1,900
Views
29
CrossRef citations to date
0
Altmetric
Research Article

Solution NMR studies of peptide-lipid interactions in model membranes

Pages 155-176 | Received 22 Dec 2011, Accepted 22 Feb 2012, Published online: 14 May 2012

References

  • Abrams FS, London E. 1993. Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 32:10826–10831.
  • Akke M, Palmer AG. 1996. Monitoring macromolecular motions on microsecond to millisecond time scales by R(1)r-R(1) constant relaxation time NMR spectroscopy. J Am Chem Soc 118:911–912.
  • Andersson A, Mäler L. 2002. NMR solution structure and dynamics of motilin in isotropic phospholipid bicellar solution. J Biomol NMR 24:103–112.
  • Andersson A, Almqvist J, Hagn F, Mäler L. 2004. Diffusion and dynamics of penetratin in different membrane mimicking media. BBA 1661:18–25.
  • Andersson A, Mäler L. 2005. Magnetic resonance investigations of lipid motion in isotropic bicelles. Langmuir 21:7702–7709.
  • Andersson A, Biverståhl H, Nordin J, Danielsson J, Lindahl E, Mäler L. 2007. The membrane-induced structure of melittin is correlated with the fluidity of the lipids. Biochim Biophys Acta 1768:115–121.
  • Aniansson E, Wall S, Almgren M, Hoffmann H, Kielmann I, Ulbricht W, 1976. Theory of the kinetics of micellar equilibria and quantitative interpretation of chemical relaxation studies of micellar solutions of ionic surfactants. J Phys Chem 80:905–922.
  • Arora A, Tamm LK. 2001. Biophysical approaches to membrane protein structure determination. Curr Opin Struct Biol 11:540–547.
  • Arora A, Abildgaard F, Bushweller JH, Tamm LK. 2001. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat Struct Biol 8:334–338.
  • Baas BJ, Denisov IG, Sligar SG. 2004. Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch Biochem Biophys 430:218–228.
  • Bárány-Wallje E, Andersson A, Gräslund A, Mäler L. 2004. NMR solution structure and position of transportan in neutral phospholipid bicelles. FEBS Lett 567:265–269.
  • Bárány-Wallje E, Andersson A, Gräslund A, Mäler L. 2006. Dynamics of transportan in bicelles is surface charge dependent. J Biomol NMR 35:137–147.
  • Batenburg AM, van Esch JH, de Kruijff B. 1988. Melittin-induced changes of the macroscopic structure of phosphatidylethanolamines. Biochemistry 27:2324–2331.
  • Bayburt TH, Grinkova YV, Sligar SG. 2002. Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Letters 2:853–856.
  • Bayburt TH, Sligar SG. 2002. Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc Natl Acad Sci USA 99:6725.
  • Bayburt TH, Sligar SG. 2003. Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers. Protein Sci 12:2476–2481.
  • Biverståhl H, Andersson A, Gräslund A, Mäler L. 2004. NMR solution structure and membrane interaction studies of the N-terminal sequence (1–30) of the bovine prion protein. Biochemistry 43:14940–14947.
  • Bodenhausen G, Wagner G, Rance M, Sørensen O, Wüthrich K, Ernst R. 1984. Longitudinal two-spin order in 2D exchange spectroscopy (NOESY). J Magn Reson 59:542–550.
  • Borch J, Hamann T. 2009. The nanodisc: a novel tool for membrane protein studies. Biol Chem 390:805–814.
  • Brender JR, Dürr UHN, Heyl D, Budarapu MB, Ramamoorthy A. 2007. Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. Biochim Biophys Acta 1768:2026–2029.
  • Brown MF, Ribeiro AA, Williams GD. 1983. New view of lipid bilayer dynamics from 2H and 13C NMR relaxation time measurements. Proc Natl Acad Sci USA 80:4325–4329.
  • Brown MF, Thurmond RL, Dodd SW, Otten D, Beyer K. 2000. Elastic deformation of membrane bilayers probed by deuterium NMR relaxation. Biochemistry 39:1833.
  • Butterwick JA, MacKinnon R. 2010. Solution structure and phospholipid interactions of the isolated voltage-sensor domain from KvAP. J Mol Biol 403:591–606.
  • Callaghan P, Komlosh M, Nydén M. 1998. High magnetic field gradient PGSE NMR inthe presence of a large polarizing field. J Magn Reson 133:177–182.
  • Cantor CR, Schimmel PR. 1980. Biophysical chemistry. San Francisco: WH Freeman.
  • Cavanagh J, Fairbrother WJ, Palmer AG, Rance M, Skelton NJ. 2007. Protein NMR spectroscopy. Burlington, MA: Academic Press.
  • Chattopadhyay A, Harikumar K. 1996. Dependence of critical micelle concentration of a zwitterionic detergent on ionic strength: Implications in receptor solubilization. FEBS Lett 391:199–202.
  • Chattopadhyay A, London E. 1987. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 26:39–45.
  • Chill JH, Louis JM, Baber JL, Bax A. 2006. Measurement of 15N relaxation in detergent-solubilized tetrameric KcsA potassium channel. J Biomol NMR 36:123–136.
  • Chill JH, Naider F. 2011. A solution NMR view of protein dynamics in the biological membrane. Curr Opin Struct Biol 21:627–633.
  • Chou JJ, Kaufman JD, Stahl SJ, Wingfield PT, Bax A. 2002. Micelle-induced curvature in a water-insoluble HIV-1 env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel. J Am Chem Soc 124:2450–2451.
