Skip to main content
SpringerLink
Log in

Line Narrowing in Oriented-Sample NMR of Membrane Proteins

  • Chapter
  • First Online:
Book cover Protein NMR

Part of the book series: Biological Magnetic Resonance ((BIMR,volume 32))

  • 1770 Accesses

Abstract

The growing need for structure determination of membrane proteins incorporated within their native bilayers calls for the development of novel experimental methods and membrane mimetics for the structure-function studies of these important biological constituents. Solid-state NMR of macroscopically aligned samples has emerged as a powerful tool that enables studies of membrane proteins under their native-like conditions. Here we present an alternative alignment method based on anodic aluminum oxide nanopores, which are capable of incorporating a broad repertoire of lipids. Moreover, the temperature and pH stability of lipid bilayers within the nanopores enable solid-state NMR experiments under a wider range of conditions than ever before. Uniaxial motional averaging by rotational diffusion of membrane proteins ensures the line narrowing of experimental NMR linewidths, thus, providing structural and dynamic information for the lipid-embedded proteins.

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

Access this chapter

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

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abragam A (1961) The principles of nuclear magnetism. Oxford University Press, London, p 599

    Google Scholar 

  • Alaouie AM, Smirnov AI (2005) Cooperativity and kinetics of phase transitions in nanopore-confined bilayers studied by differential scanning calorimetry. Biophys J 88(2):L11–L13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alaouie AM, Smirnov AI (2006) Formation of a ripple phase in nanotubular dimyristoylphosphatidylcholine bilayers confined inside nanoporous aluminum oxide substrates observed by DSC. Langmuir 22(13):5563–5565

    Article  CAS  PubMed  Google Scholar 

  • Allen JA, Halverson-Tamboli RA, Rasenick MM (2007) Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8(2):128–140

    Article  CAS  PubMed  Google Scholar 

  • Andrew ER, Bradbury A, Eades RG (1958) Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182(4650):1659

    Article  CAS  Google Scholar 

  • Bielecki A, Kolbert AC, de Groot HJM, Griffin RG, Levitt MH (1990) Frequency-switched Lee-Goldburg sequences in solids. Adv Magn Reson 14:111

    Google Scholar 

  • Borst P, Evers R, Kool M, Wijnholds J (2000) A family of drug transporters: the multidrug resistance-associated proteins. J Natl Cancer Inst 92(16):1295–1302

    Article  CAS  PubMed  Google Scholar 

  • Brender JR, Durr UH, 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. Biochimic Biophys Acta. 1768(9):2026–2029

    Article  CAS  Google Scholar 

  • Burger K, Gimpl G, Fahrenholz F (2000) Regulation of receptor function by cholesterol. Cell Mol Life Sci 57(11)1577–1592

    Article  CAS  PubMed  Google Scholar 

  • Cady SD, Hong M (2009) Effects of amantadine on the dynamics of membrane-bound influenza A M2 transmembrane peptide studied by NMR relaxation. J Biomol NMR 45:185–196

    Article  CAS  PubMed  Google Scholar 

  • Cady SD, Goodman C, Tatko CD, DeGrado WF, Hong M (2007) Determining the orientation of uniaxially rotating membrane proteins using unoriented samples: A (2)H, (13)C, and (15)N solid-state NMR investigation of the dynamics and orientation of a transmembrane helical bundle. J Am Chem Soc 129(17):5719–5729

    Article  CAS  PubMed  Google Scholar 

  • Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature. 463(7281):689–U127

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chekmenev EY, Hu J, Gor'kov PL, Brey WW, Cross TA, Ruuge A, Smirnov AI ( 2005) 15N and 31P solid-state NMR study of transmembrane domain alignment of M2 protein of influenza A virus in hydrated cylindrical lipid bilayers confined to anodic aluminum oxide nanopores. J Magn Reson 173(2):322–327

    Article  CAS  PubMed  Google Scholar 

  • Chekmenev, EY, Gor'kov PL, Cross TA, Alaouie AM, Smirnov AI (2006) Flow-through lipid nanotube arrays for structure-function studies of membrane proteins by solid-state NMR spectroscopy. Biophys J 91:3076–3084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng X, Jo S, Marassi FM, Im W (2013) NMR-based simulation studies of Pf1 coat protein in explicit membranes. Biophys J 105(3):691–698

