Skip to main content
SpringerLink
Log in

Probing membrane protein orientation and structure using fast magic-angle-spinning solid-state NMR

  • Published:
Journal of Biomolecular NMR Aims and scope Submit manuscript

Abstract

One and two-dimensional solid-state NMR experiments are discussed that permit probing local structure and overall molecular conformation of membrane-embedded polypeptides under Magic Angle Spinning. The functional dependence of a series of anisotropic recoupling schemes is analyzed using theoretical and numerical methods. These studies lead to the construction of a set of polarization dephasing or transfer units that probe local backbone conformation and overall molecular orientation within the same NMR experiment. Experimental results are shown for a randomly oriented peptide and for two model membrane–peptides reconstituted into lipid bilayers and oriented on polymer films according to a method proposed by Bechinger etal. [J. Am. Chem. Soc., 124, (2002), 1146–1147].

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

Similar content being viewed by others

Abbreviations

ssNMR:

solid state NMR

MAS:

Magic Angle Spinning

R.F.:

Radio Frequency

CSA:

Chemical Shift Anisotropy

CP:

Cross Polarization

APHH-CP:

Adiabatic-Passage Hartmann-Hahn Cross-Polarization

SPECIFIC-CP:

Spectrally Induced Filtering In Combination with Cross-Polarization

TPPM:

Two Pulse Phase Modulation

TPPI:

Time Proportional Phase Incrementation

DQ:

Double Quantum

SQ:

Single Quantum

POST-C7:

Permutationally Offset Stabilized C7

SPC-5:

Supercycled POST-C5

SD:

Spin Diffusion

AHT:

Average Hamiltonian Theory

TFE:

Trifluoroethanol

DMPC:

1,2-Dimyristoyl-sn-glycero-3-Phosphocholine

WALP23:

Trp-flanked poly(alanine-leucine) peptides

PEEK:

Polyetheretherketone

PTFE:

Polytetrafluoroethylene

Fmoc:

9-Fluorenylmethoxycarbonyl

References

  • E.R. Andrew A. Bradbury R.G Eades (1958) Nature 182 1659 Occurrence Handle10.1038/1821659a0 Occurrence Handle1958Natur.182.1659A

    Article  ADS  Google Scholar 

  • H.D. Arndt A. Vescovi A. Schrey J.R. Pfeifer U. Koert (2002) Tetrahedron 58 2789–2801 Occurrence Handle10.1016/S0040-4020(02)00179-5

    Article  Google Scholar 

  • S. Auge H. Mazarguil M. Tropis A. Milon (1997) J. Magn. Reson. 124 455–458 Occurrence Handle10.1006/jmre.1996.1051 Occurrence Handle1997JMagR.124..455A

    Article  ADS  Google Scholar 

  • M. Baldus (2002) Prog. NMR Spectrosc. 41 1–47 Occurrence Handle10.1016/S0079-6565(02)00007-9

    Article  Google Scholar 

  • M. Baldus D.G. Geurts S. Hediger B.H. Meier (1996) J. Magn. Reson. A118 140–144

    Google Scholar 

  • M. Baldus T.O. Levante B.H. Meier (1994a) Z. Naturforsch. Section a-a J. Phys. Sci. 49 80–88

    Google Scholar 

  • M. Baldus M. Tomaselli B.H. Meier R.R. Ernst (1994b) Chem. Phys. Lett. 230 329–336 Occurrence Handle10.1016/0009-2614(94)01209-1 Occurrence Handle1994CPL...230..329B

    Article  ADS  Google Scholar 

  • M. Baldus A.T. Petkova J. Herzfeld R.G. Griffin (1998) Mol. Phys. 95 1197–1207 Occurrence Handle1998MolPh..95.1197B

    ADS  Google Scholar 

  • A. Bax R. Freeman S.P. Kempsell (1980) J. Am. Chem. Soc. 102 4849–4851 Occurrence Handle10.1021/ja00534a056

    Article  Google Scholar 

  • B. Bechinger R. Kinder M. Helmle T.C.B. Vogt U. Harzer S. Schinzel (1999) Biopolymers 51 174–190 Occurrence Handle10.1002/(SICI)1097-0282(1999)51:3<174::AID-BIP2>3.0.CO;2-7

