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

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 The review is completed by new, previously unpublished results, calculating an NMR structure of NiSOD model peptide-bound cyanide based on experimental restraints measured by us and derived from the literature and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.

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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)

    Article  Google Scholar 

  2. 2.

    F.H. Hu, W.B. Luo, M. Hong, Science 330, 505–508 (2010)

    Article  ADS  Google 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)

    Article  Google Scholar 

  4. 4.

    I. Sack, A. Goldbourt, S. Vega, G. Buntkowsky, J. Magn. Reson. 138, 154 (1999)

    Article  Google 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)

    Article  Google Scholar 

  6. 6.

    R.K. Harris, Analyst 131, 351–373 (2006)

    Article  ADS  Google Scholar 

  7. 7.

    B. Elena, G. Pintacuda, N. Mifsud, L. Emsley, J. Am. Chem. Soc. 128, 9555–9560 (2006)

    Article  Google Scholar 

  8. 8.

    S. M. Reutzel-Edens, in Engineering of Crystalline Materials Properties, Springer, pp. 351–374 (2008)

  9. 9.

    M. J. Potrzebowski, Crystallography and NMR: Applications to Organic and Pharmaceutical Chemistry, eMag Res (2008)

  10. 10.

    R. K. Harris, Crystallography and NMR: an Overview, eMag Res (2008)

  11. 11.

    F. Taulelle, Fundamental Principles of NMR Crystallography, Wiley Online Library (2009)

  12. 12.

    S. Macholl, D. Tietze, G. Buntkowsky, Cryst. Eng. Comm. 15, 8627–8638 (2013)

    Article  Google Scholar 

  13. 13.

    T.G. Oas, R.G. Griffin, M.H. Levitt, J. Chem. Phys. 89, 692 (1988)

    Article  ADS  Google Scholar 

  14. 14.

    T. Gullion, J. Schaefer, J. Magn. Reson. 81, 196 (1989)

    ADS  Google Scholar 

  15. 15.

    T. Gullion and J. Schaefer, W.S. Warren (ed), Adv. in Magn. and Opt. Res. 13, 57 (1989)

  16. 16.

    M. Levitt, D.P. Raleigh, F. Creuzet, R.G. Griffin, J. Chem. Phys. 92, 6347 (1990)

    Article  ADS  Google Scholar 

  17. 17.

    A. Hing, S. Vega, J. Schaefer, J. Magn. Reson. 96, 205 (1992)

    ADS  Google 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)

    Article  Google Scholar 

  21. 21.

    S. Macholl, F. Boerner, G. Buntkowsky, Chem. Eur. J. 10, 4808–4816 (2004)

    Article  Google Scholar 

  22. 22.

    S. Macholl, F. Boerner, G. Buntkowsky, Z. Phys. Chem. 217, 1473–1505 (2003)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

  28. 28.

    J.A. Ripmeester, R.E. Wasylishen, Cryst. Eng. Comm. 15, 8598 (2013)

    Article  Google Scholar 

  29. 29.

    T. Gullion, Concept Magn. Reson. 10, 277 (1998)

    Article  Google 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)

    Article  Google 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. 129–138

  33. 33.

    I. Fridovich, J. Biol. Chem. 264, 7761–7764 (1989)

    Google Scholar 

  34. 34.

    J.J. Haddad, Cell. Signal. 14, 879–897 (2002)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

    Article  Google Scholar 

  44. 44.

    D.P. Riley, W.J. Rivers, R.H. Weiss, Anal. Biochem. 196, 344–349 (1991)

    Article  Google Scholar 

  45. 45.

    J. Shearer, L.M. Long, Inorg. Chem. 45, 2358–2360 (2006)

    Article  Google 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)

    Article  Google 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)

    Article  Google Scholar 

  48. 48.

    R.H. Holm, P. Kennepohl, E.I. Solomon, Chem. Rev. 96, 2239–2314 (1996)

    Article  Google Scholar 

  49. 49.

    W.G. Han, T. Lovell, L. Noodleman, Inorg. Chem. 41, 205–218 (2002)

    Article  Google Scholar 

  50. 50.

    A.F. Miller, K. Padmakumar, D.L. Sorkin, A. Karapetian, C.K. Vance, J. Inorg. Biochem. 93, 71–83 (2003)

    Article  Google 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)

  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)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

    Article  Google 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)

    Article  Google Scholar 

  57. 57.