    Article  CAS  PubMed  Google Scholar 

  • Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SGF, Thian FS, Kobilka TS, Choi HJ, Kuhn P, Weis WI, Kobilka BK, Stevens RC, (2007)High-resolution crystal structure of an engineered human beta(2)-adrenergic G protein-coupled receptor. Science 318(5854):1258–1265

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cornell BA, Separovic F, Baldassi AJ, Smith R (1988) Conformation and orientation of gramicidin-a in oriented phospholipid-bilayers measured by solid-state C-13 NMR. Biophys J 53(1):67–76

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • De Angelis AA, Opella SJ (2007) Bicelle samples for solid-state NMR of membrane proteins. Nat Protoc 2(10):2332–2338

    Article  PubMed  Google Scholar 

  • De Angelis AA, Nevzorov AA, Park SH, Howell SC, Mrse AA, Opella SJ (2004) High-resolution NMR spectroscopy of membrane proteins in “unflipped” bicelles. J Am Chem Soc 126:15340–15341

    Article  PubMed  Google Scholar 

  • De Angelis AA, Howell SC, Nevzorov AA, Opella SJ, (2006) 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(37):12256–12267

    Article  PubMed  Google Scholar 

  • Dowhan W, Bogdanov M (2009) Lipid-dependent membrane protein topogenesis. Annu Rev Biochem 78:515–540

    Google Scholar 

  • Durr UHN, Gildenberg M, Ramamoorthy A (2012) The magic of bicelles lights up membrane protein structure. Chem Rev 112(11):6054–6074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dvinskikh SV, Yamamoto K, Ramamoorthy A (2006) Heteronuclear isotopic mixing separted local field NMR spectroscopy. J Chem Phys 125:034507

    Article  Google Scholar 

  • Esteban-Martin S, Strandberg E, Fuertes G, Ulrich AS, Salgado J (2009) Influence of whole-body dynamics on (15)N PISEMA NMR spectra of membrane proteins: a theoretical analysis. Biophys J 96(8):3233–3241

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fraser JS, van den Bedem H, Samelson AJ, Lang PT, Holton JM, Echols N, Alber T (2011) Accessing protein conformational ensembles using room-temperature X-ray crystallography. Proc Natl Acad Sci U S A 108(39):16247–16252

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freed JH (1972) ESR line shapes and saturation in the slow motional region—the stochastic Liouville approach. In: Muus LT, Atkins PW (eds) Electron spin relaxation in liquids. Plenum Press: New York. pp 387–410

    Google Scholar 

  • Furoiscorbin S, Smith JC, Kneller GR, (1993) Picosecond timescale rigid-helix and side-chain motions in deoxymyoglobin. Proteins 16(2):141–154

    Article  CAS  Google Scholar 

  • Gaede HC, Luckett KM, Polozov IV, Gawrisch K (2004) Multinuclear NMR studies of single lipid bilayers supported in cylindrical aluminum oxide nanopores. Langmuir 20(18):7711–7719

    Article  CAS  PubMed  Google Scholar 

  • Gleason NJ, Vostrikov VV, Greathouse DV, Koeppe RE (2013) Buried lysine, but not arginine, titrates and alters transmembrane helix tilt. Proc Natl Acad Sci U S A 110(5):1692–1695

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Glover KJ, Whiles JA, Wu G, Yu N-J, Deems R, Struppe JO, Stark RE, Komives EA, Vold RR (2001) Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys J 81:2163–2171

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gor’kov PL, Chekmenev EY, Fu RQ, Hu J, Cross TA, cotton M, Brey WW (2006) A large volume flat coil probe for oriented membrane proteins. J Magn Reson 181(1):9–20

    Article  PubMed  Google Scholar 

  • Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, Weis WI, Kobilka BK (2012) Structure of the delta-opioid receptor bound to naltrindole. Nature 485(7398):400–U171

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gurevich VV, Gurevich EV (2008a) How and why do GPCRs dimerize? Trends Pharm Sci 29(5):234–240

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gurevich VV, Gurevich EV (2008b) GPCR monomers and oligomers: it takes all kinds. Trends Neurosci 31(2):74–81

