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Developing DNP/Solid-State NMR Spectroscopy of Oriented Membranes

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Abstract

Dynamic nuclear polarization (DNP)/solid-state nuclear magnetic resonance (NMR) spectroscopy bears great potential for the investigation of membrane-associated polypeptides which can often be produced only in small amounts and which need to be ‘diluted’ in lipid bilayer environments to adopt or maintain their functional structure. Here we present investigations using biradicals, such as TOTAPOL and bTbK, for solid-state NMR signal enhancement using DNP in the context of lipid membranes. By transferring polarization from electron to nuclear spins using microwave irradiation signal enhancement factors of up to 13 are obtained with TOTAPOL and up to 17 with bTbK. The possible reasons why these factors are below those obtained in glassy samples of bulk solvents (40–60 under similar conditions) are evaluated and discussed. In order to further ameliorate the enhancement factors the physico-chemical characteristics of TEMPOL, TOTAPOL, bTbK, and bCTbK, such as their partitioning between hydrophilic and hydrophobic solvents or their stability under different environmental conditions are presented. Finally, having provided proof-of-concept that DNP/solid-state NMR measurements can be performed with oriented membrane samples work in progress is presented on the development of a flat-coil probe for DNP/solid-state NMR experiments on oriented membranes.

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References

  1. E. Wallin, G. von Heijne, Protein Sci. 7, 1029–1038 (1998)

    Article  Google Scholar 

  2. D. Boyd, C. Schierle, J. Beckwith, Protein Sci. 7, 201–205 (1998)

    Article  Google Scholar 

  3. B.L. Wu, E.Y.T. Chien, C.D. Mol, G. Fenalti, W. Liu, V. Katritch, R. Abagyan, A. Brooun, P. Wells, F.C. Bi, D.J. Hamel, P. Kuhn, T.M. Handel, V. Cherezov, R.C. Stevens, Science 330, 1066–1071 (2010)

    Article  ADS  Google Scholar 

  4. D. Wacker, G. Fenalti, M.A. Brown, V. Katritch, R. Abagyan, V. Cherezov, R.C. Stevens, J. Am. Chem. Soc. 132, 11443–11445 (2010)

    Article  Google Scholar 

  5. A. Bockmann, Angew. Chem. Int. Ed. Engl. 47, 6110–6113 (2008)

    Article  Google Scholar 

  6. M. Renault, M.P. Bos, J. Tommassen, M. Baldus, J. Am. Chem. Soc. 133, 4175–4177 (2011)

    Article  Google Scholar 

  7. T. Jacso, W.T. Franks, H. Rose, U. Fink, J. Broecker, S. Keller, H. Oschkinat, B. Reif, Angew. Chem. Int. Ed. Engl. 51, 432–435 (2011)

    Article  Google Scholar 

  8. D.E. Warschawski, A.A. Arnold, M. Beaugrand, A. Gravel, E. Chartrand, I. Marcotte, Biochim. Biophys. Acta 1808, 1957–1974 (2011)

    Article  Google Scholar 

  9. J.M. Resende, C. Mendonca Moraes, V.H.D.O. Munhoz, C. Aisenbrey, R.M. Verly, P. Bertani, A. Cesar, D. Pilo-Veloso, B. Bechinger, Proc. Natl. Acad. Sci. USA. 106, 16639–16644 (2009)

