Advertisement

Applied Magnetic Resonance

, Volume 45, Issue 9, pp 841–857 | Cite as

NMR Crystallography as a Novel Tool for the Understanding of the Mode of Action of Enzymes: SOD a Case Study

  • Daniel Tietze
  • Stephan Voigt
  • Doreen Mollenhauer
  • Gerd BuntkowskyEmail author
Article

Abstract

Nuclear magnetic resonance (NMR) crystallography is an approach for revealing molecular and supramolecular structures and molecular packing for systems where standard X-ray crystallography gives no results. It combines solid-state NMR techniques with chemical models and/or molecular dynamics and/or quantum chemical calculations. These techniques are often supported by other structure characterization methods. In the present review, recent results on the application of NMR crystallography for the investigation of the mode of action of superoxide dismutases are discussed. Studies of substrate–inhibitor complexes of human manganese and Streptomyces nickel superoxide dismutase are presented, which are chemical models of the transient enzyme–substrate complex. The review is completed by new, previously unpublished results, calculating an NMR structure of NiSOD model peptide-bound cyanide based on experimental restraints measured by us and derived from the literature and extended DFT calculations.

Keywords

Nuclear Magnetic Resonance Nuclear Magnetic Resonance Spectroscopy Nuclear Magnetic Resonance Structure Continuum Solvation Model Cyanide Anion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Financial support by the Deutsche Forschungsgemeinschaft DFG under contract Bu 911-21-1 is gratefully acknowledged.