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gustavsson M, Traaseth NJ, Karim CB, Lockamy EL, Thomas DD, Veglia G (2011) Lipid-mediated folding/unfolding of phospholamban as a regulatory mechanism for the sarcoplasmic reticulum Ca(2+)-ATPase. J Mol Biol 408(4):755–765

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hester RK, Ackerman JL, Neff BL, Waugh JS (1976) Separated local field spectra in NMR—determination of structure in solids. Phys Rev Letts 36(18):1081–1083

    Google Scholar 

  • Holt A, Rougier L, Reat V, Jolibois F, Saurel O, Czaplicki J, Killian JA, Milon A (2010) Order parameters of a transmembrane helix in a fluid bilayer: case study of a WALP peptide. Biophys J 98(9):1864–1872

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jo S, Im W (2011) Transmembrane helix orientation and dynamics: insights from ensemble dynamics with solid-state NMR observables. Biophys J 100(12):2913–2921

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karp ES, Inbaraj JJ, Laryukhin M, Lorigan GA (2006) Electron paramagnetic resonance studies of an integral membrane peptide inserted into aligned phospholipid bilayer nanotube arrays. J Am Chem Soc 128(37):12070–12071

    Article  CAS  PubMed  Google Scholar 

  • Ketchem RR, Hu W, Cross TA (1993) High-resolution conformation of gramidicin A in a lipid bilayer by solid-state NMR. Science 261:1457–1460

    Article  CAS  PubMed  Google Scholar 

  • Kubo R (1969) Stochastic theories of randomly modulated systems. J Phy Soc Jpn Suppl 26:1–5

    Article  Google Scholar 

  • Kucerka N, Liu YF, Chu NJ, Petrache HI, Tristram-Nagle ST, Nagle JF (2005) Structure of fully hydrated fluid phase DMPC and DLPC lipid bilayers using X-ray scattering from oriented multilamellar arrays and from unilamellar vesicles. Biophys J 88(4):2626–2637

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu YF, Nagle JF (2004) Diffuse scattering provides material parameters and electron density profiles of biomembranes. Phys Review E 69(4):040901

    Google Scholar 

  • Lorigan GA, Dave PC, Tiburu EK, Damodaran K, Abu-Baker S, Karp ES, Gibbons WJ, Minto RE (2004) Solid-state NMR spectroscopic studies of an integral membrane protein inserted into aligned phospholipid bilayer nanotube arrays. J Am Chem Soc 126(31):9504–9505

    Article  CAS  PubMed  Google Scholar 

  • Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, Sunahara RK, Pardo L, Weis WI, Kobilka BK, Granier S (2012) Crystal structure of the mu-opioid receptor bound to a morphinan antagonist. Nature 485(7398):321–U170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marassi FM, Opella SJ (2000) A solid-state NMR index of helical membrane protein structure and topology. J Magn Reson 144:150–155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marassi FM, Opella SJ (2004) Structure determination of membrane proteins by NMR spectroscopy. Chem Rev 104:3587–3606

    Article  PubMed Central  PubMed  Google Scholar 

  • Marek A, Tang W, Milikisiyants S, Nevzorov AA, Smirnov AI (2015) Nanotube array method for studying lipid-induced conformational changes of a membrane protein by solid-state NMR. Biophys J 108(1):5–9

    Google Scholar 

  • Masuda H, Fukuda K (1995) Ordered metal nanohole arrays made by a two-step replication of honeycomb structures of anodic alumina. Science 268:1466–1468

    Article  CAS  PubMed  Google Scholar 

  • McDermott, A (2009) Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu Rev Biophys 38:385–403

    Article  CAS  PubMed  Google Scholar 

  • Mote KR, Gopinath T, Traaseth NJ, Kitchen J, Gor'kov PL, Brey WW, Veglia G (2011) Multidimensional oriented solid-state NMR experiments enable the sequential assignment of uniformly N-15 labeled integral membrane proteins in magnetically aligned lipid bilayers. J Biomol NMR 51(3):339–346

    Article  CAS  PubMed  Google Scholar 

  • Murray DT, Das N, Cross TA (2013) Solid state NMR strategy for characterizing native membrane protein structures. Acc Chem Res 46(9):2172–2181

