Nature of the peroxo intermediate of the W48F/D84E ribonucleotide reductase variant: Implications for O2 activation by binuclear non-heme iron enzymes

Journal of the American Chemical Society

Volumn 126, Issue 28, 2004, Pages 8842-8855

  Skulan, Andrew J ^a   Brunold, Thomas C ^a,c   Baldwin, Jeffrey ^b   Saleh, Lana ^b   Bollinger Jr , J Martin ^b   Solomon, Edward I ^a  

^a STANFORD UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; COMPLEXATION; COMPUTATIONAL GEOMETRY; CONSTRAINT THEORY; COORDINATION REACTIONS; ELECTROCHEMISTRY; ELECTRONIC STRUCTURE; ENZYMES; IRON COMPOUNDS; MATHEMATICAL MODELS; OPTIMIZATION;

COORDINATION GEOMETRY; PEROXO INTERMEDIATES; SPECTROSCOPIC SIGNATURES;

RNA;

IRON; OXYGEN; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; BIOSYNTHESIS; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME STRUCTURE; GEOMETRY; ISOMER; SPECTROSCOPY; STRUCTURE ANALYSIS; WILD TYPE;

BINDING SITES; COMPUTER SIMULATION; FERROUS COMPOUNDS; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NONHEME IRON PROTEINS; OXYGEN; PEROXIDES; RIBONUCLEOTIDE REDUCTASES; SPECTRUM ANALYSIS, RAMAN;

EID: 3242684036     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja049106a     Document Type: Article

References (84)

