The structures and electronic configuration of compound I intermediates of Helicobacter pylori and Penicillium vitale catalases determined by X-ray crystallography and QM/MM density functional theory calculations

Journal of the American Chemical Society

Volumn 129, Issue 14, 2007, Pages 4193-4205

  Alfonso Prieto, Mercedes ^a   Borovik, Anton ^b   Carpena, Xavier ^c   Murshudov, Garib ^d   Melik Adamyan, William ^b   Fita, Ignacio ^c   Rovira, Carme ^a,f   Loewen, Peter C ^e  

^a UNIVERSITY OF BARCELONA   (Spain)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d UNIVERSITY OF YORK   (United Kingdom)

^e UNIVERSITY OF MANITOBA   (Canada)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL BONDS; DENSITY FUNCTIONAL THEORY; ELECTRONIC STRUCTURE; OXIDATION; PROTONATION; X RAY CRYSTALLOGRAPHY;

ELECTRONIC CONFIGURATIONS; HELICOBACTER PYLORI (HPC); IRON OXYGEN COORDINATION; PENICILLIUM VITALE (PVC);

ENZYMES;

ACETIC ACID DERIVATIVE; HEME; HISTIDINE; IRON; OXYGEN; PORPHYRIN;

ARTICLE; CHEMICAL BOND; CRYSTAL STRUCTURE; DENSITY FUNCTIONAL THEORY; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBUNIT; HELICOBACTER PYLORI; NONHUMAN; OXIDATION; PENICILLIUM; PENICILLIUM VITALE; PROTON TRANSPORT; QUALITATIVE ANALYSIS; QUANTUM MECHANICS; X RAY CRYSTALLOGRAPHY;

EID: 34147171814     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja063660y     Document Type: Article

References (98)