References

  1. 1.
    J.K. Williams, D. Tietze, J. Wang, Y. Wu, W.F. Degrado, M. Hong, J. Am. Chem. Soc. 135, 9885–9897 (2013)CrossRefGoogle Scholar
  2. 2.
    F.H. Hu, W.B. Luo, M. Hong, Science 330, 505–508 (2010)CrossRefADSGoogle Scholar
  3. 3.
    D.M. Grant, F. Liu, R.J. Iuliucci, C. Phung, J.C. Facelli, D. Alderman, Acta Crystallogr. B 51, 540–546 (1995)CrossRefGoogle Scholar
  4. 4.
    I. Sack, A. Goldbourt, S. Vega, G. Buntkowsky, J. Magn. Reson. 138, 154 (1999)CrossRefGoogle Scholar
  5. 5.
    I. Sack, S. Macholl, F. Wehrmann, J. Albrecht, H.H. Limbach, F. Fillaux, M.H. Baron, G. Buntkowsky, Appl. Magn. Reson. 17, 413 (1999)CrossRefGoogle Scholar
  6. 6.
    R.K. Harris, Analyst 131, 351–373 (2006)CrossRefADSGoogle Scholar
  7. 7.
    B. Elena, G. Pintacuda, N. Mifsud, L. Emsley, J. Am. Chem. Soc. 128, 9555–9560 (2006)CrossRefGoogle Scholar
  8. 8.
    S. M. Reutzel-Edens, in Engineering of Crystalline Materials Properties, Springer, pp. 351–374 (2008)Google Scholar
  9. 9.
    M. J. Potrzebowski, Crystallography and NMR: Applications to Organic and Pharmaceutical Chemistry, eMag Res (2008)Google Scholar
  10. 10.
    R. K. Harris, Crystallography and NMR: an Overview, eMag Res (2008)Google Scholar
  11. 11.
    F. Taulelle, Fundamental Principles of NMR Crystallography, Wiley Online Library (2009)Google Scholar
  12. 12.
    S. Macholl, D. Tietze, G. Buntkowsky, Cryst. Eng. Comm. 15, 8627–8638 (2013)CrossRefGoogle Scholar
  13. 13.
    T.G. Oas, R.G. Griffin, M.H. Levitt, J. Chem. Phys. 89, 692 (1988)CrossRefADSGoogle Scholar
  14. 14.
    T. Gullion, J. Schaefer, J. Magn. Reson. 81, 196 (1989)ADSGoogle Scholar
  15. 15.
    T. Gullion and J. Schaefer, W.S. Warren (ed), Adv. in Magn. and Opt. Res. 13, 57 (1989)Google Scholar
  16. 16.
    M. Levitt, D.P. Raleigh, F. Creuzet, R.G. Griffin, J. Chem. Phys. 92, 6347 (1990)CrossRefADSGoogle Scholar
  17. 17.
    A. Hing, S. Vega, J. Schaefer, J. Magn. Reson. 96, 205 (1992)ADSGoogle Scholar
  18. 18.
    A.E. Bennett, J.H. Ok, R.G. Griffin, S. Vega, J. Chem. Phys. 96, 8642 (1992)Google Scholar
  19. 19.
    A.E. Bennett, R.G. Griffin, S. Vega, Springer Series NMR 33, 1 (1994)Google Scholar
  20. 20.
    G. Cornilescu, F. Delaglio, A. Bax, J. Biomol. NMR 13, 289–302 (1999)CrossRefGoogle Scholar
  21. 21.
    S. Macholl, F. Boerner, G. Buntkowsky, Chem. Eur. J. 10, 4808–4816 (2004)CrossRefGoogle Scholar
  22. 22.
    S. Macholl, F. Boerner, G. Buntkowsky, Z. Phys. Chem. 217, 1473–1505 (2003)CrossRefGoogle Scholar
  23. 23.
    S. Macholl, D. Lentz, F. Borner, G. Buntkowsky, Chem. Eur. J. 13, 6139–6149 (2007)Google Scholar
  24. 24.
    L. Seyfarth, J. Seyfarth, B.V. Lotsch, W. Schnick, J. Senker, Phys. Chem. Chem. Phys. 12, 2227–2237 (2010)CrossRefGoogle Scholar
  25. 25.
    M. Schmidt, J.J. Wittmann, R. Kress, D. Schneider, D. Schneider, H.W. Schmidt, Jr Senker, Cryst. Growth Des. 12, 2543–2551 (2012)CrossRefGoogle Scholar
  26. 26.
    E. Wirnhier, M.B. Mesch, J. Senker, W. Schnick, Chem. Eur. J. 19, 2041–2049 (2013)Google Scholar
  27. 27.
    R.K. Harris, R.E. Wasylishen, M.J. Duer, NMR Crystallography (Wiley, New York, 2009)Google Scholar
  28. 28.
    J.A. Ripmeester, R.E. Wasylishen, Cryst. Eng. Comm. 15, 8598 (2013)CrossRefGoogle Scholar
  29. 29.
    T. Gullion, Concept Magn. Reson. 10, 277 (1998)CrossRefGoogle Scholar
  30. 30.
    B.B. Keele Jr, J.M. McCord, I. Fridovich, J. Biol. Chem. 245, 6176–6181 (1970)Google Scholar
  31. 31.
    J.L. Hsu, Y. Hsieh, C. Tu, D. O’Connor, H.S. Nick, D.N. Silverman, J. Biol. Chem. 271, 17687–17691 (1996)CrossRefGoogle Scholar
  32. 32.
    J.M. McCord, J.A. Boyle, E.D. Day Jr., L.J. Rizzolo, M.L. Salin, in Superoxide and Superoxide Dismutases, ed. by A.M. Michelson, J.M. McCord, I. Fridovich (Academic Press, New York, 1977), pp. 129–138Google Scholar