    Article  Google Scholar 

  10. S.D. Cady, K. Schmidt-Rohr, J. Wang, C.S. Soto, W.F. Degrado, M. Hong, Nature 463, 689–692 (2010)

    Article  ADS  Google Scholar 

  11. S. Tapaneeyakorn, A.D. Goddard, J. Oates, C.L. Willis, A. Watts, Biochim. Biophys. Acta 1808, 1462–1475 (2011)

    Article  Google Scholar 

  12. R. Fu, E.D. Gordon, D.J. Hibbard, M. Cotten, J. Am. Chem. Soc. 131, 10830–10831 (2009)

    Article  Google Scholar 

  13. E. Salnikov, B. Bechinger, Biophys. J. 100, 1473–1480 (2011)

    Article  Google Scholar 

  14. M. Sharma, M. Yi, H. Dong, H. Qin, E. Peterson, D.D. Busath, H.X. Zhou, T.A. Cross, Science 330, 509–512 (2010)

    Article  ADS  Google Scholar 

  15. R. Verardi, L. Shi, N.J. Traaseth, N. Walsh, G. Veglia, Proc. Natl. Acad. Sci. USA. 108, 9101–9106 (2011)

    Article  ADS  Google Scholar 

  16. A. Ramamoorthy, D.K. Lee, T. Narasimhaswamy, R.P.R. Nanga, Biochim. Biophys. Acta 1798, 223–227 (2010)

    Article  Google Scholar 

  17. S.D. Cady, C. Goodman, C.D. Tatko, W.F. DeGrado, M. Hong, J. Am. Chem. Soc. 129, 5719–5729 (2007)

    Article  Google Scholar 

  18. J. Hirschinger, J. Raya, B. Perrone, B. Bechinger, Chem. Phys. Lett. 508, 155–164 (2011)

    Article  ADS  Google Scholar 

  19. B. Bechinger, J.M. Resende, C. Aisenbrey, Biophys. Chem. 153, 115–125 (2011)

    Article  Google Scholar 

  20. T.A. Cross, Method Enzymol. 289, 672–696 (1997)

    Article  Google Scholar 

  21. J.H. Prestegard, C.M. Bougault, A.I. Kishore, Chem. Rev. 104, 3519–3540 (2004)

    Article  Google Scholar 

  22. C. Aisenbrey, M. Cusan, S. Lambotte, P. Jasperse, J. Georgescu, U. Harzer, B. Bechinger, Chem. Biol. Chem. 9, 944–951 (2008)

    Google Scholar 

  23. T. Prisner, W. Köckenberger, Dynamic Nuclear Polarization: New Experimental and Methodology Approaches and Applications in Physics, Chemistry, Biology and Medicine (Springer, Wien, 2008)

    Google Scholar 

  24. A.B. Barnes, B. Corzilius, M.L. Mak-Jurkauskas, L.B. Andreas, V.S. Bajaj, Y. Matsuki, M.L. Belenky, J. Lugtenburg, J.R. Sirigiri, R.J. Temkin, J. Herzfeld, R.G. Griffin, Phys. Chem. Chem. Phys. 12, 5861–5867 (2010)

    Article  Google Scholar 

  25. V.S. Bajaj, M.L. Mak-Jurkauskas, M. Belenky, J. Herzfeld, R.G. Griffin, J. Magn. Reson. 202, 9–13 (2010)

    Article  ADS  Google Scholar 

  26. L.R. Becerra, G.J. Gerfen, R.J. Temkin, D.J. Singel, R.G. Griffin, Phys. Rev. Lett. 71, 3561–3564 (1993)

    Article  ADS  Google Scholar 

  27. D.A. Hall, D.C. Maus, G.J. Gerfen, S.J. Inati, L.R. Becerra, F.W. Dahlquist, R.G. Griffin, Science 276, 930–932 (1997)

    Article  Google Scholar 

  28. T. Maly, G.T. Debelouchina, V.S. Bajaj, K.N. Hu, C.G. Joo, M.L. Mak-Jurkauskas, J.R. Sirigiri, P.C. Van Der Wel, J. Herzfeld, R.J. Temkin, R.G. Griffin, J. Chem. Phys. 128, 052211 (2008)

    Article  ADS  Google Scholar 

  29. U. Akbey, W.T. Franks, A. Linden, S. Lange, R.G. Griffin, B.J. van Rossum, H. Oschkinat, Angew. Chem. Int. Ed. Engl. 49, 7803–7806 (2010)

    Article  Google Scholar 

  30. M.J. Bayro, G.T. Debelouchina, M.T. Eddy, N.R. Birkett, C.E. MacPhee, M. Rosay, W.E. Maas, C.M. Dobson, R.G. Griffin, J. Am. Chem. Soc. 133, 13967–13974 (2011)

    Article  Google Scholar 

  31. L. Reggie, J.J. Lopez, I. Collinson, C. Glaubitz, M. Lorch, J. Am. Chem. Soc. 133, 19084–19086 (2011)

    Article  Google Scholar 

  32. A.H. Linden, S. Lange, W.T. Franks, U. Akbey, E. Specker, B.J. van Rossum, H. Oschkinat, J. Am. Chem. Soc. 133, 19266–19269 (2011)