1. Nichols, P.; Fita, I.; Loewen, P. C. Enzymology and structure of catalases. In Advanced Inorganic Chemistry; Sykes, A. G., Mauk, G., Eds.; Academic Press: New York, 2001; Vol. 51, pp 51-106.
2. Chelikani, P.; Fita, I.; Loewen, P. C. Cell. Mol. Life Sci. 2004, 61, 192-208.
3. Benecky, M. J.; Frew, J. E.; Scowen, N.; Jones, P.; Hoffman, B. M. Biochemistry 1993, 32, 11929-11933.
4. (a) Deiseroth, A.; Dounce, A. L. Physiol. Rev. 1970, 50, 319-375.
5. (b) Dunford, H. B. Heme Peroxidases; Wiley: New York, 1999.
6. (c) Veitch, G.; Smith, A. T. Horseradish peroxidase. In Advanced Inorganic Chemistry; Sykes, A. G., Mauk, G., Eds.; Academic Press: New York, 2001; Vol. 51, pp 107-162.
7. Schonbaum, G. R.; Chance, B. Catalase. In The Enzymes; Boyer, P. D., Ed.; Academic Press: New York, 1976; Vol. 13, pp 363-408.
8. (a) Deiseroth, A.; Dounce, A. L. Physiol. Rev. 1970, 50, 319-375.
9. (b) Dunford, H. B. Heme Peroxidases; Wiley: New York, 1999.
10. (c) Veitch, G.; Smith, A. T. Horseradish peroxidase. In Advanced Inorganic Chemistry; Sykes, A. G., Mauk, G., Eds.; Academic Press: New York, 2001; Vol. 51, pp 107-162.
11. Lardinois, O. M. Free Radical Res. 1995, 21, 251-274.
12. Berglund, G. I.; Carlsson, G. H.; Smith, A. T.; Szoke, H.; Henriksen, A.; Hajdu, J. Nature 2002, 417, 463-468.
13. Nilsson, K.; Hersleth, H. P.; Rod, T. H.; Andersson, K. K.; Ryde, U. Biophys. J. 2004, 87, 3437-3447.
14. Rovira, C. Chem. Phys. Chem. 2005, 6, 1-8.
15. Silaghi-Dumitriescu, R. J. Biol. Inorg. Chem. 2004, 9. 470-476.
16. Green, M. T.; Dawson, J. H.; Gray, H. B. Science 2004, 304, 1653-1656.
17. Hersleth, H. P.; Ryde, U.; Rydberg, P.; Gorbitz, C. H.; Andersson, K. K. J. Inorg. Biochem. 2006, 100, 460-476.
18. Carpena, X.; Wiseman, B.; Deemagarn, T.; Singh, R.; Switala, J.; Ivancich, A.; Fita, I.; Loewen, P. EMBO Rep. 2005, 6, 1156-1162.
19. (a) Green, M. T. J. Am. Chem. Soc. 2006, 128, 1902-1906.
20. (b) Behan, R. K.; Green, M. T. J. Inorg. Biochem. 2006, 100, 448-459.
21. Chance, B. Acta Chem. Scand. 1947, 1, 236-267.
22. Ivancich, A.; Jouve, H. M.; Sartor, B.; Gaillard, J. Biochemistry 1997, 36, 9356-9364.
23. Ivancich, A.; Jouve, H. M.; Gaillard, J. J. Am. Chem. Soc. 1996, 118, 12852-12853.
24. Hillar, A.; Nicholls, P.; Switala, L.; Lowen, P. C. Biochem. J. 1994, 300, 531-539.
25. Zámocky, M.; Koller, F. Prog. Biophys. Mol. Biol. 1999, 72, 19-66.
26. Hiner, A. N. P.; Raven, E. L.; Thorenley, R. N. F.; Carcia-Canovas, F.; Rodriguez-Lopez, J. N. J. Inorg. Biochem. 2002, 91, 27-34.
27. (a) Bonagura, C. A.; Bhaskar, B.; Shimizu, H.; Li, H.; Sundaramoorthy, M.; McRee, D. E.; Goodin, D. B.; Poulos, T. L. Biochemistry 2003, 42, 5600-5608.
28. (b) Sivaraja, M.; Goodin, D. B.; Smith, M.; Hoffman, B. M. Science 1989, 245, 738-740.
29. Ivancich, A.; Jakopitsch, C.; Auer, M.; Un, S.; Obinger, C. J. Am. Chem. Soc. 2003, 125, 14093-14102.
30. Jakopitsch, C.; Obinger, C.; Un, S.; Ivancich, A. J. Inorg. Biochem. 2006 100, 1091-1099.
31. Lardinois, O. M.; Ortiz de Montellano, P. M. Biochemistry 2004, 43, 4601-4610.
32. Schuenemann, V.; Lendzian, F.; Jung, C.; Contzen, J.; Barra, A.-L.; Sugar, S. G.; Trautwein, A. X. J. Biol. Chem. 2004, 279, 10919-10930.
33. Hersleth, H. P.; Dalhus, B.; Görbitz, C. H.; Andersson, K. K. J. Biol. Inorg. Chem. 2002, 7, 299-304.
