On the functional role of a water molecule in Clade 3 catalases: A proposal for the mechanism by which NADPH prevents the formation of compound II

Journal of the American Chemical Society

Volumn 130, Issue 23, 2008, Pages 7345-7356

  Sicking, Willi ^a   Korth, Hans Gert ^a   De Groot, Herbert ^b   Sustmann, Reiner ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MECHANISMS; MIXTURES; PORPHYRINS; TELLURIUM COMPOUNDS; WATER CONSERVATION;

GAIN INSIGHT; IN ORDER; INTERMEDIATE COMPOUNDS; WATER MOLECULES; X RAY STRUCTURES;

PLANTS (BOTANY);

ANION; CARBONYL DERIVATIVE; CATALASE; CHEMICAL COMPOUND; HEME; HYDROXYL GROUP; PORPHYRIN; PROLINE; PROTEIN SUBUNIT; PROTON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SERINE; THREONINE; WATER;

ARTICLE; CATALYSIS; CHEMICAL REACTION; CHEMICAL STRUCTURE; CLADISTICS; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME KINETICS; HYDROGEN BOND; MOLECULE;

CATALASE; CRYSTALLOGRAPHY, X-RAY; FERRIC COMPOUNDS; HEME; MODELS, MOLECULAR; NADP; QUANTUM THEORY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 44949182706     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja077787e     Document Type: Article

References (84)

