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 The review is completed by new, previously unpublished results, calculating an NMR structure of NiSOD model peptide-bound cyanide based on experimental restraints measured by us and derived from the literature and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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J.K. Williams, D. Tietze, J. Wang, Y. Wu, W.F. Degrado, M. Hong, J. Am. Chem. Soc. 135, 9885–9897 (2013)
F.H. Hu, W.B. Luo, M. Hong, Science 330, 505–508 (2010)
D.M. Grant, F. Liu, R.J. Iuliucci, C. Phung, J.C. Facelli, D. Alderman, Acta Crystallogr. B 51, 540–546 (1995)
I. Sack, A. Goldbourt, S. Vega, G. Buntkowsky, J. Magn. Reson. 138, 154 (1999)
I. Sack, S. Macholl, F. Wehrmann, J. Albrecht, H.H. Limbach, F. Fillaux, M.H. Baron, G. Buntkowsky, Appl. Magn. Reson. 17, 413 (1999)
R.K. Harris, Analyst 131, 351–373 (2006)
B. Elena, G. Pintacuda, N. Mifsud, L. Emsley, J. Am. Chem. Soc. 128, 9555–9560 (2006)
S. M. Reutzel-Edens, in Engineering of Crystalline Materials Properties, Springer, pp. 351–374 (2008)
M. J. Potrzebowski, Crystallography and NMR: Applications to Organic and Pharmaceutical Chemistry, eMag Res (2008)
R. K. Harris, Crystallography and NMR: an Overview, eMag Res (2008)
F. Taulelle, Fundamental Principles of NMR Crystallography, Wiley Online Library (2009)
S. Macholl, D. Tietze, G. Buntkowsky, Cryst. Eng. Comm. 15, 8627–8638 (2013)
T.G. Oas, R.G. Griffin, M.H. Levitt, J. Chem. Phys. 89, 692 (1988)
T. Gullion, J. Schaefer, J. Magn. Reson. 81, 196 (1989)
T. Gullion and J. Schaefer, W.S. Warren (ed), Adv. in Magn. and Opt. Res. 13, 57 (1989)
M. Levitt, D.P. Raleigh, F. Creuzet, R.G. Griffin, J. Chem. Phys. 92, 6347 (1990)
A. Hing, S. Vega, J. Schaefer, J. Magn. Reson. 96, 205 (1992)
A.E. Bennett, J.H. Ok, R.G. Griffin, S. Vega, J. Chem. Phys. 96, 8642 (1992)
A.E. Bennett, R.G. Griffin, S. Vega, Springer Series NMR 33, 1 (1994)
G. Cornilescu, F. Delaglio, A. Bax, J. Biomol. NMR 13, 289–302 (1999)
S. Macholl, F. Boerner, G. Buntkowsky, Chem. Eur. J. 10, 4808–4816 (2004)
S. Macholl, F. Boerner, G. Buntkowsky, Z. Phys. Chem. 217, 1473–1505 (2003)
S. Macholl, D. Lentz, F. Borner, G. Buntkowsky, Chem. Eur. J. 13, 6139–6149 (2007)
L. Seyfarth, J. Seyfarth, B.V. Lotsch, W. Schnick, J. Senker, Phys. Chem. Chem. Phys. 12, 2227–2237 (2010)
M. Schmidt, J.J. Wittmann, R. Kress, D. Schneider, D. Schneider, H.W. Schmidt, Jr Senker, Cryst. Growth Des. 12, 2543–2551 (2012)
E. Wirnhier, M.B. Mesch, J. Senker, W. Schnick, Chem. Eur. J. 19, 2041–2049 (2013)
R.K. Harris, R.E. Wasylishen, M.J. Duer, NMR Crystallography (Wiley, New York, 2009)
J.A. Ripmeester, R.E. Wasylishen, Cryst. Eng. Comm. 15, 8598 (2013)
T. Gullion, Concept Magn. Reson. 10, 277 (1998)
B.B. Keele Jr, J.M. McCord, I. Fridovich, J. Biol. Chem. 245, 6176–6181 (1970)
J.L. Hsu, Y. Hsieh, C. Tu, D. O’Connor, H.S. Nick, D.N. Silverman, J. Biol. Chem. 271, 17687–17691 (1996)
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
I. Fridovich, J. Biol. Chem. 264, 7761–7764 (1989)
J.J. Haddad, Cell. Signal. 14, 879–897 (2002)
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)
H.-D. Youn, E.-J. Kim, J.-H. Roe, Y.C. Hah, S.-O. Kang, Biochem. J. 318, 889–896 (1996)
M. Schmidt, B. Meier, C. Scherk, O. Iakovleva, F. Parak, Prog. Biophys. Mol. Biol. 65, Pa113–Pa113 (1996)
M. Schmidt, B. Meier, F. Parak, J. Biol. Inorg. Chem. 1, 532–541 (1996)
A.-F. Miller, D.L. Sorkin, Comments Mol. Cell. Biophys. 9, 1–48 (1997)
B. Meier, C. Scherk, M. Schmidt, F. Parak, Biochem. J. 331, 403–407 (1998)
D.P. Barondeau, C.J. Kassmann, C.K. Bruns, J.A. Tainer, E.D. Getzoff, Biochemistry 43, 8038–8047 (2004)
P.A. Bryngelson, S.E. Arobo, J.L. Pinkham, D.E. Cabelli, M.J. Maroney, J. Am. Chem. Soc. 126, 460–461 (2004)
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)