1. Reichard, P.; Ehrenberg, A. Science 1983, 221, 514-519.
2. Solomon, E. I.; Brunold, T. C.; Davis, M. I.; Kemsley, J. N.; Lee, S. K.; Lehnert, N.; Neese, F.; Skulan, A. J.; Yang, Y. S.; Zhou, J. Chem. Rev. 2000, 100, 235-349.
3. Wallar, B. J.; Lipscomb, J. D. Chem. Rev. 1996, 96, 2625-2658.
4. Wada, H.; Schmidt, H.; Heinz, E.; Murata, N. J. Bacteriology 1983, 175, 544-547.
5. Schmidt, H.; Heinz, E. Plant Physiol. 1990, 94, 214-220.
6. Elango, N.; Radhakrishnan, R.; Froland, W.; Wallar, B.; Earhart, C.; Lipscomb, J.; Ohlendorf, D. Protein Sci. 1997, 6, 556-568.
7. Rosenzweig, A.; Nordlund, P.; Takahara, P.; Frederick, C.; Lippard, S. Chem. Biol. 1995, 2, 409-418.
8. Lindqvist, Y.; Huang, W.; Schneider, G.; Shanklin, J. EMBO J. 1996, 15, 4081-4092.
9. Nordlund, P.; Sjoberg, B.; Eklund, H. Nature 1990, 345, 593-598.
10. Nordlund, P.; Eklund, H. J. Mol. Biol. 1993, 232, 123-164.
11. Lovell, T.; Li, J.; Noodleman, L. Inorg. Chem. 2001, 40, 5267-5278.
12. Lovell, T.; Li, J.; Noodleman, L. J. Biol. Inorg. Chem. 2002, 7, 799-809.
13. Parkin, S.; Chen, S.; Ley, B.; Mangravite, L.; Edmondson, D.; Huynh, B.; Bollinger, J. Biochemistry 1998, 37, 1124-1130.
14. Baldwin, J.; Moenne-Loccoz, P.; Krebs, C.; Ley, B.; Edmondson, D.; Huynh, B.; Loehr, T.; Bollinger, J. J. Inorg. Biochem. 1999, 74, 74.
15. Baldwin, J.; Krebs, C.; Ley, B.; Edmondson, D.; Huynh, B.; Bollinger, J. J. Am. Chem. Soc. 2000, 122, 12195-12206.
16. Krebs, C.; Davydov, R.; Baldwin, J.; Hoffman, B.; Bollinger, J.; Huynh, B. J. Am. Chem. Soc. 2000, 122, 5327-5336.
17. Bollinger, J. M.; Krebs, C.; Vicol, A.; Chen, S. X.; Ley, B. A.; Edmondson, D. E.; Huynh, B. H. J. Am. Chem. Soc. 1998, 120, 1094-1095.
18. Moenne-Loccoz, P.; Baldwin, J.; Ley, B.; Loehr, T.; Bollinger, J. Biochemistry 1998, 37, 14659-14663.
19. Krebs, C.; Chen, S.; Baldwin, J.; Ley, B.; Patel, U.; Edmondson, D.; Huynh, B.; Bollinger, J. J. Am. Chem. Soc. 2000, 122, 12207-12219.
20. Riggs-Gelasco, P. J.; Shu, L. J.; Chen, S. X.; Burdi, D.; Huynh, B. H.; Que, L.; Stubbe, J. J. Am. Chem. Soc. 1998, 120, 849-860.
21. Mitic, N.; Saleh, L.; Schenk, G.; Bollinger, J. M.; Solomon, E. I. J. Am. Chem. Soc. 2003, 125, 11200-11201.
22. Burdi, D.; Willems, J. P.; Riggs-Gelasco, P.; Antholine, W. E.; Stubbe, J.; Hoffman, B. M. J. Am. Chem. Soc. 1998, 120, 12910-12919.
23. Lee, S.; Lipscomb, J. Biochemistry 1999, 38, 4423-4432.
24. Valentine, A.; Stahl, S.; Lippard, S. J. Am. Chem. Soc. 1999, 121, 3876-3887.
25. Liu, K.; Valentine, A.; Wang, D.; Huyhn, B.; Edmonson, D.; Salifoglou, A.; Lippard, S. J. Am. Chem. Soc. 1995, 117, 10174-10185.
26. Shu, L. J.; Nesheim, J. C.; Kauffmann, K.; Münck, E.; Lipscomb, J. D.; Que, L. Science 1997, 275, 515-518.
27. Gherman, B. F.; Baik, M.-H.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2004, 126, 2978-2990.
28. Siegbahn, P. E. M. Inorg. Chem. 1999, 38, 2880-2889.
29. Broadwater, J. A.; Ai, J. Y.; Loehr, T. M.; Sanders-Loehr, J.; Fox, B. G. Biochemistry 1998, 37, 14664-14671.
30. Broadwater, J. A.; Achim, C.; Münck, E.; Fox, B. G. Biochemistry 1999, 38, 12197-12204.
31. Lyle, K.; Moenne-Loccoz, P.; Ai, J.; Sanders-Loehr, J.; Loehr, T.; Fox, B. Biochemistry 2000, 39, 10507-10513.
32. Brunold, T. C.; Tamura, N.; Kitajima, N.; Morooka, Y.; Solomon, E. I. J. Am. Chem. Soc. 1998, 120, 5674-5690.
33. Baldwin, J.; Voegtli, W.; Khidekel, N.; Moenne-Loccoz, P.; Krebs, C.; Pereira, A.; Ley, B.; Huynh, B.; Loehr, T.; Riggs-Gelasco, P.; Rosenzweig, A.; Bollinger, J. J. Am. Chem. Soc. 2001, 123, 7017-7030.
34. Krebs, C.; Bollinger, J.; Theil, E.; Huynh, B. J. Biol. Inorg. Chem. 2002, 7, 863-869.
35. Wei, P.; Skulan, A. J.; Mitic, N.; Yang, Y. S.; Saleh, L.; Solomon, E. I.; Bollinger, J. M. J. Am. Chem. Soc. 2004, in press.
36. Dunietz, B. D.; Beachy, M. D.; Cao, Y. X.; Whittington, D. A.; Lippard, S. J.; Friesner, R. A. J. Am. Chem. Soc. 2000, 122, 2828-2839.
37. Kim, K.; Lippard, S. J. Am. Chem. Soc. 1996, 118, 4914-4915.
38. Geometry convergence criteria were as follows: change in total energy, ΔE < 5e-5 Hartrees, maximum local energy gradient, δE/δS < 4.5e-4 Hartrees/Å, δE/δS(RMS) < 3e-4 Hartrees/Å, ΔS < 1.8e-3 Å, ΔS(RMS) < 1.2e-5 Å. Frequency calculations to verify that true minima had been attained were not possible as Jaguar 4.1 and subsequent Jaguar 5.0 have not implemented parallelized analytical frequency determination. Such calculations will be performed once this functionality has been added.
39. The residue truncation was performed as follows; the α-carbon was replaced by a hydrogen atom with concommitent shortening of the α-C-β-C bond to 1.08 Å, with the β-C retaining its original position. This hydrogen was then frozen in all geometry optimizations.