  • Chou JJ, Baber JL, Bax A. 2004. Characterization of phospholipid mixed micelles by translational diffusion. J Biomol NMR 29:299–308.
  • Chromy BA, Arroyo E, Blanchette CD, Bench G, Benner H, Cappuccio JA, 2007. Different apolipoproteins impact nanolipoprotein particle formation. J Am Chem Soc 129:14348–14354.
  • Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, Gronenborn AM. 1990. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989–4991.
  • Clore GM, Gronenborn AM. 1994. Multidimensional heteronuclear nuclear magnetic resonance of proteins. Meth Enzymol 239:349–363.
  • Czajlik A, Meskó E, Penke B, Perczel A. 2002. Investigation of penetratin peptides part 1. The environment dependent conformational properties of penetratin and two of its derivatives. J Peptide Sci 8:151–171.
  • Damberg P, Jarvet J, Gräslund A. 2001. Micellar systems as solvents in peptide and protein structure determination. Meth Enzymol 339:271–285.
  • De Angelis AAD, Jones D, Grant C, Park S, Mesleh M, Opella S. 2005. NMR experiments on aligned samples of membrane proteins. Meth Enzymol 394:350–382.
  • De Angelis AA, Opella SJ. 2007. Bicelle samples for solid-state NMR of membrane proteins. Nature Protocols 2:2332–2338.
  • De Angelis AA, Howell SC, Nevzorov AA, Opella SJ. 2005. Structure determination of a membrane protein with two trans-membrane helices in aligned phospholipid bicelles by solid-state NMR spectroscopy. J Am Chem Soc 128:12256–12267.
  • 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.
  • de Planque MRR, Kruijtzer JAW, Liskamp RMJ, Marsh D, Greathouse DV, Koeppe RE, 1999. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides. J Biol Chem 274:20839–20846.
  • de Planque MRR, Goormaghtigh E, Greathouse DV, Koeppe RE II, Kruijtzer JAW, Liskamp RMJ, 2001. Sensitivity of single membrane-spanning α-helical peptides to hydrophobic mismatch with a lipid bilayer: Effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry 40:5000–5010.
  • de Planque MRR, Boots JWP, Rijkers DTS, Liskamp RMJ, Greathouse DV, Killian JA. 2002. The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane α-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 41:8396–8404.
  • de Planque MRR, Bonev BB, Demmers JAA, Greathouse DV, Koeppe RE II, Separovic F, 2003. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 42:5341–5348.
  • de Planque MRR, Killian JA. 2003. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol Membr Biol 20:271–284.
  • Dempsey CE. 1990. The actions of melittin on membranes. Biochim Biophys Acta 1031:143–161.
  • Denisov I, Grinkova Y, Lazarides A, Sligar S. 2004. Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J Am Chem Soc 126:3477–3487.
  • Derossi D, Joliot AH, Chassaing G, Prochiantz A. 1994. The third helix of the antennapedia homeodomain translocates through biological membranes. J Biol Chem 269:10444–10450.
  • Derossi D, Calvet S, Trembleau A, Brunissen A, Chassaing G, Prochiantz A. 1996. Cell internalization of the third helix of the antennapedia homeodomain is receptor-independent. J Biol Chem 271:18188–18193.
  • Derossi D, Chassing G, Prochiantz A. 1998. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol 8:84–87.
  • Deshayes S, Plénat T, Aldrian-Herrada G, Divita G, Le Grimellec C, Heitz F. 2004. Primary amphipathic cell-penetrating peptides: structural requirements and interactions with model membranes. Biochemistry 43:7698–7706.
  • Deshayes S, Morris M, Divita G, Heitz F. 2005. Cell-penetrating peptides: Tools for intracellular delivery of therapeutics. Cell Mol Life Sci 62:1839–1849.
  • Dufourc EJ, Smith ICP, Dufourcq J. 1986. Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR. Biochemistry 25:6448–6455.
  • Dufourcq J, Faucon JF, Fourche G, Dasseux JL, Le Maire M, Gulik-Krzywicki T. 1986. Morphological changes of phosphatidylcholine bilayers induced by melittin: Vesicularization, fusion, discoidal particles. Biochim Biophys Acta 859:33–48.
  • Dürr UHN, Yamamoto K, Im SC, Waskell L, Ramamoorthy A. 2007. Solid-state NMR reveals structural and dynamical properties of a membrane-anchored electron-carrier protein, cytochrome b 5. J Am Chem Soc 129:6670–6671.
  • Dvinskikh S, Dürr U, Yamamoto K, Ramamoorthy A. 2006. A high resolution solid state NMR approach for the structural studies of bicelles. J Am Chem Soc 128:6326.
  • Dvinskikh SV, Castro V, Sandström D. 2005. Probing segmental order in lipid bilayers at variable hydration levels by amplitude-and phase-modulated cross-polarization NMR. Phys Chem Chem Phys 7:3255–3257.
  • Ellena JF, Lepore LS, Cafiso DS. 1993. Estimating lipid lateral diffusion in phospholipid vesicles from carbon-13 spin-spin relaxation. J Phys Chem 97:2952–2957.
  • Englander S, Downer N, Teitelbaum H. 1972. Hydrogen exchange. Annu Rev Biochem 41:903–924.
  • Evans FD, Wennerström H. 1999. The colloidal domain. New York: Wiley. 1999.
  • Fernández C, Hilty C, Bonjour S, Adeishvili K, Pervushin K, Wüthrich K. 2001. Solution NMR studies of the integral membrane proteins OmpX and OmpA from Escherichia coli. FEBS Lett 504:173–178.