D.P. Riley, W.J. Rivers, R.H. Weiss, Anal. Biochem. 196, 344–349 (1991)
J. Shearer, L.M. Long, Inorg. Chem. 45, 2358–2360 (2006)
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)
G.E.O. Borgstahl, H.E. Parge, M.J. Hickey, W.F. Beyer, R.A. Hallewell, J.A. Tainer, Cell 71, 107–118 (1992)
R.H. Holm, P. Kennepohl, E.I. Solomon, Chem. Rev. 96, 2239–2314 (1996)
W.G. Han, T. Lovell, L. Noodleman, Inorg. Chem. 41, 205–218 (2002)
A.F. Miller, K. Padmakumar, D.L. Sorkin, A. Karapetian, C.K. Vance, J. Inorg. Biochem. 93, 71–83 (2003)
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)
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)
M.S. Lah, M.M. Dixon, K.A. Pattridge, W.C. Stallings, J.A. Fee, M.L. Ludwig, Biochemistry 34, 1646–1660 (1995)
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)
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)
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)
I. Bertini, C. Luchinat, NMR of Paramagnetic Molecules in Biological Systems (Benjamin/Cummings Publ. Menlo Park, CA, 1987)
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)
L. McDowell, M. Lee, R.A. McKay, K.S. Anderson, J. Schaefer, Biochemistry 35, 3328 (1996)
H.L. van Camp, R.H. Sands, J.A. Fee, Biochim. Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 704, 75–89 (1982)
G. Rotilio, L. Morpurgo, C. Giovagnoli, L. Calabrese, B. Mondovi, Biochemistry 11, 2187–2192 (1972)
J. Han, N.J. Blackburn, T.M. Loehr, Inorg. Chem. 31, 3223–3229 (1992)
K.D. Carugo, A. Battistoni, M.T. Carrì, F. Polticelli, A. Desideri, G. Rotilio, A. Coda, M. Bolognesi, FEBS Lett. 349, 93–98 (1994)
J.A. Tainer, E.D. Getzoff, J.S. Richardson, D.C. Richardson, Nature 306, 284–287 (1983)
J.W. Whittaker, M.M. Whittaker, J. Am. Chem. Soc. 113, 5528–5540 (1991)
M. Schmidt, S. Zahn, M. Carella, O. Ohlenschlager, M. Gorlach, E. Kothe, J. Weston, Chem. Bio. Chem. 9, 2135–2146 (2008)
K.P. Neupane, K. Gearty, A. Francis, J. Shearer, J. Am. Chem. Soc. 129, 14605–14618 (2007)
J. Shearer, K.P. Neupane, P.E. Callan, Inorg. Chem. 48, 10560–10571 (2009)
D. Tietze, H. Breitzke, D. Imhof, E. Kothe, J. Weston, G. Buntkowsky, Chem. Eur. J. 15, 517–523 (2009)
D. Tietze, M. Tischler, S. Voigt, D. Imhof, O. Ohlenschlager, M. Görlach, G. Buntkowsky, Chem. Eur. J. 16, 7572–7578 (2010)
M.-S. Cheung, M.L. Maguire, T.J. Stevens, R.W. Broadhurst, J. Magn. Reson. 202, 223–233 (2010)
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)
R. Ahlrichs, M. Bar, M. Haser, H. Horn, C. Kolmel, Chem. Phys. Lett. 162, 165–169 (1989)
A.D. Becke, Phys. Rev. A 38, 3098–3100 (1988)
J.P. Perdew, W. Yue, Phys. Rev. B 33, 8800–8802 (1986)
S. Grimme, J. Chem. Phys. 118, 9095–9102 (2003)
A. Schäfer, C. Huber, R. Ahlrichs, J. Chem. Phys. 100, 5829–5835 (1994)
A. Schäfer, H. Horn, R. Ahlrichs, J. Chem. Phys. 97, 2571–2577 (1992)
M. Sierka, A. Hogekamp, R. Ahlrichs, J. Chem. Phys. 118, 9136–9148 (2003)
K. Eichkorn, O. Treutler, H. Ohm, M. Haser, R. Ahlrichs, Chem. Phys. Lett. 240, 283–289 (1995)
A. Klamt, G. Schuurmann, J. Chem. Soc., Perkin Trans. 2, 799–805 (1993)
E. Krieger, T. Darden, S.B. Nabuurs, A. Finkelstein, G. Vriend, Proteins 57, 678–683 (2004)
E. Krieger, K. Joo, J. Lee, J. Lee, S. Raman, J. Thompson, M. Tyka, D. Baker, K. Karplus, Proteins 77, 114–122 (2009)
E. Krieger, G. Koraimann, G. Vriend, Proteins 47, 393–402 (2002)
E. Krieger, J.E. Nielsen, C.A. Spronk, G. Vriend, J. Mol. Graph. Model. 25, 481–486 (2006)
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Financial support by the Deutsche Forschungsgemeinschaft DFG under contract Bu 911-21-1 is gratefully acknowledged.
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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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DOI: https://doi.org/10.1007/s00723-014-0576-9