 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 31:2670–2677

    Article  PubMed  CAS  Google Scholar 

  • Plesniak LA, Yu L, Dennis EA (1995) Conformation of micellar phospholipid bound to the active site of phospholipase A2. Biochemistry 34:4943–4951

    Article  PubMed  CAS  Google Scholar 

  • Ponder JW, Richards FM (1987) Tertiary templates for proteins. Use of packing criteria in the enumeration of allowed sequences for different structural classes. J Mol Biol 193:775–791

    Article  PubMed  CAS  Google Scholar 

  • Powell GL, Knowles PF, Marsh D (1985) 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 816:191–194

    Article  PubMed  CAS  Google Scholar 

  • Powell GL, Knowles PF, Marsh D (1987) Spin label studies on the specificity of interaction of cardiolipin with beef heart cytochrome oxidase. Biochemistry 26:8138–8145

    Article  PubMed  CAS  Google Scholar 

  • Russell NJ, Harwood JL (1979) Changes in the acyl lipid composition of photosynthetic bacteria grown under photosynthetic and non-photosynthetic conditions. Biochem J 181:339–345

    PubMed  CAS  Google Scholar 

  • Ryba NJP, Marsh D (1992) 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 31:7511–7518

    Article  PubMed  CAS  Google Scholar 

  • Ryba NJP, Horváth LI, Watts A, Marsh D (1987) Molecular exchange at the lipid-rhodopsin interface: spin-label electron spin resonance studies of rhodopsin-dimyristoyl phosphatidylcholine recombinants. Biochemistry 26:3234–3240

    Article  PubMed  CAS  Google Scholar 

  • Scott DL, Sigler PB (1994) Structure and catalytic mechanism of secretory phospholipase A2. Adv Protein Chem 45:53–88

    Article  PubMed  CAS  Google Scholar 

  • Seelig J (1977) Deuterium magnetic resonance: theory and application to lipid membranes. Q Rev Biophys 10:358–418

    Article  Google Scholar 

  • Seelig J, Gally HU (1976) Investigation of phosphatidylethanolamine bilayers by deuterium and phosphorus-31 nuclear magnetic resonance. Biochemistry 15:5199–5204

    Article  PubMed  CAS  Google Scholar 

  • Seelig A, Seelig J (1974) Dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry 13:4839–4845

    Article  PubMed  CAS  Google Scholar 

  • Seelig J, Seelig A (1980) Lipid conformation in model membranes and biological membranes. Q Rev Biophys 13:19–61

    Article  PubMed  CAS  Google Scholar 

  • Seelig J, Gally HU, Wohlgemuth R (1977) Orientation and flexibility of the choline head group in phosphatidylcholine bilayers. Biochim Biophys Acta 467:109–119

    Article  PubMed  CAS  Google Scholar 

  • Seelig J, Seelig A, Tamm L (1982) Nuclear magnetic resonance and lipid–protein interactions. In: Jost PC, Griffith OH (eds) Lipid–protein interactions, vol 2. Wiley, New York, pp 127–148

    Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418

    Article  PubMed  CAS  Google Scholar 

  • Sundaralingam M (1972) Molecular structures and conformations of phospholipids and sphingomyelins. Ann N Y Acad Sci 195:324–355

    Article  PubMed  CAS  Google Scholar 

  • Svensson-Ek M, Abramson J, Larsson G, Törnroth S, Brzezinski P, Iwata S (2002) The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J Mol Biol 321:329–339

    Article  PubMed  CAS  Google Scholar 

  • Takeda K, Matsui Y, Sato H, Hino T, Kanamori E, Okumura H, Yamane T, Kamiya N, Kouyama T (2000) Deposition 1QM8 in the Protein Database

  • Thunnissen MMGM, Ab E, Kalk KH, Drenth J, Dijkstra BW, Kuipers OP, Dijkman R, de Haas GH, Verheij HM (1990) X-ray structure of phospholipase A2 complexed with a substrate derived inhibitor. Nature 347:689–691

    Article  PubMed  CAS  Google Scholar 

  • Träuble H (1971) The movement of molecules across lipid membranes: a molecular theory. J Membrane Biol 4:193–208

    Article  Google Scholar 

  • Tsukihara T, Shimokata K, Katayama Y, Shimada H, Muramoto K, Aoyama H, Mochizuki M, Shinzawa-Itoh K, Yamashita A, Yao M, Ishimura Y, Yoshikawa S (2003) The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc Natl Acad Sci USA 100:15304–15309

    Article  PubMed  CAS  Google Scholar 

  • Valiyaveetil FI, Zhou YF, MacKinnon R (2002) Lipids in the structure, folding, and function of the KcsA K+ channel. Biochemistry 41:10771–10777

    Article  PubMed  CAS  Google Scholar 

  • van Tilbeurgh H, Egloff MP, Martinez C, Rugani N, Verger R, Cambillau C (1993) Interfacial activation of the lipase–procolipase complex by mixed micelles revealed by X-ray crystallography. Nature 362:814–820

    Article  PubMed  Google Scholar 

  • Yankovskaya V, Horsefield R, Törnröth S, Luna-Chavez C, Miyoshi H, Léger C, Byrne B, Cecchini G, Iwata S (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299:700–704

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi Y-I, Kim KK, Hung L-W, Crofts AR, Berry EA, Kim S-H (1998) Electron transfer by domain movement in cytochrome bc 1. Nature 392:677–684

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

DM gratefully acknowledges financial assistance from Christian Griesinger and the Dept. of NMR-Based Structural Biology.

Author information

Authors and Affiliations

  1. Max-Planck-Institut für biophysikalische Chemie, 37070, Göttingen, Germany

    Derek Marsh

  2. Institute of Biophysics, Biological Research Centre, 6701, Szeged, Hungary

    Tibor Páli

Authors
  1. Derek Marsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tibor Páli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Derek Marsh.

Additional information

Special Issue: Structure, function, folding and assembly of membrane proteins—Insight from Biophysics.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marsh, D., Páli, T. Orientation and conformation of lipids in crystals of transmembrane proteins. Eur Biophys J 42, 119–146 (2013). https://doi.org/10.1007/s00249-012-0816-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-012-0816-6

Keywords

Search

Navigation