  • Fernández C, Hilty C, Wider G, Guntert P, Wüthrich K. 2004. NMR structure of the integral membrane protein OmpX. J Mol Biol 336:1211–1221.
  • Filippov A, Orädd G, Lindblom G. 2004. Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys J 86:891–896.
  • Freed J. 2000. New technologies in electron spin resonance. Annu Rev Phys Chem 51:655–689.
  • Funasaki N, Hada S, Neya S. 1991. Odd-even alternation in the aggregation number dependence of stepwise aggregation constants. J Phys Chem 95:1846–1850.
  • Fuson M, Prestegard J. 1983. Dynamics of an interfacial methylene in dimyristoylphosphatidylcholine vesicles using carbon-13 spin relaxation. Biochemistry 22:1311–1316.
  • Gabriel NE, Roberts MF. 1984. Spontaneous formation of stable unilamellar vesicles. Biochemistry 23:4011–4015.
  • Gaede HC, Gawrisch K. 2003. Lateral diffusion rates of lipid, water, and a hydrophobic drug in a multilamellar liposome. Biophys J 85:1734–1740.
  • Gaemers S, Bax A. 2001. Morphology of three lyotropic liquid crystalline biological NMR media studied by translational diffusion anisotropy. J Am Chem Soc 123:12343–12352.
  • Gautier A, Mott HR, Bostock MJ, Kirkpatrick JP, Nietlispach D. 2010. Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nature Struct Mol Biol 17:768–774.
  • Gent M, Prestegard J. 1974. Comparison of 13C spin-lattice relaxation times in phospholipid vesicles and multilayers. Biochem Biophys Res Commun 58:549–555.
  • Glover KJ, Whiles JA, Wu G, Yu N, Deems R, Struppe JO, 2001. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys J 81:2163–2171.
  • Glück JM, Wittlich M, Feuerstein S, Hoffmann S, Willbold D, Koenig BW. 2009. Integral membrane proteins in nanodiscs can be studied by solution NMR spectroscopy. J Am Chem Soc 131:12060–12061.
  • Gräslund A, Mäler L. 2011. Testing membrane interactions of CPPs. Methods Mol Biol 683:33–40.
  • Guterstam P, Madani F, Hirose H, Takeuchi T, Futaki S, EL Andaloussi S, 2009. Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate. Biochim Biophys Acta 1788:2509–2517.
  • Habermann E. 1972. Bee and wasp venoms. Science 177:314.
  • Halle B, Wennerström H. 1981. Interpretation of magnetic resonance data from water nuclei in heterogeneous systems. J Chem Phys 75:1928–1943.
  • Hansen DF, Vallurupalli P, Kay LE. 2008. Using relaxation dispersion NMR spectroscopy to determine structures of excited, invisible protein states. J Biomol NMR 41:113–120.
  • Hauser H. 2000. Short-chain phospholipids as detergents. Biochim Biophys Acta 1508:164–181.
  • Herbig ME, Weller K, Krauss U, Beck-Sickinger AG, Merkle HP, Zerbe O. 2005. Membrane surface-associated helices promote lipid interactions and cellular uptake of human calcitonin-derived cell penetrating peptides. Biophys J 89:4056–4066.
  • Higashijima T, Uzu S, Nakajima T, Ross EM. 1988. Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem 263:6491.
  • Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G. 2008. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206.
  • Hope M, Bally M, Mayer L, Janoff A, Cullis P. 1986. Generation of multilamellar and unilamellar phospholipid vesicles. Chem Phys Lipids 40:89–107.
  • Hristova K, Wimley WC. 2011. A look at arginine in membranes. J Membr Biol 239:49–56.
  • Hwang PM, Bishp RE, Kay LE. 2004. The integral membrane enzyme PagP alternates between two dynamically distinct states. Proc Natl Acad Sci USA 101:9618–9623.
  • Itri R, Amaral L. 1991. Distance distribution function of sodium dodecyl sulfate micelles by x-ray scattering. J Phys Chem 95:423–427.
  • Jarvet J, Zdunek J, Damberg P, Gräslund A. 1997. Three-dimensional structure and position of porcine motilin in sodium dodecyl sulfate micelles determined by 1H NMR. Biochemistry 36:8153–8163.
  • Jeener J, Meier BH, Bachmann P, Ernst RR. 1979. Investigation of exchange processes by two-dimensional NMR spectroscopy. J Chem Phys 71:4546.
  • Jhun BH, Berenski CJ, Craik JD, Paterson ARP, Cass CE, Jung CY. 1991. Glucose and nucleoside transporters of human erythrocytes: effects of detergents on immunoadsorption of a membrane protein to its monoclonal antibody. Biochim Biophys Acta 1061:149–155.
  • Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, 2003a. X-ray structure of a voltage-dependent K+ channel. Nature 423:33–41.
  • Jiang Y, Ruta V, Chen J, Lee A, MacKinnon R. 2003b. The principle of gating charge movement in a voltage-dependent K+ channel. Nature 423:42–48.
  • Jonas A. 1986. Reconstitution of high-density lipoproteins. Meth Enzymol 128:553–582.
  • Kainosho M, Torizawa T, Iwashita Y, Terauchi T, Mei Ono A, Güntert P. 2006. Optimal isotope labelling for NMR protein structure determinations. Nature 440:52–57.
  • Kang CB, Li Q. 2011. Solution NMR study of integral membrane proteins. Curr Opin Chem Biol 15:560–569.
  • Katsaras J, Harroun TA, Pencer J, Nieh MP. 2005. “Bicellar” lipid mixtures as used in biochemical and biophysical studies. Naturwissenschaften 92:355–366.