    Article  Google Scholar 

  • A.E. Bennett C.M. Rienstra M. Auger K.V. Lakshmi R.G. Griffin (1995) J. Chem. Phys. 103 6951–6958 Occurrence Handle10.1063/1.470372 Occurrence Handle1995JChPh.103.6951B

    Article  ADS  Google Scholar 

  • N. Bloembergen (1949) Physica 15 386–426 Occurrence Handle10.1016/0031-8914(49)90114-7 Occurrence Handle1949Phy....15..386B

    Article  ADS  Google Scholar 

  • A. Bockmann A. Lange A. Galinier S. Luca N. Giraud M. Juy H. Heise R. Montserret F. Penin M. Baldus (2003) J. Biomol. NMR 27 323–339 Occurrence Handle10.1023/A:1025820611009

    Article  Google Scholar 

  • M.L. Bodner C.M. Gabrys P.D. Parkanzky J. Yang C.A. Duskin D.P. Weliky (2004) Magn. Reson. Chem. 42 187–194 Occurrence Handle10.1002/mrc.1331

    Article  Google Scholar 

  • Brink, D.M. and Satchler, G.R. (1961) Angular Momentum, Oxford University Press.

  • M. Carravetta M. Eden X. Zhao A. Brinkmann M.H. Levitt (2000) Chem. Phys. Lett. 321 205–215 Occurrence Handle10.1016/S0009-2614(00)00340-7 Occurrence Handle2000CPL...321..205C

    Article  ADS  Google Scholar 

  • V.B. Cheng H.H. Suzukawa M. Wolfsber (1973) J. Chem. Phys. 59 3992–3999 Occurrence Handle10.1063/1.1680590 Occurrence Handle362848 Occurrence Handle1973JChPh..59.3992C

    Article  MathSciNet  ADS  Google Scholar 

  • G. Cornilescu F. Delaglio A. Bax (1999) J. Biomol. NMR 13 289–302 Occurrence Handle10.1023/A:1008392405740

    Article  Google Scholar 

  • P.R. Costa B.Q. Sun R.G. Griffin (1997) J. Am. Chem. Soc. 119 10821–10830 Occurrence Handle10.1021/ja964313z

    Article  Google Scholar 

  • T.A. Cross S.J. Opella (1994) Curr. Opin. Struct. Biol. 4 574–581 Occurrence Handle10.1016/S0959-440X(94)90220-8

    Article  Google Scholar 

  • T.A. Cross J.R. Quine (2000) Concepts Magn. Reson. 12 55–70 Occurrence Handle10.1002/(SICI)1099-0534(2000)12:2<55::AID-CMR1>3.0.CO;2-K

    Article  Google Scholar 

  • T.A. Cross A. Arseniev B.A. Cornell J.H. Davis J.A. Killian L.K. Nicholson F. Separovic B. A. Wallace (1999) Nat. Struct. Biol. 6 610–611 Occurrence Handle10.1038/10650

    Article  Google Scholar 

  • M.R.R. Planque ParticleDe J.A. Killian (2003) Mol. Membr. Biol. 20 271–284 Occurrence Handle10.1080/09687680310001605352

    Article  Google Scholar 

  • M.R.R. Planque Particlede J.W.P. Boots D.T.S. Rijkers R.M.J. Liskamp D.V. Greathouse J.A. Killian (2002) Biochemistry 41 8396–8404 Occurrence Handle10.1021/bi0257686

    Article  Google Scholar 

  • M. Demura M. Minami T. Asakura T.A. Cross (1998) J. Am. Chem. Soc. 120 1300–1308 Occurrence Handle10.1021/ja972069l

    Article  Google Scholar 

  • Ernst, R.R., Bodenhausen, G. and Wokaun, A. (1987) Principles of Nuclear Magnetic Resonance in One and Two Dimensions, Clarendon Press.