    I. Bertini, C. Luchinat, NMR of Paramagnetic Molecules in Biological Systems (Benjamin/Cummings Publ. Menlo Park, CA, 1987)

  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)

    Article  Google Scholar 

  59. 59.

    L. McDowell, M. Lee, R.A. McKay, K.S. Anderson, J. Schaefer, Biochemistry 35, 3328 (1996)

    Article  Google 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)

    Article  Google Scholar 

  61. 61.

    G. Rotilio, L. Morpurgo, C. Giovagnoli, L. Calabrese, B. Mondovi, Biochemistry 11, 2187–2192 (1972)

    Article  Google Scholar 

  62. 62.

    J. Han, N.J. Blackburn, T.M. Loehr, Inorg. Chem. 31, 3223–3229 (1992)

    Article  Google 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)

    Article  Google Scholar 

  64. 64.

    J.A. Tainer, E.D. Getzoff, J.S. Richardson, D.C. Richardson, Nature 306, 284–287 (1983)

  65. 65.

    J.W. Whittaker, M.M. Whittaker, J. Am. Chem. Soc. 113, 5528–5540 (1991)

    Article  Google Scholar 

  66. 66.

    M. Schmidt, S. Zahn, M. Carella, O. Ohlenschlager, M. Gorlach, E. Kothe, J. Weston, Chem. Bio. Chem. 9, 2135–2146 (2008)

    Article  Google Scholar 

  67. 67.

    K.P. Neupane, K. Gearty, A. Francis, J. Shearer, J. Am. Chem. Soc. 129, 14605–14618 (2007)

    Article  Google Scholar 

  68. 68.

    J. Shearer, K.P. Neupane, P.E. Callan, Inorg. Chem. 48, 10560–10571 (2009)

    Article  Google 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)

    Article  ADS  Google 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)

    Article  Google Scholar 

  73. 73.

    R. Ahlrichs, M. Bar, M. Haser, H. Horn, C. Kolmel, Chem. Phys. Lett. 162, 165–169 (1989)

    Article  ADS  Google Scholar 

  74. 74.

    A.D. Becke, Phys. Rev. A 38, 3098–3100 (1988)

    Article  ADS  Google Scholar 

  75. 75.

    J.P. Perdew, W. Yue, Phys. Rev. B 33, 8800–8802 (1986)

    Article  ADS  Google Scholar 

  76. 76.

    S. Grimme, J. Chem. Phys. 118, 9095–9102 (2003)

    Article  ADS  Google Scholar 

  77. 77.

    A. Schäfer, C. Huber, R. Ahlrichs, J. Chem. Phys. 100, 5829–5835 (1994)

    Article  ADS  Google Scholar 

  78. 78.

    A. Schäfer, H. Horn, R. Ahlrichs, J. Chem. Phys. 97, 2571–2577 (1992)

    Article  ADS  Google Scholar 

  79. 79.

    M. Sierka, A. Hogekamp, R. Ahlrichs, J. Chem. Phys. 118, 9136–9148 (2003)

    Article  ADS  Google Scholar 

  80. 80.

    K. Eichkorn, O. Treutler, H. Ohm, M. Haser, R. Ahlrichs, Chem. Phys. Lett. 240, 283–289 (1995)

    Article  ADS  Google Scholar 

  81. 81.

    A. Klamt, G. Schuurmann, J. Chem. Soc., Perkin Trans. 2, 799–805 (1993)

    Article  Google Scholar 

  82. 82.

    E. Krieger, T. Darden, S.B. Nabuurs, A. Finkelstein, G. Vriend, Proteins 57, 678–683 (2004)

    Article  Google 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)

    Article  Google Scholar 

  84. 84.

    E. Krieger, G. Koraimann, G. Vriend, Proteins 47, 393–402 (2002)

    Article  Google Scholar 

  85. 85.

    E. Krieger, J.E. Nielsen, C.A. Spronk, G. Vriend, J. Mol. Graph. Model. 25, 481–486 (2006)

    Article  Google Scholar 

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Acknowledgments

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

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Correspondence to Gerd Buntkowsky.

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Tietze, D., Voigt, S., Mollenhauer, D. et al. NMR Crystallography as a Novel Tool for the Understanding of the Mode of Action of Enzymes: SOD a Case Study. Appl Magn Reson 45, 841–857 (2014). https://doi.org/10.1007/s00723-014-0576-9

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Keywords

  • Nuclear Magnetic Resonance
  • Nuclear Magnetic Resonance Spectroscopy
  • Nuclear Magnetic Resonance Structure
  • Continuum Solvation Model
  • Cyanide Anion