  • Killian JA, Salemink I, de Planque MRR, Lindblom G, Koeppe RE II, Greathouse DV. 1996. Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane α-helical peptides: Importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry 35:1037–1045.
  • Killian JA. 1998. Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta 1376:401–415.
  • Killian JA, von Heijne G. 2000. How proteins adapt to a membrane-water interface. Trends Biochem Sci 25:429–434.
  • Killian JA. 2003. Synthetic peptides as models for intrinsic membrane proteins. FEBS Lett 555:134–138.
  • Kim HJ, Howell SC, Van Horn WD, Jeon YH, Sanders CR. 2009. Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog Nucl Magn Reson Spectrosc 55:335.
  • Kobayashi S, Takeshima K, Park CB, Kim SC, Matsuzaki K. 2000. Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: Proline as a translocation promoting factor. Biochemistry 39:8648–8654.
  • Korstanje LJ, van Faassen EE, Levine YK. 1989. Reorientational dynamics in lipid vesicles and liposomes studied with ESR: Effects of hydration, curvature and unsaturation. Biochim Biophys Acta 982:196–204.
  • Kosol S, Zangger K. 2010. Dynamics and orientation of a cationic antimicrobial peptide in two membrane-mimetic systems. J Struct Biol 170:172–179.
  • Kowalewski J, Mäler L. 2006. Nuclear spin relaxation in liquids: Theory, experiments, and applications. Boca Raton, FL: Taylor & Francis.
  • Langel Ü. 2002. Cell-penetrating peptides. Processes and applications. Boca Raton, FL: CRC Press.
  • Lau TL, Kim C, Ginsberg MH, Ulmer TS. 2009. The structure of the integrin αIIbβ3 transmembrane complex explains integrin transmembrane signalling. EMBO J 28:1351–1361.
  • Lau TL, Partridge AW, Ginsberg MH, Ulmer TS. 2008. Structure of the integrin β3 transmembrane segment in phospholipid bicelles and detergent micelles. Biochemistry 47:4008–4016.
  • Lauterwein J, Bosch C, Brown LR, Wuthrich K. 1979. Physicochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim Biophys Acta 556:244–264.
  • Leftin A, Brown MF. 2011. An NMR database for simulations of membrane dynamics. Biochim Biophys Acta 1808:818–839.
  • le Maire M, Champeil P, Møller JV. 2000. Interaction of membrane proteins and lipids with solubilizing detergents. Biochimica et Biophysica Acta (BBA) – Biomembranes 1508:86–111.
  • Lepore LS, Ellena JF, Cafiso DS. 1992. Comparison of the lipid acyl chain dynamics between small and large unilamellar vesicles. Biophys J 61:767–775.
  • Liang B, Arora A, Tamm LK. 2010. Fast-time scale dynamics of outer membrane protein A by extended model-free analysis of relaxation data. Biochim Biophys Acta 1798:68–76.
  • Lin TL, Chen SH, Gabriel NE, Roberts MF. 1986. The use of small-angle neutron scattering to determine the structure and interaction of dihexanoylphosphatidylcholine micelles. J Am Chem Soc 108:3499–3507.
  • Lin TL, Chen SH, Gabriel NE, Roberts MF. 1987. Small-angle neutron scattering techniques applied to the study of polydisperse rodlike diheptanoylphosphatidylcholine micelles. J Phys Chem 91:406–413.
  • Lin TL, Liu CC, Roberts MF, Chen SH. 1991. Structure of mixed short-chain lecithin/long-chain lecithin aggregates studied by small-angle neutron scattering. J Phys Chem 95:6020–6027.
  • Lind J, Rämö T, Klement MLR, Bárány-Wallje E, Epand RM, Epand RF, 2007. High cationic charge and bilayer interface-binding helices in a regulatory lipid glycosyltransferase. Biochemistry 46:5664–5677.
  • Lind J, Nordin J, Mäler L. 2008. Lipid dynamics in fast-tumbling bicelles with varying bilayer thickness: Effect of model transmembrane peptides. Biochim Biophys Acta 1778:2526–2534.
  • Lindberg M, Jarvet J, Langel U, Gräslund A. 2001. Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 40:3141–3149.
  • Lindberg M, Biverståhl H, Gräslund A, Mäler L. 2003. Structure and positioning comparison of two variants of penetratin in two different membrane mimicking systems by NMR. FEBS Journal 270:3055–3063.
  • Lindblom G, Orädd G. 1994. NMR studies of translational diffusion in lyotropic liquid crystals and lipid membranes. Prog Nuc Mag Reson Specstrosc 26:483–516.
  • Lindgren M, Gallet X, Soomets U, Hällbrink M, Bråkenhielm E, Pooga M, 2000a. Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjug Chem 11:619–626.
  • Lindgren M, Hällbrink M, Prochiantz A, Langel Ü. 2000b. Cell-penetrating peptides. Trends Pharmacol Sci 21:99–103.
  • Lipari G, Szabo A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546–4559.
  • Lipari G, Szabo A. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 104:4559–4570.
  • Liu JJ, Horst R, Katritch V, Stevens RC, Wüthrich K. 2012. Biased signaling pathways in b2-adrenergic receptor characterized by 19F-NMR. Science 335:1106–110.
  • Long SB, Tao X, Campbell EB, MacKinnon R. 2007. Atomic structure of a voltage-dependent K channel in a lipid membrane-like environment. Nature 450:376–382.
  • Loria JP, Rance M, Palmer AG III. 1999. A relaxation-compensated carr-purcell-meiboom-gill sequence for characterizing chemical exchange by NMR spectroscopy. J Am Chem Soc 121:2331–2332.