  33. 33.
    I. Fridovich, J. Biol. Chem. 264, 7761–7764 (1989)Google Scholar
  34. 34.
    J.J. Haddad, Cell. Signal. 14, 879–897 (2002)CrossRefGoogle Scholar
  35. 35.
    J.M. Matés, J.M. Segura, C. Pérez-Gómez, R. Rosado, L. Olalla, M. Blanca, F.M. Sánchez-Jiménez, Blood Cells Mol. Dis. 25, 103–109 (1999)CrossRefGoogle Scholar
  36. 36.
    H.-D. Youn, E.-J. Kim, J.-H. Roe, Y.C. Hah, S.-O. Kang, Biochem. J. 318, 889–896 (1996)Google Scholar
  37. 37.
    M. Schmidt, B. Meier, C. Scherk, O. Iakovleva, F. Parak, Prog. Biophys. Mol. Biol. 65, Pa113–Pa113 (1996)Google Scholar
  38. 38.
    M. Schmidt, B. Meier, F. Parak, J. Biol. Inorg. Chem. 1, 532–541 (1996)CrossRefGoogle Scholar
  39. 39.
    A.-F. Miller, D.L. Sorkin, Comments Mol. Cell. Biophys. 9, 1–48 (1997)Google Scholar
  40. 40.
    B. Meier, C. Scherk, M. Schmidt, F. Parak, Biochem. J. 331, 403–407 (1998)Google Scholar
  41. 41.
    D.P. Barondeau, C.J. Kassmann, C.K. Bruns, J.A. Tainer, E.D. Getzoff, Biochemistry 43, 8038–8047 (2004)CrossRefGoogle Scholar
  42. 42.
    P.A. Bryngelson, S.E. Arobo, J.L. Pinkham, D.E. Cabelli, M.J. Maroney, J. Am. Chem. Soc. 126, 460–461 (2004)CrossRefGoogle Scholar
  43. 43.
    S.B. Choudhury, J.W. Lee, G. Davidson, Y. Yim, K. Bose, M.L. Sharma, S. Kang, D.E. Cabelli, M.J. Maroney, Biochemistry 38, 3744–3752 (1999)CrossRefGoogle Scholar
  44. 44.
    D.P. Riley, W.J. Rivers, R.H. Weiss, Anal. Biochem. 196, 344–349 (1991)CrossRefGoogle Scholar
  45. 45.
    J. Shearer, L.M. Long, Inorg. Chem. 45, 2358–2360 (2006)CrossRefGoogle Scholar
  46. 46.
    D. Tietze, S. Voigt, D. Mollenhauer, M. Tischler, D. Imhof, T. Gutmann, L. González, O. Ohlenschlager, H. Breitzke, M. Görlach, G. Buntkowsky, Angew. Chem. Int. Ed. 50, 2946–2950 (2011)CrossRefGoogle Scholar
  47. 47.
    G.E.O. Borgstahl, H.E. Parge, M.J. Hickey, W.F. Beyer, R.A. Hallewell, J.A. Tainer, Cell 71, 107–118 (1992)CrossRefGoogle Scholar
  48. 48.
    R.H. Holm, P. Kennepohl, E.I. Solomon, Chem. Rev. 96, 2239–2314 (1996)CrossRefGoogle Scholar
  49. 49.
    W.G. Han, T. Lovell, L. Noodleman, Inorg. Chem. 41, 205–218 (2002)CrossRefGoogle Scholar
  50. 50.
    A.F. Miller, K. Padmakumar, D.L. Sorkin, A. Karapetian, C.K. Vance, J. Inorg. Biochem. 93, 71–83 (2003)CrossRefGoogle Scholar
  51. 51.
    W.C. Stallings, C. Bull, J.A. Fee, M.S. Lah, M.L. Ludwig, in Molecular Biology of Free Radical Scavenging Systems (Cold Spring Harbor Laboratory Press, Plainview, 1992)Google Scholar
  52. 52.
    A.S. Hearn, M.E. Stroupe, D.E. Cabelli, C.A. Ramilo, J.P. Luba, J.A. Tainer, H.S. Nick, D.S. Silverman, Biochemistry 42, 2781–2789 (2003)CrossRefGoogle Scholar
  53. 53.
    M.S. Lah, M.M. Dixon, K.A. Pattridge, W.C. Stallings, J.A. Fee, M.L. Ludwig, Biochemistry 34, 1646–1660 (1995)CrossRefGoogle Scholar
  54. 54.
    I. Ayala, J.J.P. Perry, J. Szczepanski, M.T. Vala, J.A. Tainer, H.S. Nick, D.N. Silverman, Biophys. J. 89, 4171–4179 (2005)CrossRefGoogle Scholar
  55. 55.
    T. Emmler, I. Ayala, D. Silverman, S. Hafner, A.S. Galstyan, E.W. Knapp, G. Buntkowsky, Solid State Nucl. Magn. Reson. 34, 6–13 (2008)CrossRefGoogle Scholar
  56. 56.
    P. Quint, I. Ayala, S.A. Busby, M.J. Chalmers, P.R. Griffin, J. Rocca, H.S. Nick, D.N. Silverman, Biochemistry 45, 8209–8215 (2006)CrossRefGoogle Scholar
  57. 57.
    I. Bertini, C. Luchinat, NMR of Paramagnetic Molecules in Biological Systems (Benjamin/Cummings Publ. Menlo Park, CA, 1987)Google Scholar
  58. 58.
    S.M. Holl, G.R. Marshall, D.D. Beusen, K. Kociolek, A.S. Redlinski, M.T. Le-plawy, R.A. McKay, S. Vega, J. Schaefer, J. Am. Chem. Soc. 114, 4830 (1992)CrossRefGoogle Scholar
  59. 59.