  • R.Q. Fu M. Cotten T.A. Cross (2000) J. Biomol. NMR 16 261–268 Occurrence Handle10.1023/A:1008372508024

    Article  Google Scholar 

  • C.M. Gabrys J. Yang D.P. Weliky (2003) J. Biomol. NMR 26 49–68 Occurrence Handle10.1023/A:1023060102409

    Article  Google Scholar 

  • C. Glaubitz A. Watts (1998) J. Magn. Reson. 130 305–316 Occurrence Handle10.1006/jmre.1997.1344 Occurrence Handle1998JMagR.130..305G

    Article  ADS  Google Scholar 

  • C. Glaubitz I.J. Burnett G. Grobner A.J. Mason A. Watts (1999) J. Am. Chem. Soc. 121 5787–5794 Occurrence Handle10.1021/ja990350p

    Article  Google Scholar 

  • C. Glaubitz G. Grobner A. Watts (2000) Biochim. Biophys. Acta 1463 151–161 Occurrence Handle10.1016/S0005-2736(99)00195-9

    Article  Google Scholar 

  • C.C. Glaubitz M. Eden M. Levitt M.H. (2001) NoChapterTitle S. Kiihne H.J.M. Groot Particlede (Eds) In Focus on Structural Biology Vol. 1: Perspectives on Solid-State NMR in Biology Kluwer Academic Publishers Dordrecht 71–81

    Google Scholar 

  • R.G. Griffin (1998) Nat. Struct. Biol. 5 508–512 Occurrence Handle10.1038/749

    Article  Google Scholar 

  • G. Grobner I.J. Burnett C. Glaubitz G. Choi A.J. Mason A. Watts (2000) Nature 405 810–813 Occurrence Handle10.1038/35015604 Occurrence Handle2000Natur.405..810G

    Article  ADS  Google Scholar 

  • Haeberlen U. 1976 In Advances in Magnetic Resonance High Resolution NMR in Solids: Selective Averaging Waugh, J. S., Academic Press

  • G.S. Harbison H.W. Spiess (1986) Chem. Phys. Lett. 124 128–134 Occurrence Handle10.1016/0009-2614(86)85131-4 Occurrence Handle1986CPL...124..128H

    Article  ADS  Google Scholar 

  • S.R. Hartmann E.L. Hahn (1962) Phys. Rev. 128 2042–2053 Occurrence Handle0113.46404 Occurrence Handle10.1103/PhysRev.128.2042 Occurrence Handle1962PhRv..128.2042H

    Article  MATH  ADS  Google Scholar 

  • J. Herzfeld A.E. Berger (1980) J. Chem. Phys. 73 6021–6030 Occurrence Handle10.1063/1.440136 Occurrence Handle1980JChPh..73.6021H

    Article  ADS  Google Scholar 

  • D.J. Hirsh J. Hammer W.L. Maloy J. Blazyk J. Schaefer (1996) Biochemistry 35 12733–12741 Occurrence Handle10.1021/bi961468a

    Article  Google Scholar 

  • M. Hohwy H.J. Jakobsen M. Eden M.H. Levitt N.C. Nielsen (1998) J. Chem. Phys. 108 2686–2694 Occurrence Handle10.1063/1.475661 Occurrence Handle1998JChPh.108.2686H

    Article  ADS  Google Scholar 

  • M. Hohwy C.M. Rienstra C.P. Jaroniec R.G. Griffin (1999) J. Chem. Phys. 110 7983–7992 Occurrence Handle10.1063/1.478702 Occurrence Handle1999JChPh.110.7983H

    Article  ADS  Google Scholar 

  • W. Hu N.D. Lazo T.A. Cross (1995) Biochemistry 34 14138–14146 Occurrence Handle10.1021/bi00043a019

    Article  Google Scholar 

  • C.E. Hughes S. Luca M. Baldus (2004) Chem. Phys. Lett. 385 435–440 Occurrence Handle10.1016/j.cplett.2004.01.009 Occurrence Handle2004CPL...385..435H

    Article  ADS  Google Scholar 

  • R.R. Ketchem W. Hu T.A. Cross (1993) Science 261 1457–1460 Occurrence Handle10.1126/science.7690158 Occurrence Handle1993Sci...261.1457K

    Article  ADS  Google Scholar 

  • R.R. Ketchem B. Roux T.A. Cross (1997) Structure 5 1655–1669 Occurrence Handle10.1016/S0969-2126(97)00312-2

    Article  Google Scholar 

  • J.A. Killian (1992) Biochim. Biophys. Acta 1113 391–425

    Google Scholar 

  • A. Lange S. Luca M. Baldus (2002) J. Am. Chem. Soc. 124 9704–9705 Occurrence Handle10.1021/ja026691b