34. Murshudov, G. N.; Grebenko, J. A.; Branningan, J. A.; Antson, A. A.; Barynin, V. V.; Dodson, G. G.; Dauter, Z.; Wilson, K.; Melik-Adamyan, W. R. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58, 1972-1982.
35. Gouet, P.; Jouve, H. M.; Williams, P. A.; Andersson, I.; Andreoletti, P.; Nussaume, L.; Hajdu, J. Nat. Struct. Biol. 1996, 3, 951-956.
36. Maté, M.; Murshudov, G.; Bravo, J.; Melik-Adamyan, W.; Loewen, P. C.; Fita, I. Heme-catalases. In Handbook of Metalloproteins; Messerschmidt, A., Huber, R., Poulos, T., Wieghardt, K., Eds.; John Wiley & Sons: Chichester, U.K., 2001.
37. (a) Deeth, R. J. J. Am. Chem. Soc. 1999, 121, 6074-6075.
38. (b) Green, M. T. J. Am. Chem. Soc. 2001, 123, 9218-9219.
39. (c) Bathelt, C. M.; Mulholland, A. J.; Harvey, J. N. Dalton Trans. 2005, 3470-3476.
40. (a) Derat, E.; Cohen, S.; Shaik, S.; Altun, A.; Thiel, W. J. Am. Chem. Soc. 2005, 127, 13611-13621.
41. (b) Derat, E.; Shaik, S. J. Phvs. Chem. B 2006, 110, 10526-10533.
42. (c) Derat, E.; Shaik, S. J. Am. Chem. Soc. 2006, 128, 8185-8198.
43. (a) Jouve, H. M.; Andreoletti, P.; Gouet, P.; Hajdu, J.; Gagnon, J. Biochemie 1997, 79, 667-671.
44. (b) Andreoletti, P.; Pernoud, A.; Sainz G.; Gouet, P.; Jouve, H. M. Acta Crvstallogr., Sect. D: Biol. Crystallogr. 2003, 59, 2163-2168.
45. (a) Kikuchi-Torii, K.; Hayashi, S.; Nakamoto, H.; Nakamura, S. J. Biochem. 1982, 92, 1449-1456.
46. (b) Obinger, C.; Maj, M.; Nicholls, P.; Loewen, P. C. Arch. Biochem. Biophys. 1997, 342, 58-67.
47. (c) Chelikani, P.; Carpena, X.; Perez-Luque, R.; Donald, L. J.; Duckworth, H. W.; Switala, J.; Fita, I.; Loewen, P. C. Biochemistry 2005, 44, 5597-5605.
48. Odenbreit, S.; Wieland, B.; Haas, R. J. Bacteriol. 1996, 178, 6960-6967.
49. Switala, J.; Loewen, P. C. Arch. Biochem. Biophys. 2002, 401, 145-154.
50. Loewen, P. C.; Carpena, X.; Rovira, C.; Ivancich, A.; Perez-Luque, R.; Haas, R.; Odenbreit, S.; Nicholls, P.; Fita, I. Biochemistry 2004, 43, 3089-3103.
51. Collaborative Computational Project, Number 4. Acta Crystallogr. 1994, A50, 760-763.
52. Evans, P. R. Scala. Joint CCP4 ESF-EACBM Newsl. 1997, 33, 22-24.
53. Vagin, A.; Teplyakov, A. J. Appl. Cryst. 1997, 30, 1022-1025.
54. Murshudov, G. N.; Vaain, A. A.; Dodson, E. J. Acta Crvstallogr., Sect. D: Biol. Crtystcillogr. 1997, 53, 240-255.
55. Jones, T. A.; Zou, J. Y.; Cowan, S. W.; Kjeldgaard, M. Acta Crystallogr., Sect. A: Found. Crystallogr. 1991, 47, 110-119.
56. Gulyi, M. F.; Gudkova, L. V.; Degtyarj, R. G.; Mironenko, N. I.; Latyshko, N. V. Dokl. Akad. Nauk SSSR 1975, 225, 211-213.
57. Vainshtein, B. K.; Melik-Adamyan, W. R.; Barynin, V. V.; Vagin, A. A.; Grebenko, A. I.; Borisov, V. V.; Bartels, K. S.; Fita, I.; Rossmann, M. G. J. Mol. Biol. 1986, 188, 49-61.
58. Otwinowski, Z.; Minor, W. Methods Enzvmol. 1997, 276, 307-326.
59. Evans, S. J. Mol. Graphics 1993, 11, 134-138.
60. Humphrey, W.; Dalke, A.; Schulten, K. J. Mol. Graphics 1996, 14, 33-38.
61. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M., Jr.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J. Am. Chem. Soc. 1995, 117, 5179-5197.
62. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E.; Debolt, S.; Ferguson, D.; Seibel, G.; and Kollman, P. Comput. Phys. Commun. 1995, 91, 1-41.
63. Banci, L.; Gori-Savellini, G.; Turano, P. Eur. J. Biochem. 1997, 249, 716.