1. Zamocky, M.; Koller, F. Prog. Biophys. Mol. Biol. 1999, 72, 19-66.
2. Nicholls, P.; Fita, I.; Loewen, P. C. Adv. Inorg. Chem. 2001, 51, 51-106.
3. Chelikani, P.; Fita, I.; Loewen, P. C. Cell. Mol. Life Sci. 2004, 61, 192-208.
4. Kirkman, H. N.; Gaetani, G. F. Trends Biochem. Sci. 2007, 32, 44-50.
5. Bartosz, G. Handb. Environ. Chem. 2005, 2, 109-149.
6. Putnam, C. D.; Arvai, A. S.; Bourne, Y.; Tainer, J. A. J. Mol. Biol. 2000, 296, 295-309.
7. Schonbaum, G. R.; Chance, B. In The Enzymes, 3rd ed.; Boyer, P. D., Ed.; Academic Press: New York, 1976; Vol. 13, pp 363-408.
8. Deisseroth, A.; Dounce, A. L. Physiol. Rev. 1970, 50, 319-375.
9. Nicholls, P.; Schonbaum, G. R. In The Enzymes, 2nd ed.; Boyer, P. D., Lardy, H., Myrbäck, K., Eds.; Academic Press: New York, 1963; Vol. 8, pp 147-225.
10. Klotz, M. G.; Loewen, P. C. Mol. Biol. Evol. 2003, 20, 1098-1112.
11. Kirkman, H. N.; Galiano, S.; Gaetani, G. F. J. Biol. Chem. 1987, 262, 660-666.
12. Almarsson, Ö.; Sinha, A.; Gopinath, E.; Bruice, T. C. J. Am. Chem. Soc. 1993, 115, 7093-7102.
13. Hillar, A.; Nicholls, P.; Switala, J.; Loewen, P. C. Biochem. J. 1994, 300, 531-539.
14. Olson, L. P.; Bruice, T. C. Biochemistry 1995, 34, 7335-7347.
15. Bicout, D. J.; Field, M. J.; Gouet, P.; Jouve, H. M. Biochim. Biophys. Acta 1995, 1252, 172-176.
16. Kirkman, H. N.; Rolfo, M.; Ferraris, A. M.; Gaetani, G. F. J. Biol. Chem. 1999, 274, 13908-13914.
17. Ivancich, A.; Jouve, H. M.; Sartor, B.; Gaillard, J. Biochemistry 1997, 36, 9356-9364.
18. Chance, B. Acta Chem. Scand. 1947, 1, 236-267.
19. Chance, B. Nature 1948, 161, 914-917.
20. Jouve, H. M.; Andreoletti, P.; Gouet, P.; Hajdu, J.; Gagnon, J. Biochimie 1997, 79, 667-671.
21. Behan, R. K.; Green, M. T. J. Inorg. Biochem. 2006, 100, 448-459.
22. Alfonso-Prieto, M.; Borovik, A.; Carpena, X.; Murshudov, G.; Melik-Adamyan, W.; Fita, I.; Rovira, C.; Loewen, P. C. J. Am. Chem. Soc. 2007, 129, 4193-4205.
23. Rovira, C. ChemPhysChem 2005, 6, 1820-1826.
24. Horner, O.; Mouesca, J. M.; Solari, P. L.; Orio, M.; Oddou, J. L.; Bonville, P.; Jouve, H. M. J. Biol. Inorg. Chem. 2007, 12, 509-525.
25. De Groot, H.; Auferkamp, O.; Bramey, T.; De Groot, K.; Kirsch, M.; Korth, H.-G.; Petrat, F.; Sustmann, R. Free Radical Res. 2006, 40, 67-74.
26. Research Collaboratory for Structural Bioinformatics. RCSB Protein Data Bank. http://www.rcsb.org/pdb/ (accessed May 5, 2008).
27. Sustmann, R.; Sicking, W. PERGRA, version 2007; Universität Duisburg-Essen: Essen, Germany, 2007.
28. Titan, version 1.0; Schrödinger, LLC: Portland, OR, 1999.
29. CorelDRAW, version X3; Corel Corporation: Ottawa, ON, 2005.
30. Frisch, M. J.; et al. Gaussian 03, revision C.02; Gaussian, Inc.: Wallingford, CT, 2004.
31. Green, M. T. J. Am. Chem. Soc. 2001, 123, 9218-9219.
32. Benecky, M. J.; Frew, J. E.; Scowen, N.; Jones, P.; Hoffman, B. M. Biochemistry 1993, 32, 11929-11933.
33. Rydberg, P.; Sigfridson, E.; Ryde, U. J. Biol. Inorg. Chem. 2004, 9, 203-223.
34. Cossi, M.; Rega, N.; Scalmani, G.; Barone, V. J. Comput. Chem. 2003, 24, 669-681.
35. Barone, V.; Cossi, M. J. Phys. Chem. A 1998, 102, 1995-2001.
36. de Visser, S. P.; Shaik, S.; Sharma, P. K.; Kumar, D.; Thiel, W. J. Am. Chem. Soc. 2003, 125, 15779-15788.
37. de Visser, S. P. J. Phys. Chem. A 2005, 109, 11050-11057.
38. Frisch, A. E.; Frisch, M. J.; Tracks, G. W. Gaussian 03 User's Reference; Gaussian, Inc.: Wallingford, CT, 2003; p 205.
39. Shaik, S.; Hirao, H.; Kumar, D. Acc. Chem. Res. 2007, 40, 532-542.
40. Shaik, S.; Kumar, D.; de Visser, S. P.; Altun, A.; Thiel, W. Chem. Rev. 2005, 105, 2279-2328.
41. Sicking, W.; Korth, H.-G.; Jansen, G.; de Groot, H.; Sustmann, R. Chem.-Eur. J. 2007, 13, 4230-4245.
42. The PDB currently lists 76 entries under the keyword "catalase" , including 52 structures of monofunctional catalases and 24 structures of catalase-peroxidases. Two of the monofunctional catalases belong to Clade 1, 17 to Clade 2, and 33 to Clade 3. The full list includes complete enzymes, subunits, substrate complexes, and catalytic intermediates.
43. Carpena, X.; Soriano, M.; Klotz, M. G.; Duckworth, H. W.; Donald, L. J.; Melik-Adamyan, W.; Fita, I.; Loewen, P. C. Proteins: Struct., Funct., Genet. 2003, 50, 423-436.
44. Hara, I.; Ichise, N.; Kojima, K.; Kondo, H.; Ohgiya, S.; Matsuyama, H.; Yumoto, I. Biochemistry 2007, 46, 11-22.
45. Melik-Adamyan, W. R.; Bravo, J.; Carpena, X.; Switala, J.; Mate, M. J.; Fita, I.; Loewen, P. C. Proteins: Struct., Funct., Genet. 2001, 44, 270-281.