  • Lou Y, Ge M, Freed JH. 2001. A multifrequency ESR study of the complex dynamics of membranes. J Phys Chem B 105:11053–11056.
  • Lu Z, Van Horn WD, Chen J, Mathew S, Zent R, Sanders CR. 2012. Bicelles at low concentrations. Mol. Pharmaceutics 9:752–761.
  • Luchette PA, Vetman TN, Prosser RS, Hancock REW, Nieh MP, Glinka CJ, 2001. Morphology of fast-tumbling bicelles: A small angle neutron scattering and NMR study. Biochim Biophys Acta 1513:83–94.
  • Lundberg P, Magzoub M, Lindberg M, Hällbrink M, Jarvet J, Eriksson L, 2002. Cell membrane translocation of the N-terminal (1–28) part of the prion protein. Biochem Biophys Res Commun 299:85–90.
  • Lyukmanova EN, Shenkarev ZO, Paramonov AS, Sobol AG, Ovchinnikova TV, Chupin VV, 2008. Lipid-protein nanoscale bilayers: A versatile medium for NMR investigations of membrane proteins and membrane-active peptides. J Am Chem Soc 130:2140–2141.
  • Madani F, Lindberg S, Langel U, Futaki S, Gräslund A. 2011. Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011:414729.
  • Magzoub M, Eriksson LE, Gräslund A. 2002. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles: Effects of surface charge and peptide concentration. Biochim Biophys Acta 1563:53–63.
  • Magzoub M, Eriksson LE, Gräslund A. 2003. Comparison of the interaction, positioning, structure induction and membrane perturbation of cell-penetrating peptides and non-translocating variants with phospholipid vesicles. Biophys Chem 103:271–288.
  • Magzoub M, Gräslund A. 2004. Cell-penetrating peptides: From inception to application. Q Rev Biophys 37:147–195.
  • Magzoub M, Oglecka K, Pramanik A, Eriksson LE, Graslund A. 2005. Membrane perturbation effects of peptides derived from the N-termini of unprocessed prion proteins. Biochim Biophys Acta 1716:126–136.
  • Mäler L, Gräslund A. 2009. Artificial membrane models for the study of macromolecular delivery. Methods Mol Biol 480:129–139.
  • Mäler L, Gräslund A. 2011. NMR studies of three-dimensional structure and positioning of CPPs in membrane model systems. Methods Mol Biol 683:57–67.
  • Marcotte I, Auger M. 2005. Bicelles as model membranes for solid-and solution-state NMR studies of membrane peptides and proteins. Concepts Magn Reson 24:17–37.
  • Matsuzaki K, Murase O, Fujii N, Miyajima K. 1995. Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 34:6521–6526.
  • Mayer C, Grobner G, Muller K, Weisz K, Kothe G. 1990. Orientation-dependent deuteron spin-lattice relaxation times in bilayer membranes: Characterization of the overall lipid motion. Chem Phys Lett 165:155–161.
  • Mayer L, Hope M, Cullis P. 1986. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim Biophys Acta 858:161–168.
  • Mayer M, Meyer B. 1999. Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angewandte Chemie 38:1784–1788.
  • Mayer M, Meyer J. 2001. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J Am Chem Soc 123:6108–6117.
  • Metcalfe EE, Zamoon J, Thomas DD, Veglia G. 2004. 1H/15N Heteronuclear NMR spectroscopy shows four dynamic domains for phospholamban reconstituted in dodecylphosphocholine micelles. Biophys J 87:1205–1214.
  • Molday R, Englander S, Kallen R. 1972. Primary structure effects on peptide group hydrogen exchange. Biochemistry 11:150–158.
  • Morein S, Koeppe RE II, Lindblom G, de Kruijff B, Antoinette Killian J. 2000. The effect of peptide/lipid hydrophobic mismatch on the phase behavior of model membranes mimicking the lipid composition in Escherichia coli membranes. Biophys J 78:2475–2485.
  • Morein S, Strandberg E, Killian J, Persson S, Arvidson G, Koeppe R, 1997. Influence of membrane-spanning alpha-helical peptides on the phase behavior of the dioleoylphosphatidylcholine/water system. Biophys J 73:3078–3088.
  • Nakano M, Fukuda M, Kudo T, Miyazaki M, Wada Y, Matsuzaki N, 2009. Static and dynamic properties of phospholipid bilayer nanodiscs. J Am Chem Soc 131:8308–8312.
  • Nath A, Atkins WM, Sligar SG. 2007. Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46:2059–2069.
  • Nieh M-P, Glinka CJ, Krueger S, Prosser RS, Katsaras J. 2001. SANS study of the structural phases of magnetically alignable lanthanide-doped phospholipid mixtures. Langmuir 17:2629–2638.
  • Nunziante M, Gilch S, Schätzl HM. 2003. Essential role of the prion protein N terminus in subcellular trafficking and half-life of cellular prion protein. J Biol Chem 278:3726.
  • Öhman A, Lycksell P, Juréus A, Langel Ü, Bartfai T, Gräslund A. 1998. NMR study of the conformation and localization of porcine galanin in SDS micelles. Comparsion with an inactive analog and a galanin receptor antagonist. Biochemistry 37:9169–9178.
  • Orädd G, Lindblom G. 2004a. Nmr studies of lipid lateral diffusion in the DMPC/gramicidin D/water system: Peptide aggregation and obstruction effects. Biophys J 87:980–987.
  • Orädd G, Lindblom G. 2004b. Lateral diffusion studied by pulsed field gradient NMR on oriented lipid membranes. Magn Reson Chem 42:123–131.
