Journal of Biomolecular NMR

, Volume 30, Issue 3, pp 253–265 | Cite as

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

  • O. C. Andronesi
  • J. R. Pfeifer
  • L. Al-Momani
  • S. Özdirekcan
  • D. T. S. Rijkers
  • B. Angerstein
  • S. Luca
  • U. Koert
  • J. A. Killian
  • M. Baldus


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].


MAS membrane proteins NMR solid-state structure determination 



solid state NMR


Magic Angle Spinning


Radio Frequency


Chemical Shift Anisotropy


Cross Polarization


Adiabatic-Passage Hartmann-Hahn Cross-Polarization


Spectrally Induced Filtering In Combination with Cross-Polarization


Two Pulse Phase Modulation


Time Proportional Phase Incrementation


Double Quantum


Single Quantum


Permutationally Offset Stabilized C7


Supercycled POST-C5


Spin Diffusion


Average Hamiltonian Theory






Trp-flanked poly(alanine-leucine) peptides








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Supplementary material

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  1. Andrew, E.R., Bradbury, A., Eades, R.G 1958Nature1821659CrossRefADSGoogle Scholar
  2. Arndt, H.D., Vescovi, A., Schrey, A., Pfeifer, J.R., Koert, U. 2002Tetrahedron5827892801CrossRefGoogle Scholar
  3. Auge, S., Mazarguil, H., Tropis, M., Milon, A. 1997J. Magn. Reson.124455458CrossRefADSGoogle Scholar
  4. Baldus, M. 2002Prog. NMR Spectrosc.41147CrossRefGoogle Scholar
  5. Baldus, M., Geurts, D.G., Hediger, S., Meier, B.H. 1996J. Magn. Reson.A118140144Google Scholar
  6. Baldus, M., Levante, T.O., Meier, B.H. 1994aZ. Naturforsch. Section a-a J. Phys. Sci.498088Google Scholar
  7. Baldus, M., Tomaselli, M., Meier, B.H., Ernst, R.R. 1994bChem. Phys. Lett.230329336CrossRefADSGoogle Scholar
  8. Baldus, M., Petkova, A.T., Herzfeld, J., Griffin, R.G. 1998Mol. Phys.9511971207ADSGoogle Scholar
  9. Bax, A., Freeman, R., Kempsell, S.P. 1980J. Am. Chem. Soc.10248494851CrossRefGoogle Scholar
  10. Bechinger, B., Kinder, R., Helmle, M., Vogt, T.C.B., Harzer, U., Schinzel , S. 1999Biopolymers51174190CrossRefGoogle Scholar
  11. Bennett, A.E., Rienstra, C.M., Auger, M., Lakshmi, K.V., Griffin, R.G. 1995J. Chem. Phys.10369516958CrossRefADSGoogle Scholar
  12. Bloembergen, N. 1949Physica15386426CrossRefADSGoogle Scholar
  13. Bockmann, A., Lange, A., Galinier, A., Luca, S., Giraud, N., Juy, M., Heise, H., Montserret, R., Penin, F., Baldus, M. 2003J. Biomol. NMR27323339CrossRefGoogle Scholar
  14. Bodner, M.L., Gabrys, C.M., Parkanzky, P.D., Yang, J., Duskin, C.A., Weliky, D.P. 2004Magn. Reson. Chem.42187194CrossRefGoogle Scholar
  15. Brink, D.M. and Satchler, G.R. (1961) Angular Momentum, Oxford University Press.Google Scholar
  16. Carravetta, M., Eden, M., Zhao, X., Brinkmann, A., Levitt, M.H. 2000Chem. Phys. Lett.321205215CrossRefADSGoogle Scholar
  17. Cheng, V.B., Suzukawa, H.H., Wolfsber, M. 1973J. Chem. Phys.5939923999CrossRefMathSciNetADSGoogle Scholar
  18. Cornilescu, G., Delaglio, F., Bax, A. 1999J. Biomol. NMR13289302CrossRefGoogle Scholar
  19. Costa, P.R., Sun, B.Q., Griffin, R.G. 1997J. Am. Chem. Soc.1191082110830CrossRefGoogle Scholar
  20. Cross, T.A., Opella, S.J. 1994Curr. Opin. Struct. Biol.4574581CrossRefGoogle Scholar
  21. Cross, T.A., Quine, J.R. 2000Concepts Magn. Reson.125570CrossRefGoogle Scholar
  22. Cross, T.A., Arseniev, A., Cornell, B.A., Davis, J.H., Killian, J.A., Nicholson, L.K., Separovic, F., Wallace, B. A. 1999Nat. Struct. Biol.6610611CrossRefGoogle Scholar