46. Diaz, A.; Horjales, E.; Rudino-Pinera, E.; Arreola, R.; Hansberg, W. J. Mol. Biol. 2004, 342, 971-985.
47. Ko, T. P.; Day, J.; Malkin, A. J.; McPherson, A. Acta Crystallogr. 1999, D55, 1383-1394.
48. Murshudov, G. N.; Grebenko, A. I.; Brannigan, J. A.; Antson, A. A.; Barynin, V. V.; Dodson, G. G.; Dauter, Z.; Wilson, K. S.; Melik-Adamyan, W. R Acta Crystallogr. 2002, D58, 1972-1982.
49. Gouet, P.; Jouve, H.-M.; Dideberg, O. J. Mol. Biol. 1995, 249, 933-954.
50. Mate, M. J.; Zamocky, M.; Nykyri, L. M.; Herzog, C.; Alzari, P. M.; Betzel, C.; Koller, F.; Fita, I. J. Mol. Biol. 1999, 286, 135-149.
51. 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.
52. Hakansson, K. O.; Brugna, M.; Tasse, L. Acta Crystallogr. 2004, D60, 1374-1380.
53. Riise, E. K.; Lorentzen, M. S.; Helland, R.; Smalas, A. O.; Leiros, H. K. S.; Willassen, N. P. Acta Crystallogr. 2007, D63, 135-148.
54. For the numbering of the atoms of the catalase heme group, see: Fita, I.; Rossmann, M. G. J. Mol. Biol. 1985, 185, 21-37.
55. Jeffrey, G. A.; Saeger, W. Hydrogen Bonding in Biological Structures; 2nd ed.; Springer: Berlin, 1994.
56. 47 However, in the related crystal structure, fewer water molecules than in the other catalases have been detected. A feature similar to the chain of water molecules (W197, W21, W224, W171) on the proximal side of the heme of HEC shown in Figure 3 was also found in all of the other catalases except BLC (see Table S1 and Figure S5 in the Supporting Information). Thus, in BLC, the water may simply have escaped detection. Therefore, we suggest that this catalase should be reanalyzed.
57. Svistunenko, D. A. Biochim. Biophys. Acta 2005, 1707, 127-155.
58. Ivancich, A.; Jouve, H. M.; Gaillard, J. J. Am. Chem. Soc. 1996, 118, 12852-12853.
59. Pipirou, Z.; Bottrill, A. R.; Metcalfe, C. M.; Mistry, S. C.; Badyal, S. K.; Rawlings, B. J.; Raven, E. L. Biochemistry 2007, 46, 2174-2180.
60. Vu, B. C.; Jones, A. D.; Lecomte, J. T. J. J. Am. Chem. Soc. 2002, 124, 8544-8545.
61. Rios-Velazquez, C.; Cox, R. L.; Donohue, T. J. Arch. Biochem. Biophys. 2001, 389, 234-244.
62. Stevens, J. M.; Uchida, T.; Daltrop, O.; Ferguson, S. J. Biochem. Soc. Trans. 2005, 33, 792-795.
63. Thöny-Meyer, L. Biochemistry 2003, 42, 13099-13105.
64. Chiavarino, B.; Crestoni, M. E.; Fornarini, S.; Rovira, C. Chem. - Eur. J. 2007, 13, 776-785.
65. Wojciechowski, G.; Ortiz de Montellano, P. R. J. Am. Chem. Soc. 2007, 129, 1663-1672.
66. Huang, L.; Wojciechowski, G.; Ortiz de Montellano, P. R. J. Biol. Chem. 2006, 281, 18983-18988.
67. Huang, L. S.; Wojciechowski, G.; Ortiz de Montellano, P. R. J. Am. Chem. Soc. 2005, 127, 5345-5353.
68. Boffi, A.; Zamparelli, C.; Verzili, D.; Ilari, A.; Chiancone, E. Arch. Biochem. Biophys. 1997, 340, 43-51.
69. Smulevich, G.; Hu, S. Z.; Rodgers, K. R.; Goodin, D. B.; Smith, K. M.; Spiro, T. G. Biospectroscopy 1996, 2, 365-376.
70. Gingrich, D. J.; Nocek, J. M.; Natan, M. J.; Hoffman, B. M. J. Am. Chem. Soc. 1987, 109, 7533-7534.
71. Zhu, Y.; Silverman, R. B. J. Org. Chem. 2007, 72, 233-239.
72. Chance, B.; Paul, K. G. Acta Chem. Scand. 1960, 14, 1711-1716.
73. Chance, B. J. Biol. Chem. 1949, 180, 947-959.
74. Jakopitsch, C.; Vlasits, J.; Wiseman, B.; Loewen, P. C.; Obinger, C. Biochemistry 2007, 46, 1183-1193.
75. 12,14,15 the THR-PRO couple adjacent to NADPH (THR149-PRO150 in BLC) in fact was located as the first relay, from which one of two favorable electron paths to the heme vinyl involves the serine residue (e.g., SER216 in BLC).
76. de Visser, S. P. Inorg. Chem. 2006, 45, 9551-9557.
77. Barea, G.; Maseras, F.; Lledos, A. THEOCHEM 2003, 632, 323-333.
78. •, the product of one-electron reduction of Cpd I by the surrounding protein, as Cpd I* (see the Introduction).
79. eq.
80. -1 greater than those of products 5 and 4. Since structures 2(H-) and 6(H-) in turn would represent the initial products of nucleophilic OH-addition to complex 5 and ferricatalase 4, respectively, it is evident that such an addition is highly unlikely to occur.
81. Kirsch, M.; Auferkamp, O.; Meier, A.-C.; Korth, H.-G.; Sustmann, R.; de Groot, H. Universität Duisburg-Essen. Unpublished results, 2007.
82. IV center.
83. Berglund, G. I.; Carlsson, G. H.; Smith, A. T.; Szoke, H.; Henriksen, A.; Hajdu, J. Nature 2002, 417, 463-468.
84. Sicking, W.; Korth, H.-G.; de Groot, H.; Sustmann, R. Universität Duisburg-Essen. Unpublished results.