    Article  Google Scholar 

  • T.O. Levante M. Baldus B.H. Meier R.R. Ernst (1995) Mol. Phys. 86 1195–1212 Occurrence Handle10.1080/00268979500102671 Occurrence Handle1995MolPh..86.1195L

    Article  ADS  Google Scholar 

  • Levitt M.H. 2002 In Encyclopedia of Nuclear Magnetic Resonance: Supplementary Volume, Symmetry-Based Pulse Sequences in Magic-Angle Spinning Solid-State NMR, Harris R. K., Wiley, 165--196

  • S. Luca D.V. Filippov J.H. Boom Particlevan H. Oschkinat H.J.M. de Groot M. Baldus (2001) J. Biomol. NMR 20 325–331 Occurrence Handle10.1023/A:1011278317489

    Article  Google Scholar 

  • S. Luca H. Heise M. Baldus (2003a) Acc. Chem. Res. 36 858–865 Occurrence Handle10.1021/ar020232y

    Article  Google Scholar 

  • S. Luca J.F. White A.K. Sohal D.V. Filippov J.H. Boom Particlevan R. Grisshammer M. Baldus (2003b) Proc. Natl. Acad. Sci. USA 100 10706–10711 Occurrence Handle10.1073/pnas.1834523100 Occurrence Handle2003PNAS..10010706L

    Article  ADS  Google Scholar 

  • W. Mai W. Hu C. Wang T.A. Cross (1993) Protein Sci. 2 532–542 Occurrence Handle10.1002/pro.5560020405

    Article  Google Scholar 

  • F.M. Marassi (2002) Concepts Magn. Reson. 14 212–224 Occurrence Handle10.1002/cmr.10022

    Article  Google Scholar 

  • F.M. Marassi S.J. Opella (1998) Curr. Opin. Struct. Biol. 8 640–648 Occurrence Handle10.1016/S0959-440X(98)80157-7

    Article  Google Scholar 

  • F.M. Marassi S.J. Opella (2000) J. Magn. Reson. 144 150–155 Occurrence Handle10.1006/jmre.2000.2035 Occurrence Handle2000JMagR.144..150M

    Article  ADS  Google Scholar 

  • L.M. McDowell J. Schaefer (1996) Curr. Opin. Struct. Biol. 6 624–629 Occurrence Handle10.1016/S0959-440X(96)80028-5

    Article  Google Scholar 

  • Mehring, M. (1983) Principles of High Resolution NMR in Solids, Springer.

  • M.F. Mesleh S. Lee G. Veglia D.S. Thiriot F.M. Marassi S.J. Opella (2003) J. Am. Chem. Soc. 125 8928–8935 Occurrence Handle10.1021/ja034211q

    Article  Google Scholar 

  • T.G. Oas C.J. Hartzell F.W. Dahlquist G.P. Drobny (1987) J. Am. Chem. Soc. 109 5962–5966 Occurrence Handle10.1021/ja00254a011

    Article  Google Scholar 

  • S.J. Opella J.S. Waugh (1977) J. Chem. Phys. 66 4919–4924 Occurrence Handle10.1063/1.433831 Occurrence Handle1977JChPh..66.4919O

    Article  ADS  Google Scholar 

  • A. Pines M.G. Gibby J.S. Waugh (1973) J. Chem. Phys. 59 569–590 Occurrence Handle10.1063/1.1680061 Occurrence Handle1973JChPh..59..569P

    Article  ADS  Google Scholar 

  • T. Salditt (2003) Curr. Opin. Struct. Biol. 13 467–478 Occurrence Handle10.1016/S0959-440X(03)00113-1

    Article  Google Scholar 

  • C. Sizun B. Bechinger (2002) J. Am. Chem. Soc. 124 1146–1147 Occurrence Handle10.1021/ja016571o

    Article  Google Scholar 

  • S.A. Smith T.O. Levante B.H. Meier R.R. Ernst (1994) J. Magn. Reson. A106 75–105

    Google Scholar 

  • S.O. Smith K. Aschheim M. Groesbeek (1996) Q. Rev. Biophys. 29 395–449 Occurrence Handle10.1017/S0033583500005898

    Article  Google Scholar 

  • S.O. Smith T. Kawakami W. Liu M. Ziliox S. Aimoto (2001a) J. Mol. Biol. 313 1139–1148 Occurrence Handle10.1006/jmbi.2001.5101