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nesmelov YE, Karim CB, Song L, Fajer PG, Thomas DD (2007) Rotational Dynamics of Phospholamban Determined by Multifrequency Electron Paramagnetic Resonance. Biophys J 93:2805–2812

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nevzorov AA (2011a) Orientational and motional narrowing of solid-state NMR lineshapes of uniaxially aligned membrane proteins. J Phys Chem B 115(51):15406–15414

    Article  CAS  PubMed  Google Scholar 

  • Nevzorov AA (2011b) Ergodicity and efficiency in cross-polarization of NMR of static solids. J Magn Reson 209:161–166

    Article  CAS  PubMed  Google Scholar 

  • Nevzorov AA (2014) Coherent and stochastic averaging in solid-state NMR. J Magn Reson 249:9–15

    Article  CAS  Google Scholar 

  • Nevzorov AA, Opella SJ (2007) Selective averaging for high-resolution solid-state NMR spectroscopy of aligned samples. J Magn Reson 185:59–70

    Article  CAS  PubMed  Google Scholar 

  • Nevzorov AA, Moltke S, Heyn MP, Brown MF (1999) Solid-state NMR lineshapes of uniaxially-oriented immobile systems. J Am Chem Soc 121:7636–7643

    Article  CAS  Google Scholar 

  • Nevzorov AA, De Angelis AA, Park SH, Opella SJ (2005) Uniaxial motional averaging of the chemical shift anisotropy of membrane proteins in bilayer environments. In: Ramamoorthy A (ed) NMR spectroscopy of biological solids. Marcel Dekker, New York, pp 177–190

    Google Scholar 

  • Nielsen NC, Daugaard P, Langer V, Thomsen JK, Nielsen S, Sorensen OW, Jakobsen HJ (1995) A flat-coil NMR probe with hydration control of oriented phospholipid-bilayer samples. J Biomol NMR 5(3):311–314

    CAS  PubMed  Google Scholar 

  • Opella SJ, Zeri AC, Park SH (2008) Structure, dynamics, and assembly of filamentous bacteriophages by nuclear magnetic resonance spectroscopy. Annu Rev Phys Chem 59:635–657

    Article  CAS  PubMed  Google Scholar 

  • Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289(5480):739–745

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Opella SJ (2005) Tilt angle of a trans-membrane helix is determined by hydrophobic mismatch. J Mol Biol 350(2):310–318

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Opella SJ (2010) Triton X-100 as the “short-chain lipid” improves the magnetic alignment and stability of membrane proteins in phosphatidylcholine bilayers for oriented-sample solid-state NMR spectroscopy. J Am Chem Soc 132(36):12552–12553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Mrse AA, Nevzorov AA, Mesleh MF, Oblatt-Montal M, Montal M, Opella SJ (2003) Three-dimensional structure of the channel-forming trans-membrane domain of virus protein “u” (Vpu) from HIV-1. J Mol Biol 333:409–424

    Article  CAS  PubMed  Google Scholar 

  • Park SH, De Angelis AA, Nevzorov AA, Wu CH, Opella SJ (2006a)Three-dimensional structure of the transmembrane domain of Vpu from HIV-1 in aligned phospholipid bicelles. Biophys J 91:3032–3042

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Mrse AA, Nevzorov AA, De Angelis AA, Opella SJ (2006b) Rotational diffusion of membrane proteins in aligned phospholipid bilayers by solid-state NMR spectroscopy. J Magn Reson 178(1):162–165

    Article  CAS  PubMed  Google Scholar 

  • Park SH, Loudet C, Marassi FM, Dufourc EJ, Opella SJ (2008) Solid-state NMR spectroscopy of a membrane protein in biphenyl phospholipid bicelles with the bilayer normal parallel to the magnetic field. J Magn Reson 193(1):133–138

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Das BB, De Angelis AA, Scrima M, Opella SJ (2010a) Mechanically, magnetically, and “rotationally aligned” membrane proteins in phospholipid bilayers give equivalent angular constraints for NMR structure determination. J Phys Chem B 114:13995–14003