64. (a) Collins, J. R.; Camper, D. L.; Loew, G. H. J. Am. Chem. Soc. 1991, 113, 2736-2743.
65. (b) Harris, D.; Loew, G. J. Am. Chem. Soc. 1995, 117, 2738-2746.
66. Rovira, C.; Fita, I. J. Phys. Chem. B 2003, 107, 5300-5305.
67. Laio, A.; vandeVondele, J.; Röthljsberger, U. J. Chem. Phys 2002, 116, 6941-6947.
68. (a) Car, R.; Parrinello, M. Phys. Rev. Lett. 1985, 55, 2471-2474.
69. (b) Marx, D.; Hutter, J. Ab initio molecular dynamics: Theory and implementation. In Modern Methods and Algorithms of Quantum Chemistry; Grotendorst, J., Ed.; John von Neumann Institute for Computing: Julich, Germany, 2000; pp 301-409.
70. (c) CPMD program; IBM Corp, MPI für Festkörperforschung: Stuttgart, 1990-2003; 1997-2001; URL: http://www.cpmd.org.
71. See for instance: (a) Carloni, P.; Röthlisberger, U.; Parrinello, M. Acc. Chem. Res. 2002, 35, 455-464.
72. (b) Ivanov, I.; Chen, B.; Raugei, S.; Klein, M. L. J. Phys. Chem. B 2006, 110, 6365-6371.
73. (c) Papoian, G. A.; DeGrado, W. F.; Klein, M. L. J. Am. Chem. Soc. 2003, 125, 560-569.
74. (d) Mordasini, T.; Curioni, A.; Andreoni, W. J. Biol. Chem. 2003, 278, 4381-4384.
75. (e) Biarnés, X.; Nieto, J.; Planas, A.; Rovira, C. J. Biol. Chem. 2006 281, 1432-1441.
76. von Lilienfeld, O. A.; Tavernelli, I.; Rothlisberger, U.; Sebastiani, D. J. Chem. Phys. 2005, 122, 013133 (1-6).
77. HUnenberger, P. J. Chem. Phys. 2000, 113, 10464-10476.
78. Troullier, M.; Martins, J. L. Phys. Rev. B 1991, 43, 1993-2006.
79. Rovira, C.; Kunc, K.; Hutter, J.; Ballone, P.; Parrinello, M. J. Phys. Chem. A 1997, 101, 8914-8925.
80. Louie, S. G.; Froyen, S.; Cohen, M. L. Phys. Rev. B 1982, 26, 1738-1742.
81. (a) Becke, A. D. J. Chem. Phys. 1986, 84, 4524-4529.
82. (b) Perdew, J. P. Phys. Rev. B. 1986, 33, 8822-8824.
83. Bassan, A.; Blomberg, M.; Borowski, T.; Siegbahn, P. E. M. J. Inorg. Biochem. 2006, 100, 727-743.
84. Vainshtein, B. K.; Melik-Adamyan, W. R.; Barynin, V. V.; Vagin, A. A.; Grebenko, A. I. Nature (London) 1981, 293, 411-412.
85. Kozlov, E. A.; Levitina, T. L.; Bobrovskaj, M. T.; Ovander, M. N.; Gudkova, L. V.; Latyshko, N. V. Biopolim. Klitina 2001, 17, 283-291.
86. Hirao, H.; Shaik, S.; Kozlowski, P. M. J. Phys. Chem. A 2006, 110, 6091-6099.
87. (a) Ghosh, A.; Almlof, J.; Que, L. J. Phys. Chem. 1994, 98, 5576-5579.
88. (b) Kuramochi, H.; Noodleman, L.; Case, D. A. J. Am. Chem. Soc. 1997, 119, 11442-11451.
89. See for instance: (a) Shaik, S.; Kumar, D.; de Visser, S. P.; Altun, A.; Thiel, W. Chem. Rev. 2005, 105, 2279-2328.
90. (b) Bathelt, C. M.; Zurek, J.; Mulholland, A. J.; Harvey, J. N. J. Am. Chem. Soc. 2005, 127, 12900-12908.
91. Steiner, T. Biophys. Chem. 2002, 95, 195-201.
92. de Visser, S. P.; Shaik, S.; Sharma, P. K.; Kumar, D.; Thiel, W. J. Am. Chem. Soc. 2003, 125, 15779-15788.
93. Guallar, V.; Friesner, R. A. J. Am. Chem. Soc. 2004, 126, 8501-8508.
94. A. Ivancich. Personal communication.
95. Jones, P.; Dunford, H. B. J. Bioinorg. Chem. 2006, 99, 2292-2298.
96. Mayer, J. M. Annu. Rev. Phys. Chem. 2004, 55, 363-390.
97. Kleywegt, G. J.; Jones, T. A. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1994, 50, 178-185.
98. Additional QM/MM calculations of the Fe(III)-OH intermediate of HPC show that the Fe-O distance enlarges to 1.81 Å. A similar trend was found in myoglobin (ref 9).