  23. Planque, M.R.R., Killian, J.A. 2003Mol. Membr. Biol.20271284CrossRefGoogle Scholar
  24. Planque, M.R.R., Boots, J.W.P., Rijkers, D.T.S., Liskamp, R.M.J., Greathouse, D.V., Killian, J.A. 2002Biochemistry4183968404CrossRefGoogle Scholar
  25. Demura, M., Minami, M., Asakura, T., Cross, T.A. 1998J. Am. Chem. Soc.12013001308CrossRefGoogle Scholar
  26. Ernst, R.R., Bodenhausen, G. and Wokaun, A. (1987) Principles of Nuclear Magnetic Resonance in One and Two Dimensions, Clarendon Press.Google Scholar
  27. Fu, R.Q., Cotten, M., Cross, T.A. 2000J. Biomol. NMR16261268CrossRefGoogle Scholar
  28. Gabrys, C.M., Yang, J., Weliky, D.P. 2003J. Biomol. NMR264968CrossRefGoogle Scholar
  29. Glaubitz, C., Watts, A. 1998J. Magn. Reson.130305316CrossRefADSGoogle Scholar
  30. Glaubitz, C., Burnett, I.J., Grobner, G., Mason, A.J., Watts, A. 1999J. Am. Chem. Soc.12157875794CrossRefGoogle Scholar
  31. Glaubitz, C., Grobner, G., Watts, A. 2000Biochim. Biophys. Acta1463151161CrossRefGoogle Scholar
  32. Glaubitz, C.C., Eden, M., Levitt, M., M.H.,  2001Kiihne, S.Groot, H.J.M. eds. In Focus on Structural Biology Vol. 1: Perspectives on Solid-State NMR in BiologyKluwer Academic PublishersDordrecht7181Google Scholar
  33. Griffin, R.G. 1998Nat. Struct. Biol.5508512CrossRefGoogle Scholar
  34. Grobner, G., Burnett, I.J., Glaubitz, C., Choi, G., Mason , A.J., Watts, A. 2000Nature405810813CrossRefADSGoogle Scholar
  35. Haeberlen U. 1976 In Advances in Magnetic Resonance High Resolution NMR in Solids: Selective Averaging Waugh, J. S., Academic PressGoogle Scholar
  36. Harbison, G.S., Spiess, H.W. 1986Chem. Phys. Lett.124128134CrossRefADSGoogle Scholar
  37. Hartmann, S.R., Hahn, E.L. 1962Phys. Rev.12820422053MATHCrossRefADSGoogle Scholar
  38. Herzfeld, J., Berger, A.E. 1980J. Chem. Phys.7360216030CrossRefADSGoogle Scholar
  39. Hirsh, D.J., Hammer, J., Maloy, W.L., Blazyk, J., Schaefer, J. 1996Biochemistry351273312741CrossRefGoogle Scholar
  40. Hohwy, M., Jakobsen, H.J., Eden, M., Levitt, M.H., Nielsen, N.C. 1998J. Chem. Phys.10826862694CrossRefADSGoogle Scholar
  41. Hohwy, M., Rienstra, C.M., Jaroniec, C.P., Griffin, R.G. 1999J. Chem. Phys.11079837992CrossRefADSGoogle Scholar
  42. Hu, W., Lazo, N.D., Cross, T.A. 1995Biochemistry341413814146CrossRefGoogle Scholar
  43. Hughes, C.E., Luca, S., Baldus, M. 2004Chem. Phys. Lett.385435440CrossRefADSGoogle Scholar
  44. Ketchem, R.R., Hu, W., Cross, T.A. 1993Science26114571460CrossRefADSGoogle Scholar
  45. Ketchem, R.R., Roux, B., Cross, T.A. 1997Structure516551669CrossRefGoogle Scholar
  46. Killian, J.A. 1992Biochim. Biophys. Acta1113391425Google Scholar
  47. Lange, A., Luca, S., Baldus, M. 2002J. Am. Chem. Soc.12497049705CrossRefGoogle Scholar
  48. Levante, T.O., Baldus, M., Meier, B.H., Ernst, R.R. 1995Mol. Phys.8611951212CrossRefADSGoogle Scholar
  49. 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--196Google Scholar
  50. Luca, S., Filippov, D.V., Boom, J.H., Oschkinat, H., de Groot, H.J.M., Baldus, M. 2001J. Biomol. NMR20325331CrossRefGoogle Scholar
  51. Luca, S., Heise, H., Baldus, M. 2003aAcc. Chem. Res.36858865CrossRefGoogle Scholar
  52. Luca, S., White, J.F., Sohal, A.K., Filippov, D.V., Boom, J.H., Grisshammer, R., Baldus, M. 2003bProc. Natl. Acad. Sci. USA1001070610711CrossRefADSGoogle Scholar