    Article  Google Scholar 

  33. M. Rosay, A.C. Zeri, N.S. Astrof, S.J. Opella, J. Herzfeld, R.G. Griffin, J. Am. Chem. Soc. 123, 1010–1011 (2001)

    Article  Google Scholar 

  34. E. Salnikov, M. Rosay, S. Pawsey, O. Ouari, P. Tordo, B. Bechinger, J. Am. Chem. Soc. 132, 5940–5941 (2010)

    Article  Google Scholar 

  35. Y. Matsuki, T. Maly, O. Ouari, H. Karoui, M.F. Le, E. Rizzato, S. Lyubenova, J. Herzfeld, T. Prisner, P. Tordo, R.G. Griffin, Angew. Chem. Int. Ed. Engl. 48, 4996–5000 (2009)

    Article  Google Scholar 

  36. D.K. Lee, B.S. Kwon, A. Ramamoorthy, Langmuir 24, 13598–13604 (2008)

    Article  Google Scholar 

  37. E.S. Salnikov, M. De Zotti, F. Formaggio, X. Li, C. Toniolo, J.D. O’Neil, J. Raap, S.A. Dzuba, B. Bechinger, J. Phys. Chem. B 113, 3034–3042 (2009)

    Article  Google Scholar 

  38. M. Rosay, L. Tometich, S. Pawsey, R. Bader, R. Schauwecker, M. Blank, P.M. Borchard, S.R. Cauffman, K.L. Felch, R.T. Weber, R.J. Temkin, R.G. Griffin, W.E. Maas, Phys. Chem. Chem. Phys. 12, 5850–5860 (2010)

    Article  Google Scholar 

  39. K.R. Thurber, R. Tycko, J. Magn. Reson. 195, 179–186 (2008)

    Article  ADS  Google Scholar 

  40. C. Ysacco, E. Rizzato, M.A. Virolleaud, H. Karoui, A. Rockenbauer, F. Le Moigne, D. Siri, O. Ouari, R.G. Griffin, P. Tordo, Phys. Chem. Chem. Phys. 12, 5841–5845 (2010)

    Article  Google Scholar 

  41. A. Zagdoun, G. Casano, O. Ouari, G. Lapadula, A.J. Rossini, M. Lelli, M. Baffert, D. Gajan, L. Veyre, W.E. Maas, M.M. Rosay, R.T. Weber, C. Thieuleux, C. Coperet, A. Lesage, P. Tordo, L. Emsley, J. Am. Chem. Soc. 134, 2284–2291 (2012)

    Article  Google Scholar 

  42. C. Sizun, B. Bechinger, J. Am. Chem. Soc. 124, 1146–1147 (2002)

    Article  Google Scholar 

  43. C. Glaubitz, A. Watts, J. Magn. Reson. 130, 305–316 (1998)

    Article  ADS  Google Scholar 

  44. C. Aisenbrey, B. Bechinger, J. Am. Chem. Soc. 126, 16676–16683 (2004)

    Article  Google Scholar 

  45. B. Bechinger, C. Sizun, Concepts Magn. Reson. 18A, 130–145 (2003)

    Article  Google Scholar 

  46. P.C. van der Wel, J.R. Lewandowski, R.G. Griffin, Biochemistry-Us 49, 9457–9469 (2010)

    Article  Google Scholar 

  47. K.N. Hu, C. Song, H.H. Yu, T.M. Swager, R.G. Griffin, J. Chem. Phys. 128, 052302 (2008)

    Article  ADS  Google Scholar 

  48. K.R. Thurber, W.M. Yau, R. Tycko, J. Magn. Reson. 204, 303–313 (2010)

    Article  ADS  Google Scholar 

  49. C. Aisenbrey, P. Bertani, B. Bechinger, Solid-state NMR investigations of membrane-associated antimicrobial peptides, in Antimicrobial Peptides Humana Press, ed. by A. Guiliani, A.C. Rinaldi (Springer, New York, 2010), pp. 209–233

    Google Scholar 

  50. M. Rosay, J.C. Lansing, K.C. Haddad, W.W. Bachovchin, J. Herzfeld, R.J. Temkin, R.G. Griffin, J. Am. Chem. Soc. 125, 13626–13627 (2003)

    Article  Google Scholar 

  51. P.C. Van Der Wel, K.N. Hu, J. Lewandowski, R.G. Griffin, J. Am. Chem. Soc. 128, 10840–10846 (2006)

    Article  Google Scholar 

  52. U. Akbey, S. Lange, W. Trent Franks, R. Linser, K. Rehbein, A. Diehl, B.J. van Rossum, B. Reif, H. Oschkinat, J. Biomol. NMR 46, 67–73 (2010)