  • Ottiger M, Bax A. 1998. Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J Biomol NMR 12:361–372.
  • Oxenoid K, Sönnichsen FD, Sanders CR. 2002. Topology and secondary structure of the N-terminal domain of diacylglycerol kinase. Biochemistry 41:12876–12882.
  • Oxenoid K, Kim HJ, Jacob J, Sönnichsen FD, Sanders CR. 2004. NMR assignments for a helical 40 kDa membrane protein. J Am Chem Soc 126:5048–5049.
  • Palmer AG. 2004. NMR characterization of the dynamics of biomacromolecules. Chem Rev 104:3623–3640.
  • Palmer AG, Kroenke CD, Loria JP. 2001. Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Meth Enzymol 339:204–238.
  • Papadopoulos E, Oglecka K, Mäler L, Jarvet J, Wright PE, Dyson HJ, 2006. NMR solution structure of the peptide fragment 1–30, derived from unprocessed mouse doppel protein, in DHPC micelles. Biochemistry 45:159–166.
  • Papavoine CHM, Christiaans BEC, Folmer RHA, Konings RNH, Hilbers CW. 1998. Solution structure of the M13 major coat protein in detergent micelles: A basis for a model of phage assembly involving specific residues. J Mol Biol 282:401–419.
  • Papavoine CHM, Remerowski ML, Horstink LM, Konings RNH, Hilbers CW, van de Ven FJM. 1997. Backbone dynamics of the major coat protein of bacteriophage M13 in detergent micelles by 15N nuclear magnetic resonance relaxation measurements using the model-free approach and reduced spectral density mapping. Biochemistry 36:4015–4026.
  • Papavoine CHM, Aelen J, Konings RNH, Hilbers CW, Ven FJM. 1995. NMR studies of the major coat protein of bacteriophage M13. Eur J Biochem 232:490–500.
  • Papavoine C, Konings R, Hilbers C, van der Van F. 1994. Location of M13 coat protein in sodium dodecyl micelles as determined by NMR. Biochemistry 33:12990–12997.
  • Park SH, Berkamp S, Cook GA, Chan MK, Viadiu H, Opella SJ. 2011. Nanodiscs vs. macrodiscs for NMR of membrane proteins. Biochemistry 50:8983–8985.
  • Pastor RW, Venable RM, Karplus M, Szabo A. 1988. A simulation based model of NMR T relaxation in lipid bilayer vesicles. J Chem Phys 89:1128.
  • Patching SG. 2011. NMR structures of polytopic integral membrane proteins. Mol Membr Biol 28:370–397.
  • Pervushin K, Riek R, Wider G, Wütrich K. 1997. Attenuated T2 relaxation by mutual cancellation of dipole-dipole couplings and chemical shift anisotropy inidcates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94:12366–12371.
  • Pintacuda G, Otting G. 2002. Identification of protein surfaces by NMR measurements with a paramagnetic gd (III) chelate. J Am Chem Soc 124:372–373.
  • Poget SF, Cahill SM, Girvin ME. 2007. Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. J Am Chem Soc 129:2432–2433.
  • Poget SF, Girvin ME. 2007. Solution NMR of membrane proteins in bilayer mimics: Small is beautiful, but sometimes bigger is better. Biochimica et Biophysica Acta (BBA) – Biomembranes 1768:3098–3106.
  • Pointer-Keenan CD, Lee DK, Hallok K, Tan A, Zand R, Ramamoorthy A. 2004. Investigation of the interaction of myelin basic protein with phospholipid bilayers using solid-state NMR spectroscopy. Chem Phys Lipids 132:47–54.
  • Pooga M, Hällbrink M, Zorko M, Langel Ü. 1998. Cell penetration by transportan. FASEB J 12:67.
  • Pooga M, Kut C, Kihlmark M, Hällbrink M, Fernaeus S, Raid R, 2001. Cellular translocation of proteins by transportan. FASEB J 15:1451–1453.
  • Popot JL. 2010. Amphipols, nanodiscs, and fluorinated surfactants: Three nonconventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737–775.
  • Prestegard J. 1990. Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO. Biophys J 58:447–460.
  • Prosser RS, Hwang JS, Vold RR. 1998. Magnetically aligned bicelles with a positive ordering: A new model membrane system. Biophys J 74:2405–2418.
  • Prosser RS, Evanics F, Kitevski JL, Al-Abdul-Wahid MS. 2006. Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 45:8453–8465.
  • Ram P, Prestegard J. 1988. Magnetic field induced ordering of bile salt/phospholipid micelles: New media for NMR structural investigations. Biochim Biophys Acta 940:289–294.
  • Ramamoorthy A, Thennarasu S, Lee DK, Tan A, Maloy L. 2006a. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys J 91:206–216.
  • Ramamoorthy A, Thennarasu S, Tan A, Lee DK, Clayberger C, Krensky AM. 2006b. Cell selectivity correlates with membrane-specific interactions: A case study on the antimicrobial peptide G15 derived from granulysin. Biochim Biophys Acta 1758:154–163.
  • Raschle T, Hiller S, Yu TY, Rice AJ, Walz T, Wagner G. 2009. Structural and functional characterization of the integral membrane protein VDAC-1 in lipid bilayer nanodiscs. J Am Chem Soc 131:17777–17779.
  • Raschle T, Hiller S, Etzkorn M, Wagner G. 2010. Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr Opin Struct Biol 20:471–479.
  • Reckel S, Gottstein D, Stehle J, Löhr F, Verhoefen M-K, Takeda M, 2011. Solution NMR structure of proteorhodopsin. Angew Chem Int Ed 50:11942–11946.