40. -. The positions of the heavy atoms (C, N, O) were frozen along with the positions of hydrogens replacing carbon atoms. Q43 and Q87 were modeled differently (as formamide and ammonia, respectively) as the R-group nitrogen of Q43 was located 2.8 Å from a carboxylate oxygen on D237 suggesting hydrogen bonding between these two residues which may have been of importance to the geometry of the active site. W/F48 residue, the second mutation from wt, was not included in the model as it does not coordinate to either iron or iron-coordinated residues.
41. 2-) by the D84E mutation and the introduction of a water molecule which is coordinated to E84 in the mutant.
42. Hay, P.; Wadt, W. J. Chem. Phys. 1985, 82, 299-310.
43. Baerends, E. J.; Ellis, D. E.; Ros, P. J. Chem. Phys. 1973, 2, 42.
44. te Velde, G.; Barerends, E. J. Int. J. Comput. Phys. 1992, 99, 84.
45. Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 1200.
46. Perdew, J. P. J. Chem. Phys. 1986, 33, 8822.
47. Becke, A. D. J. Chem. Phys. 1986, 84, 4524.
48. Gorelsky, S. I. AOMix Program, revision 5.69, http://www.obbligato.com/ software/aomix/.
49. Gorelsky, S. I.; Lever, A. B. P. J. Organomet. Chem. 2001, 635, 187-196.
50. Schachtschneider, J. H. Technical Report No. 57-65. Shell Development Company: Emeryville, CA, 1966.
51. Fuhrer, H.; Kartha, V. B.; Kidd, K. G.; Kreuger, P. J.; Mantsch, H. H. Computer Programs for Infrared Spectroscopy, Bulletin No. 15, National Research Council of Canada, 1976.
52. Myers, A. B.; Mathies, R. A. In Biological applications of Raman spectroscopy; Spiro, T. G., Ed.; John Wiley & Sons: New York, 1987; Vol. 2.
53. Neese, F.; Solomon, E. J. Am. Chem. Soc. 1998, 120, 12829-12848.
54. Siegbahn, P. Chem. Phys. Lett. 2002, 351, 311-318.
55. Wilson, E. B. J.; Decius, J. C.; Cross, P. C. Molecular Vibrations; Dover Publications: New York, 1980.
56. Badger, R. M. J. Chem. Phys. 1934, 2, 128-131.
57. Herschbach, D. R.; Laurie, V. W. J. Chem. Phys. 1961, 35, 458-463.
58. Baldwin, J.; Krebs, C.; Saleh, L.; Stelling, M.; Huynh, B.; Bollinger, J.; Riggs-Gelasco, P. Biochemistry 2003, 42, 13269-13279.
59. * for π-overlap with the metal.
60. Hitchman, M. A.; Riley, M. J. In Inorganic Electronic Structure and Spectroscopy; Solomon, E. I., Lever, A. B. P., Eds.; John Wiley & Sons: New York, 1999; Vol. 2.
61. The uncertainty in the percentage peroxo donation decrease is due to uncertainty in the extinction coefficient of the protein peroxo intermediate. This is due to the difficulty of calculating the proportion of a short-lived intermediate accumulated at any moment during a stopped flow experiment.
62. Fe-O values (Table 1). However, a 5° change in the Fe(2)-O-O bond angle (within anticipated error of the geometry optimized model) changes the stretching force constants required to fit the experimental data by ∼0.1 mdyne/Å.
63. Fel-based unoccupied 3d-orbitals are shown, Fe2-centered are similar (<5% difference) and are found in the Supporting Information.
64. 2 relative to when the effector protein, MMOB, is also present. Thus, the structure of the reactive biferrous MMO species remains unknown.
65. Henson, M. J.; Mukherjee, P.; Root, D. E.; Stack, T. D. P.; Solomon, E. I. J. Am. Chem. Soc. 1999, 121, 10332-10345.
66. Fox, S.; Karlin, K. D. In Active Oxygen in Biochemistry; Valentine, J. S., Foote, C. S., Greenberg, A., Liebman, J. F., Eds.; Blackie Academic & Professional: Glasgow, 1995.
67. Torrent, M.; Musaev, D. G.; Basch, H.; Morokuma, K. J. Comput. Chem. 2002, 23, 59-76.
68. Saleh, L.; Kelch, B.; Pathickal, B.; Baldwin, J.; Ley, B.; Bollinger, J. Biochemistry, submitted.
69. Saleh, L.; Krebs, C.; Ley, B.; Naik, S.; Huyhn, B.; Bollinger, J. Biochemistry, submitted.
70. A broad doublet at ∼0.3 and 0.8 mm/s and a sharper doublet at ∼ -0.3 and 1.2 mm/s.
71. A low intensity peak at ∼500 nm (ε < 100/M/cm).
72. Solomon, E.; Lowery, M.; Root, D.; Hemming, B. Mech. Bioinorg. Chem. 1995, 246, 121-164.
73. Solomon, E.; Tuczek, F.; Root, D.; Brown, C. Chem. Rev. 1994, 94, 827-856.
74. Root, D.; Mahroof-Tahir, M.; Karlin, K.; Solomon, E. Inorg. Chem. 1998, 37, 4838-4848.
75. Q =0.55 mm/s, δ = 0.43 mm/s).
76. Yoshizawa, K.; Ohta, T.; Yamabe, T.; Hoffmann, R. J. Am. Chem. Soc. 1997, 119, 12311-12321.
77. Torrent, M.; Musaev, D. G.; Morokuma, K. J. Phys. Chem. B 2001, 105, 322-327.
78. Yoshizawa, K.; Yokomichi, Y.; Shiota, Y.; Ohta, T.; Yamabe, T. Theor. Chem. Lett. 1997, 587-591.
79. Lipscomb, J. D.; Que, L. J. Biol. Inorg. Chem. 1998, 3, 331-336.
80. Pulver, S.; Froland, W.; Lipscomb, J.; Solomon, E. J. Am. Chem. Soc. 1997, 119, 387-395.
81. Pulver, S.; Froland, W.; Fox, B.; Lipscomb, J.; Solomon, E. J. Am. Chem. Soc. 1993, 115, 12409-12422.
82. Stenkamp, R. E. Chem. Rev. 1994, 94, 715-726.
83. Holmes, M.; Le Trong, I.; Turley, S.; Siekler, L.; Stenkamp, R. J. Mol. Biol. 1991, 218, 583-593.
84. Brunold, T. C.; Solomon, E. I. J. Am. Chem. Soc. 1999, 121, 8288-8295.