    L. McDowell, M. Lee, R.A. McKay, K.S. Anderson, J. Schaefer, Biochemistry 35, 3328 (1996)CrossRefGoogle Scholar
  60. 60.
    H.L. van Camp, R.H. Sands, J.A. Fee, Biochim. Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 704, 75–89 (1982)CrossRefGoogle Scholar
  61. 61.
    G. Rotilio, L. Morpurgo, C. Giovagnoli, L. Calabrese, B. Mondovi, Biochemistry 11, 2187–2192 (1972)CrossRefGoogle Scholar
  62. 62.
    J. Han, N.J. Blackburn, T.M. Loehr, Inorg. Chem. 31, 3223–3229 (1992)CrossRefGoogle Scholar
  63. 63.
    K.D. Carugo, A. Battistoni, M.T. Carrì, F. Polticelli, A. Desideri, G. Rotilio, A. Coda, M. Bolognesi, FEBS Lett. 349, 93–98 (1994)CrossRefGoogle Scholar
  64. 64.
    J.A. Tainer, E.D. Getzoff, J.S. Richardson, D.C. Richardson, Nature 306, 284–287 (1983)Google Scholar
  65. 65.
    J.W. Whittaker, M.M. Whittaker, J. Am. Chem. Soc. 113, 5528–5540 (1991)CrossRefGoogle Scholar
  66. 66.
    M. Schmidt, S. Zahn, M. Carella, O. Ohlenschlager, M. Gorlach, E. Kothe, J. Weston, Chem. Bio. Chem. 9, 2135–2146 (2008)CrossRefGoogle Scholar
  67. 67.
    K.P. Neupane, K. Gearty, A. Francis, J. Shearer, J. Am. Chem. Soc. 129, 14605–14618 (2007)CrossRefGoogle Scholar
  68. 68.
    J. Shearer, K.P. Neupane, P.E. Callan, Inorg. Chem. 48, 10560–10571 (2009)CrossRefGoogle Scholar
  69. 69.
    D. Tietze, H. Breitzke, D. Imhof, E. Kothe, J. Weston, G. Buntkowsky, Chem. Eur. J. 15, 517–523 (2009)Google Scholar
  70. 70.
    D. Tietze, M. Tischler, S. Voigt, D. Imhof, O. Ohlenschlager, M. Görlach, G. Buntkowsky, Chem. Eur. J. 16, 7572–7578 (2010)Google Scholar
  71. 71.
    M.-S. Cheung, M.L. Maguire, T.J. Stevens, R.W. Broadhurst, J. Magn. Reson. 202, 223–233 (2010)CrossRefADSGoogle Scholar
  72. 72.
    R.W. Herbst, A. Guce, P.A. Bryngelson, K.A. Higgins, K.C. Ryan, D.E. Cabelli, S.C. Garman, M.J. Maroney, Biochemistry 48, 3354–3369 (2009)CrossRefGoogle Scholar
  73. 73.
    R. Ahlrichs, M. Bar, M. Haser, H. Horn, C. Kolmel, Chem. Phys. Lett. 162, 165–169 (1989)CrossRefADSGoogle Scholar
  74. 74.
    A.D. Becke, Phys. Rev. A 38, 3098–3100 (1988)CrossRefADSGoogle Scholar
  75. 75.
    J.P. Perdew, W. Yue, Phys. Rev. B 33, 8800–8802 (1986)CrossRefADSGoogle Scholar
  76. 76.
    S. Grimme, J. Chem. Phys. 118, 9095–9102 (2003)CrossRefADSGoogle Scholar
  77. 77.
    A. Schäfer, C. Huber, R. Ahlrichs, J. Chem. Phys. 100, 5829–5835 (1994)CrossRefADSGoogle Scholar
  78. 78.
    A. Schäfer, H. Horn, R. Ahlrichs, J. Chem. Phys. 97, 2571–2577 (1992)CrossRefADSGoogle Scholar
  79. 79.
    M. Sierka, A. Hogekamp, R. Ahlrichs, J. Chem. Phys. 118, 9136–9148 (2003)CrossRefADSGoogle Scholar
  80. 80.
    K. Eichkorn, O. Treutler, H. Ohm, M. Haser, R. Ahlrichs, Chem. Phys. Lett. 240, 283–289 (1995)CrossRefADSGoogle Scholar
  81. 81.
    A. Klamt, G. Schuurmann, J. Chem. Soc., Perkin Trans. 2, 799–805 (1993)CrossRefGoogle Scholar
  82. 82.
    E. Krieger, T. Darden, S.B. Nabuurs, A. Finkelstein, G. Vriend, Proteins 57, 678–683 (2004)CrossRefGoogle Scholar
  83. 83.
    E. Krieger, K. Joo, J. Lee, J. Lee, S. Raman, J. Thompson, M. Tyka, D. Baker, K. Karplus, Proteins 77, 114–122 (2009)CrossRefGoogle Scholar
  84. 84.
    E. Krieger, G. Koraimann, G. Vriend, Proteins 47, 393–402 (2002)CrossRefGoogle Scholar
  85. 85.
    E. Krieger, J.E. Nielsen, C.A. Spronk, G. Vriend, J. Mol. Graph. Model. 25, 481–486 (2006)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Daniel Tietze
    • 1
  • Stephan Voigt
    • 1
  • Doreen Mollenhauer
    • 2
  • Gerd Buntkowsky
    • 1
    Email author
  1. 1.Eduard-Zintl-Institut für Anorganische und Physikalische ChemieTechnische Universität DarmstadtDarmstadtGermany
  2. 2.Institut für Chemie und BiochemieFreie Universität BerlinBerlinGermany

Personalised recommendations