  • Ritchie T, Grinkova Y, Bayburt T, Denisov I, Zolnerciks J, Atkins W, 2009. Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Meth Enzymol 464:211–231.
  • Rosen MJ, Kunjappu JT. 2012. Surfactants and interfacial phenomena. Hoboken: Wiley.
  • Rowe BA, Neal SL. 2003. Fluorescence probe study of bicelle structure as a function of temperature: Developing a practical bicelle structure model. Langmuir 19:2039–2048.
  • Ruzza P, Calderan A, Guiotto A, Osler A, Borin G. 2004. Tat cell-penetrating peptide has the characteristics of a poly (proline) II helix in aqueous solution and in SDS micelles. J Pept Sci 10:423–426.
  • Sanders CR, Schwonek JP. 1992. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 31:8898–8905.
  • Sanders CR II, Hare BJ, Howard KP, Prestegard JH. 1994. Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog Nucl Magn Reson Spectrosc 26:421–444.
  • Sanders CR, Landis GC. 1995. Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 34:4030–4040.
  • Sanders CR, Prosser RS. 1998. Bicelles: A model membrane system for all seasons? Structure 6:1227–1234.
  • Sanders CR, Oxenoid K. 2000. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins1. Biochim Biophys Acta 1508:129–145.
  • Sanders CR, Sonnichsen F. 2006. Solution NMR of membrane proteins: Practice and challenges. Magn Reson Chem 44:S24–S40.
  • Sargent D, Schwyzer R. 1986. Membrane lipid phase as catalyst for peptide-receptor interactions. Proc Natl Acad Sci USA 83:5774.
  • Schnell JR, Chou JJ. 2008. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451:591–595.
  • Seelig J. 1978. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim Biophys Acta 515:105–140.
  • Seelig J, Seelig A. 1980. Lipid conformation in model membranes and biological membranes. Q Rev Biophys 13:19–61.
  • Seelig J. 1977. Deuterium magnetic resonance: Theory and application to lipid membranes. Q Rev Biophys 10:353–418.
  • Seigneuret M, Lévy D. 1995. A high-resolution 1 H NMR approach for structure determination of membrane peptides and proteins in non-deuterated detergent: Application to mastoparan X solubilized in n-octylglucoside. J Biomol NMR 5:345–352.
  • Sharma M, Yi M, Dong H, Qin H, Peterson E, Busath DD, 2010. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330:509.
  • Shenkarev ZO, Lyukmanova EN, Paramonov AS, Shingarova LN, Chupin VV, Kirpichnikov MP, 2010a. Lipid-protein nanodiscs as reference medium in detergent screening for high-resolution NMR studies of integral membrane proteins. J Am Chem Soc 132:5628–5629.
  • Shenkarev ZO, Paramonov AS, Lyukmanova EN, Shingarova LN, Yakimov SA, Dubinnyi MA, 2010b. NMR structural and dynamical investigation of the isolated voltage-sensing domain of the potassium channel KvAP: Implications for voltage gating. J Am Chem Soc 132:5630–5637.
  • Shenkarev ZO, Balandin SV, Trunov KI, Paramonov AS, Sukhanov SV, Barsukov LI, 2011. Molecular mechanism of action of b-hairpin antimicrobial peptide arenicin: Oligomeric structure in dodecylphosphocholine micelles and pore formation in planar lipid bilayers. Biochemistry 50:6255–6265.
  • Shintani M, Yoshida K, Sakuraba S, Nakahara M, Matubayasi N. 2011. NMR-NOE and MD simulation study on phospholipid membranes: Dependence on membrane dimater and multiple time scale dynamics. J Phys Chem B 115:9106–9115.
  • Singer SJ, Nicolson GL. 1972. Fluid mosaic model of the structure of cell membranes. Science 175:720–731.
  • Skelton NJ, Palmer AG III, Akke M, Kördel J, Rance M, Chazin WJ. 1993. Practical aspects of two-dimentional proton-detected 15N spin relaxation measurements. J Magn Reson B 102:253–264.
  • Smith PES, Brender JR, Ramamoorthy A. 2009. Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: The case of islet amyloid polypeptide. J Am Chem Soc 131:4470–4478.
  • Stafford RE, Fanni T, Dennis EA. 1989. Interfacial properties and critical micelle concentration of lysophospholipids. Biochemistry 28:5113–5120.
  • Stejskal EO, Tanner JE. 1965. Spin diffusion measurements: Spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42:288.
  • Struppe J, Whiles JA, Vold RR. 2000. Acidic phospholipid bicelles: A versatile model membrane system. Biophys J 78:281–289.
  • Sunyach C, Jen A, Deng J, Fitzgerald KT, Frobert Y, Grassi J, 2003. The mechanism of internalization of glycosylphosphatidylinositol-anchored prion protein. EMBO J 22:3591–3601.
  • Szyperski T, Lüginbuhl P, Otting G, Güntert P, Wüthrich K. 1993. Protein dynamics studied by rotating frame N-15 spin relaxation times. J Biomol NMR 3:151–164.
  • Takeshima K, Chikushi A, Lee KK, Yonehara S, Matsuzaki K. 2003. Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J Biol Chem 278:1310–1315.
  • Tanford C, Reynolds JA. 1976. Characterization of membrane proteins in detergent solutions. Biochim Biophys Acta 457:133–170.
  • Tjandra N, Bax A. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111–1114.