    Article  Google Scholar 

  • S.O. Smith D. Song S. Shekar M. Groesbeek M. Ziliox S. Aimoto (2001b) Biochemistry 40 6553–6558 Occurrence Handle10.1021/bi010357v

    Article  Google Scholar 

  • L. Sonnenberg S. Luca M. Baldus (2004) J. Magn. Reson. 166 100–110 Occurrence Handle10.1016/j.jmr.2003.10.014 Occurrence Handle2004JMagR.166..100S

    Article  ADS  Google Scholar 

  • E. Strandberg S. Morein D.T.S. Rijkers R.M.J. Liskamp P.C.A. Wel Particlevan der J.A. Killian (2002) Biochemistry 41 7190–7198 Occurrence Handle10.1021/bi012047i

    Article  Google Scholar 

  • K. Takegoshi K. Nomura T. Terao (1995) Chem. Phys. Lett. 232 424–428 Occurrence Handle10.1016/0009-2614(94)01399-G Occurrence Handle1995CPL...232..424T

    Article  ADS  Google Scholar 

  • L.K. Thompson (2002) Curr. Opin. Struct. Biol. 12 661–669 Occurrence Handle10.1016/S0959-440X(02)00374-3

    Article  Google Scholar 

  • F. Tian T.A. Cross (1998) J. Magn. Reson. 135 535–540 Occurrence Handle10.1006/jmre.1998.1596 Occurrence Handle1998JMagR.135..535T

    Article  ADS  Google Scholar 

  • P.C.A. Wel Particlevan der E. Strandberg J.A. Killian R.E. Koeppe (2002) Biophys J. 83 1479–1488 Occurrence Handle10.1016/S0006-3495(02)73918-0

    Article  Google Scholar 

  • J. Wang J. Denny C. Tian S. Kim Y. Mo F. Kovacs Z. Song K. Nishimura Z. Gan R. Fu J.R. Quine T.A. Cross (2000) J. Magn. Reson. 144 162–167 Occurrence Handle10.1006/jmre.2000.2037 Occurrence Handle2000JMagR.144..162W

    Article  ADS  Google Scholar 

  • J. Yang D.P. Weliky (2003) Biochemistry 42 11879–11890 Occurrence Handle10.1021/bi0348157

    Article  Google Scholar 

  • A.C. Zeri M.F. Mesleh A.A. Nevzorov S.J. Opella (2003) Proc. Natl. Acad. Sci. USA 100 6458–6463 Occurrence Handle10.1073/pnas.1132059100 Occurrence Handle2003PNAS..100.6458Z

    Article  ADS  Google Scholar 

  • X. Zhao M. Eden M.H. Levitt (2001) Chem. Phys. Lett. 342 353–361 Occurrence Handle10.1016/S0009-2614(01)00593-0 Occurrence Handle2001CPL...342..353Z

    Article  ADS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of NMR-Based Structural Biology, Max-Planck-Institute for Biophysical Chemistry, Am Fassberg 11, 37077, Göttingen, Germany

    O. C. Andronesi, B. Angerstein, S. Luca & M. Baldus

  2. Fachbereich Chemie, Philipps-Universität Marburg, Hans-Meerwein-Strasse, 35032, Marburg, Germany

    J. R. Pfeifer, L. Al-Momani & U. Koert

  3. Department of Biochemistry of Membranes, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    S. Özdirekcan & J. A. Killian

  4. Department of Medicinal Chemistry, Utrecht Institute for Pharmaceutical Sciences, Faculty of Pharmacy, Utrecht University, Sorbonnelaan 16, 3584 CA, Utrecht, The Netherlands

    D. T. S. Rijkers

Authors
  1. O. C. Andronesi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. R. Pfeifer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Al-Momani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Özdirekcan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. T. S. Rijkers
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. B. Angerstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S. Luca
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. U. Koert
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. J. A. Killian
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Baldus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Baldus.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andronesi, O.C., Pfeifer, J.R., Al-Momani, L. et al. Probing membrane protein orientation and structure using fast magic-angle-spinning solid-state NMR. J Biomol NMR 30, 253–265 (2004). https://doi.org/10.1007/s10858-004-3452-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10858-004-3452-3

Keywords

Search

Navigation