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Marassi FM, Black D, Opella SJ (2010b) Structure and dynamics of the membrane-bound form of Pf1 coat protein: implications of structural rearrangement for virus assembly. Biophys J 99(5):1465–1474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Berkamp S, Cook GA, Chan MK, Viadiu H, Opella SJ (2011) Nanodiscs versus macrodiscs for NMR of membrane proteins. Biochemistry 50(42):8983–8985

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Park SH, Das BB, Casagrande F, Tian Y, Nothnagel HJ, Chu MN, Kiefer H, Maier K, De Angelis AA, Marassi FM, Opella SJ (2012) Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491(7426):779–783

    Google Scholar 

  • Prosser RS, Hwang JS, Vold RR (1998) Magnetically aligned phospholipid bilayers with positive ordering: a new model membrane system. Biophys J 74:2405–2418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rainey JK, Sykes BD (2005) Optimizing oriented planar-supported lipid samples for solid-state protein NMR. Biophys J 89(4):2792–2805

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rasmussen SGF, DeVree BT, Zou YZ, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah STA, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the beta(2) adrenergic receptor-Gs protein complex. Nature 477(7366):549–U311

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Redfield AG (1965) The theory of relaxation processes. Adv Magn Reson 1:1–32

    Article  Google Scholar 

  • Renault M, Bos MP, Tommassen J, Baldus M (2011) Solid-state NMR on a large multidomain integral membrane protein: the outer membrane protein assembly factor BamA. J Am Chem Soc 133(12):4175–4177

    Article  CAS  PubMed  Google Scholar 

  • Saffman PG, Delbruck M (1975) Brownian motion in biological membranes. Proc Natl Acad Sci U S A 72:3111–3113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sanders CR, Hare BJ, Howard KP, Prestegard JH (1994) Magnetically oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog NMR Spectrosc 26:421–444

    Article  CAS  Google Scholar 

  • Schneider DJ, Freed JH (1989) Spin relaxation and motional dynamics. Adv Chem Phys 73:387–527

    CAS  Google Scholar 

  • Shapiro RA, Brindley AJ, Martin RW (2010) Thermal stabilization of DMPC/DHPC bicelles by addition of cholesterol sulfate. J Am Chem Soc 132(33):11406–11407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sharma M, Yi MG, Dong H, Qin HJ, Peterson E, Busath DD, Zhou HX, Cross TA (2010) Insight into the mechanism of the Influenza A Proton channel from a structure in a lipid bilayer. Science 330(6003):509–512

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shi LC, Lake EMR, Ahmed MAM, Brown LS, Ladizhansky V (2009) Solid-state NMR study of proteorhodopsin in the lipid environment: secondary structure and dynamics. Biochim Biophys Acta 1788(12):2563–2574

    Article  CAS  PubMed  Google Scholar 

  • Smirnov AI, Poluektov OG (2003) Substrate-supported lipid nanotube arrays. J Am Chem Soc 125(28):8434–8435

    Article  CAS  PubMed  Google Scholar 

  • Soubias O, Gawrisch K (2007) Nuclear magnetic resonance investigation of oriented lipid membranes. In: Dopico A (ed) Methods in membrane lipids. Humana Press, New York, pp 77–88

    Google Scholar 

  • Soubias O, Polozov IV, Teague WE, Yeliseev AA, Gawrisch K (2006) Functional reconstitution of rhodopsin into tubular lipid bilayers supported by nanoporous media. Biochemistry 45(51):15583–15590

    Article  CAS  PubMed  Google Scholar 

  • Soubias O, Niu S-L, Mitchell DC, Gawrisch K (2008) Lipid-rhodopsin hydrophobic mismatch alters rhodopsin helical content. J Am Chem Soc 130:12465–12471

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spille JH, Zurn A, Hoffmann C, Lohse MJ, Harms GS (2011) Rotational diffusion of the alpha(2a) adrenergic receptor revealed by FlAsH labeling in living cells. Biophys J 100(4):1139–48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Spooner PJR, Friesen RHE, Knol J, Poolman B, Watts A, (2000) Rotational mobility and orientational stability of a transport protein in lipid membranes. Biophys J 79(2):756–766

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steeb WH (1997)Matrix Calculus and Kronecker Product with Applications and C++ Programs, Singapore: World Scientific. 254