  53. Mai, W., Hu, W., Wang, C., Cross, T.A. 1993Protein Sci.2532542CrossRefGoogle Scholar
  54. Marassi, F.M. 2002Concepts Magn. Reson.14212224CrossRefGoogle Scholar
  55. Marassi, F.M., Opella, S.J. 1998Curr. Opin. Struct. Biol.8640648CrossRefGoogle Scholar
  56. Marassi, F.M., Opella, S.J. 2000J. Magn. Reson.144150155CrossRefADSGoogle Scholar
  57. McDowell, L.M., Schaefer, J. 1996Curr. Opin. Struct. Biol.6624629CrossRefGoogle Scholar
  58. Mehring, M. (1983) Principles of High Resolution NMR in Solids, Springer.Google Scholar
  59. Mesleh, M.F., Lee, S., Veglia, G., Thiriot, D.S., Marassi, F.M., Opella, S.J. 2003J. Am. Chem. Soc.12589288935CrossRefGoogle Scholar
  60. Oas, T.G., Hartzell, C.J., Dahlquist, F.W., Drobny, G.P. 1987J. Am. Chem. Soc.10959625966CrossRefGoogle Scholar
  61. Opella, S.J., Waugh, J.S. 1977J. Chem. Phys.6649194924CrossRefADSGoogle Scholar
  62. Pines, A., Gibby, M.G., Waugh, J.S. 1973J. Chem. Phys.59569590CrossRefADSGoogle Scholar
  63. Salditt, T. 2003Curr. Opin. Struct. Biol.13467478CrossRefGoogle Scholar
  64. Sizun, C., Bechinger, B. 2002J. Am. Chem. Soc.12411461147CrossRefGoogle Scholar
  65. Smith, S.A., Levante, T.O., Meier, B.H., Ernst, R.R. 1994J. Magn. Reson.A10675105Google Scholar
  66. Smith, S.O., Aschheim, K., Groesbeek, M. 1996Q. Rev. Biophys.29395449CrossRefGoogle Scholar
  67. Smith, S.O., Kawakami, T., Liu, W., Ziliox, M., Aimoto, S. 2001aJ. Mol. Biol.31311391148CrossRefGoogle Scholar
  68. Smith, S.O., Song, D., Shekar, S., Groesbeek, M., Ziliox, M., Aimoto, S. 2001bBiochemistry4065536558CrossRefGoogle Scholar
  69. Sonnenberg, L., Luca, S., Baldus, M. 2004J. Magn. Reson.166100110CrossRefADSGoogle Scholar
  70. Strandberg, E., Morein, S., Rijkers, D.T.S., Liskamp, R.M.J., Wel, P.C.A., Killian, J.A. 2002Biochemistry4171907198CrossRefGoogle Scholar
  71. Takegoshi, K., Nomura, K., Terao, T. 1995Chem. Phys. Lett.232424428CrossRefADSGoogle Scholar
  72. Thompson, L.K. 2002Curr. Opin. Struct. Biol.12661669CrossRefGoogle Scholar
  73. Tian, F., Cross, T.A. 1998J. Magn. Reson.135535540CrossRefADSGoogle Scholar
  74. Wel, P.C.A., Strandberg, E., Killian, J.A., Koeppe, R.E. 2002Biophys J.8314791488CrossRefGoogle Scholar
  75. Wang, J., Denny, J., Tian, C., Kim, S., Mo, Y., Kovacs, F., Song, Z., Nishimura, K., Gan, Z., Fu, R., Quine, J.R., Cross, T.A. 2000J. Magn. Reson.144162167CrossRefADSGoogle Scholar
  76. Yang, J., Weliky, D.P. 2003Biochemistry421187911890CrossRefGoogle Scholar
  77. Zeri, A.C., Mesleh, M.F., Nevzorov, A.A., Opella, S.J. 2003Proc. Natl. Acad. Sci. USA10064586463CrossRefADSGoogle Scholar
  78. Zhao, X., Eden, M., Levitt, M.H. 2001Chem. Phys. Lett.342353361CrossRefADSGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • O. C. Andronesi
    • 1
  • J. R. Pfeifer
    • 2
  • L. Al-Momani
    • 2
  • S. Özdirekcan
    • 3
  • D. T. S. Rijkers
    • 4
  • B. Angerstein
    • 1
  • S. Luca
    • 1
  • U. Koert
    • 2
  • J. A. Killian
    • 3
  • M. Baldus
    • 1
  1. 1.Department of NMR-Based Structural BiologyMax-Planck-Institute for Biophysical ChemistryGöttingenGermany
  2. 2.Fachbereich ChemiePhilipps-Universität MarburgMarburgGermany
  3. 3.Department of Biochemistry of MembranesUtrecht UniversityUtrechtThe Netherlands
  4. 4.Department of Medicinal Chemistry, Utrecht Institute for Pharmaceutical Sciences, Faculty of PharmacyUtrecht UniversityUtrechtThe Netherlands

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