    Article  Google Scholar 

  53. E.G. Finer, J. Chem. Soc., Faraday Trans. II(69), 1590–1600 (1973)

    Google Scholar 

  54. C. Mendonca de Moraes, B. Bechinger, Magn. Reson. Chem. 42, 155–161 (2004)

    Article  Google Scholar 

  55. K.N. Hu, G.T. Debelouchina, A.A. Smith, R.G. Griffin, J. Chem. Phys. 134, 125105 (2011)

    Article  ADS  Google Scholar 

  56. K. Yamamoto, J.D. Xu, K.E. Kawulka, J.C. Vederas, A. Ramamoorthy, J. Am. Chem. Soc. 132, 6929 (2010)

    Google Scholar 

  57. K. Yamamoto, S. Vivekanandan, A. Ramamoorthy, J. Phys. Chem. B 115, 12448–12455 (2011)

    Article  Google Scholar 

  58. A. Ramamoorthy, Y. Wei, D. Lee, Annu. Rep. NMR Spectrosc. 52, 1–52 (2004)

    Article  Google Scholar 

  59. C.S. Song, K.N. Hu, C.G. Joo, T.M. Swager, R.G. Griffin, J. Am. Chem. Soc. 128, 11385–11390 (2006)

    Article  Google Scholar 

  60. Y. Matsuki, T. Maly, O. Ouari, S. Lyubenova, J. Herzfeld, T. Prisner, P. Tordo, R.G. Griffin, Angewandte Chemie 48, 4996–5000 (2009)

    Google Scholar 

  61. M. Bak, J.T. Rasmussen, N.C. Nielsen, J. Magn. Reson. 147, 296–330 (2000)

    Article  ADS  Google Scholar 

  62. E.J. Dufourc, C. Mayer, J. Stohrer, G. Althoff, G. Kothe, Biophys. J. 61, 42–57 (1992)

    Article  Google Scholar 

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Acknowledgments

We are grateful to Ralph Weber from Bruker BioSpin for acquiring EPR spectra and the EPR service of the University of Strasbourg for access to their spectrometers. The discussions with Fabien Aussenac and Werner Maas have provided valuable insight and helped us to advance with this work. We acknowledge the Bio-NMR European Commission’s Program 7 (FP7), project number 261863, BIO-NMR 00060 for access to DNP/solid-state NMR instrumentation in Berlin. The financial support by the CNRS (grant to support H.S.), the RTRA Foundation International Center for Frontier Research in Chemistry, Strasbourg and the University of Strasbourg (PPF RMN) is gratefully acknowledged. The Bechinger laboratory is grateful to the Institute of Supramolecular Chemistry for hosting the team.

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Author notes

  1. Eline Koers

    Present address: Bijvoet Center for Biomolecular Research, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

Authors and Affiliations

  1. Institut de Chimie, UMR7177, CNRS, Université de Strasbourg, 4, rue Blaise Pascal, 67070, Strasbourg, France

    Evgeniy S. Salnikov, Hiba Sarrouj & Burkhard Bechinger

  2. Faculté des Sciences, Institut de Chimie Radicalaire, UMR 7273, Aix-Marseille University, 13397, Marseille Cedex 20, France

    Olivier Ouari & Paul Tordo

  3. Bruker BioSpin Corporation, 15 Fortune Drive, Billerica, MA, 01821, USA

    Eline Koers, Melanie Rosay & Shane Pawsey

  4. Bruker BioSpin, Silberstreifen, 76287, Rheinstetten, Germany

    Hiba Sarrouj, Christian Reiter, Priyanga Bandara & Frank Engelke

  5. Leibniz-Institut für Molekulare Pharmakologie, Robert-Rössle-Straße 10, 13125, Berlin, Germany

    Trent Franks & Hartmut Oschkinat

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  1. Evgeniy S. Salnikov
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Correspondence to Melanie Rosay, Frank Engelke or Burkhard Bechinger.

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Salnikov, E.S., Ouari, O., Koers, E. et al. Developing DNP/Solid-State NMR Spectroscopy of Oriented Membranes. Appl Magn Reson 43, 91–106 (2012). https://doi.org/10.1007/s00723-012-0338-5

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