    Google Scholar 

  • Stein RA, Hustedt EJ, Staros JV, Beth AH (2002) Rotational Dynamics of the Epidermal Growth Factor Receptor. Biochemistry 41:1957–1964

    Article  CAS  PubMed  Google Scholar 

  • Straus SK, Scott WRP, Watts A (2003) Assessing the effects of time and spatial averaging in N-15 chemical shift/N-15-H-1 dipolar correlation solid state NMR experiments. J Biomol NMR 26(4):283–295

    Article  CAS  PubMed  Google Scholar 

  • Tamm LK (2005) Protein-lipid interactions: from membrane domains to cellular networks. Protein-lipid interactions: from membrane domains to cellular networks, ed. 1–444

    Google Scholar 

  • 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(2):77–81

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Traaseth NJ, Shi L, Verardi R, Mullen DG, Barany G, Veglia G (2009) Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc Natll Acad Sci U S A 106(25):10165–10170

    Article  CAS  Google Scholar 

  • Triba MN, Devaux PF, Warschawski DE (2006) Effects of lipid chain length and unsaturation on bicelles stability. A phosphorus NMR study. Biophys J 91(4):1357–1367

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vold RR, Prosser RS (1996) Magnetically oriented phospholipid bilayered micelles for structural studies of polypeptides. Does the ideal bicelle exist? J Magn Reson B 113:267–271

    Article  CAS  Google Scholar 

  • Wang J, Denny J, Tian C, Kim S, Mo Y, Kovacs F, Song Z, Nishimura K, Gan Z, Fu R, Quine JR, Cross TA (2000) Imaging membrane protein helical wheels. J Magn Reson 144:162–167

    Google Scholar 

  • Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, Henderson R, Leslie AGW, Tate CG, Schertler GFX (2008) Structure of a beta(1)-adrenergic G-protein-coupled receptor. Nature 454(7203):486–491

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wattraint O, Sarazin C (2006) Static and MAS solid-state study of supported phospholipid bilayer cylindrically oriented. Comptes Rendus Chimie 9(3–4):408–412

    Article  CAS  Google Scholar 

  • Wu CH, Ramamoorthy A, Opella SJ (1994) High-resolution heteronuclear dipolar solid-state NMR spectroscopy. J Magn Reson A 109:270–272

    Article  Google Scholar 

  • Yamamoto K, Gildenberg M, Ahuja S, Im SC, Pearcy P, Waskell L, Ramamoorthy A (2013) Probing the transmembrane structure and topology of microsomal cytochrome-P450 by solid-state NMR on temperature-resistant bicelles. Scientific Reports. 3

    Google Scholar 

  • Yildirim MA, Goh KI, Cusick ME, Barabasi AL, Vidal M (2007) Drug-target network. Nat Biotechnol 25(10):1119–1126

    Article  CAS  PubMed  Google Scholar 

  • Zweckstetter M, Bax A (2001) Characterization of molecular alignment in aqueous suspensions of Pf1 bacteriophage. J Biomol NMR 20(4):365–377

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The assistance of Dr. Antonin Marek (NCSU) in the preparation of Fig. 7 is gratefully acknowledged. The fabrication of AAO and development of lipid nanotube technology for lipid bilayers and membrane proteins was supported by US DOE Contract DE-FG02-02ER15354 to AIS. OS NMR experiments were supported by NSF MRI 1229547 to AAN.

Author information

Authors and Affiliations

  1. Department of Chemistry, North Carolina State University, 2620 Yarbrough Drive, 27695-8204, Raleigh, NC, USA

    Alexander A. Nevzorov & Alex I. Smirnov PhD

Authors
  1. Alexander A. Nevzorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alex I. Smirnov PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alex I. Smirnov PhD .

Editor information

Editors and Affiliations

  1. Department of Chemistry and Biochemistry, University of Denver, Denver, Colorado, USA

    Lawrence Berliner

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Nevzorov, A., Smirnov, A. (2015). Line Narrowing in Oriented-Sample NMR of Membrane Proteins. In: Berliner, L. (eds) Protein NMR. Biological Magnetic Resonance, vol 32. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-7621-5_5

Download citation

Publish with us

Policies and ethics

Search

Navigation