  • Toke O, Bánóczi Z, Király P, Heinzmann R, Bürck J, Ulrich AS, 2011. A kinked antimicrobial peptide from Bombina maxima. I. Three-dimensional structure determined by NMR in membrane-mimicking environments. Eur J Biophys 40:447–462.
  • Tolman J, Flanagan J, Kennedy MA, Prestegard J. 1995. Nuclear magnetic dipole interactions in field-oriented proteins: Information for structure determination in solution. Proc Natl Acad Sci USA 92:9279.
  • Traaseth NJ, Veglia G. 2010. Probing excited states and activation energy for the integral membrane protein phospholamban by NMR CPMG relaxation dispersion experiments. Biochim Biophys Acta 1798:77–81.
  • Triba MN, Devaux PF, Warschawski DE. 2006. Effects of lipid chain length and unsaturation on bicelles stability. A phosphorus NMR study. Biophys J 91:1357–1367.
  • Triba MN, Warschawski DE, Devaux PF. 2005. Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys J 88:1887–1901.
  • Unnerståle S, Lind J, Papadopoulos E, Mäler L. 2009. Solution structure of the HsapBK K -channel voltage-sensor paddle sequence. Biochemistry 48:5813–5821.
  • van Dam L, Karlsson G, Edwards K. 2004. Direct observation and characterization of DMPC/DHPC aggregates under conditions relevant for biological solution NMR. Biochim Biophys Acta 1664:241–256.
  • Van Horn WD, Kim HJ, Ellis CD, Hadziselimovic A, Sulistijo ES, Karra MD, 2009. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324:1726.
  • Vinogradova O, Sönnichsen F, Sanders CR. 1998. On choosing a detergent for solution NMR studies of membrane proteins. J Biomol NMR 11:381–386.
  • Vold RR, Prosser RS, Deese AJ. 1997. Isotropic solutions of phospholipid bicelles: A new membrane mimetic for high-resolution NMR studies of polypeptides. J Biomol NMR 9:329–335.
  • Von Meerwall E, Kamat M. 1989. Effect of residual field gradients on pulsed-gradient NMR diffusion measurements. J Magn Reson 83:309–323.
  • Wagner G, Bodenhausen G, Mueller N, Rance M, Soerensen OW, Ernst RR, 1985. Exchange of two-spin order in nuclear magnetic resonance: Separation of exchange and cross-relaxation processes. J Am Chem Soc 107:6440–6446.
  • Wakamatsu K, Okada A, Miyazawa T, Ohya M, Higashijima T. 1992. Membrane-bound conformation of mastoparan-X, a G-protein-activating peptide. Biochemistry 31:5654–5660.
  • Walmsley AR, Zeng F, Hooper NM. 2003. The N-terminal region of the prion protein ectodomain contains a lipid raft targeting determinant. J Biol Chem 278:37241–37248.
  • Wang C, Grey MJ, Palmer AG. 2001. CPMG sequences with enhanced sensitivity to chemical exchange. J Biomol NMR 21:361–366.
  • Wang G. 2008. Structures of human host defense cathelicidin LL-37 and its smallest antimicrobial peptide KR-12 in lipid micelles. J Biol Chem 283:32637–32643.
  • Wang G, Elliott M, Cogen AL, Ezell EL, Gallo RL, Hancock REW. 2011. Structure, dynamics and antimicrobial and immune modulatory activities of human LL-23 and its single-residue variants mutated on the basis of homologous primate cathelicidins. Biochemistry 51:653–664.
  • Warschawski DE, Arnold AA, Beaugrand M, Gravel A, Chartrand É, Marcotte I. 2011. Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim Biophys Acta 1808:1957–1974.
  • Waskell L, Ramamoorthy A. 2007. The cytochromes P450 and b5 and their reductases – promising targets for structural studies by advanced solid-state NMR spectroscopy. Biochimica et Biophysica Acta (BBA) – Biomembranes 1768:3235–3259.
  • Weiss TM, van der Wel PCA, Killian JA, Koeppe RE II, Huang HW. 2003. Hydrophobic mismatch between helices and lipid bilayers. Biophys J 84:379–385.
  • Wennerström H, Lindblom G, Lindman B. 1974. Theoretical aspects on the NMR of quadrupolar ionic nuclei in micellar solutions and amphiphilic liquid crystals. Chem Scr 6:97–103.
  • Whiles JA, Glover KJ, Vold RR, Komives EA. 2002. Methods for studying transmembrane peptides in bicelles: Consequences of hydrophobic mismatch and peptide sequence. J Magn Reson 158:149–156.
  • Whiles JA, Brasseur R, Glover KJ, Melacini G, Komives EA, Vold RR. 2001. Orientation and effects of mastoparan X on phospholipid bicelles. Biophys J 80:280–293.
  • Wimley WC, Hristova K. 2011. Antimicrobial peptides: Successes, challenges and unanswered questions. J Membr Biol 239:27–34.
  • Wüthrich K. 1986. NMR of proteins and nucleic acids. New York: Wiley.
  • Yeagle P. 2005. The structure of biological membranes. Boca Raton, FL: CRC Press.
  • Zasloff M. 1987. Magainins, a class of antimicrobial peptides from xenopus skin: Isolation, characterization of two active forms, partial cDNA sequence of a precursor. Proc Natl Acad Sci USA 84:5549–5453.
  • Zinn-Justin S, Berthault P, Guenneugues M, Desvaux H. 1997. Off-resonance r.f. fields in heteronuclear NMR: Application to the study of slow motions. J Biomol NMR 10:363–372.
  • Zhang W, Smith SO. 2005. Mechanism of penetration of antp (43–58) into membrane bilayers. Biochemistry 44:10110–10118.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.