The Molecular Mechanism of the Catalase-like Activity in Horseradish Peroxidase

Journal of the American Chemical Society

Volumn 137, Issue 34, 2015, Pages 11170-11178

  Campomanes, Pablo ^a,d   Rothlisberger, Ursula ^a   Alfonso Prieto, Mercedes ^b   Rovira, Carme ^b,c  

^a EPFL   (Switzerland)

^b UNIVERSITY OF BARCELONA   (Spain)

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

^d UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMS; BIOCHEMISTRY; ENZYMES; FOOD PRODUCTS; FREE ENERGY; FREE RADICAL REACTIONS; HYDROGEN BONDS; IODINE; MOLECULES;

CATALASE-LIKE ACTIVITY; DISPROPORTIONATIONS; HORSERADISH PEROXIDASE; HYDROGEN BOND NETWORKS; HYDROGEN-ATOM TRANSFER; METADYNAMICS SIMULATIONS; MOLECULAR MECHANISM; RATE DETERMINING STEP;

PLANTS (BOTANY);

CATALASE; HORSERADISH PEROXIDASE; HYDROGEN; HYDROGEN PEROXIDE; PEROXY RADICAL;

ARTICLE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STRUCTURE; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; BIOCATALYSIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; PENICILLIUM; QUANTUM THEORY;

BIOCATALYSIS; CATALASE; CATALYTIC DOMAIN; HORSERADISH PEROXIDASE; HYDROGEN PEROXIDE; MOLECULAR DYNAMICS SIMULATION; PENICILLIUM; QUANTUM THEORY;

EID: 84941005037     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/jacs.5b06796     Document Type: Article

References (69)

1. Zamocky, M.; Furtmuller, P. G.; Obinger, C. Antioxid. Redox Signaling 2008, 10, 1527-1548 10.1089/ars.2008.2046
2. Krainer, F. W.; Glieder, A. Appl. Microbiol. Biotechnol. 2015, 99, 1611-1625 10.1007/s00253-014-6346-7
3. Derat, E.; Cohen, S.; Shaik, S.; Altun, A.; Thiel, W. J. Am. Chem. Soc. 2005, 127, 13611-13621 10.1021/ja0534046
4. Dunford, H. B. Heme Peroxidases; John Wiley: New York, 1999.
5. Kim, S. H.; Perera, R.; Hager, L. P.; Dawson, J. H.; Hoffman, B. M. J. Am. Chem. Soc. 2006, 128, 5598-5599 10.1021/ja060776l
6. Ivancich, A.; Jouve, H. M.; Sartor, B.; Gaillard, J. Biochemistry 1997, 36, 9356-9364 10.1021/bi970886s
7. Chuang, W. J.; Vanwart, H. E. J. Biol. Chem. 1992, 267, 13293-13301
8. Derat, E.; Shaik, S. J. Am. Chem. Soc. 2006, 128, 8185-8198 10.1021/ja0600734
9. Dunford, H. B.; Dunford, H. B. Peroxidases and Catalases: Biochemistry, Biophysics, Biotechnology, and Physiology, 2 nd ed.; Wiley: Hoboken, NJ, 2010.
10. Nicholls, P.; Fita, I.; Loewen, P. C. In Advances in Inorganic Chemistry; Sykes, A. G. G. M., Ed.; Academic Press: Waltham, MA, 2001; pp 51-106.
11. Matsui, T.; Ozaki, S.; Liong, E.; Phillips, G. N., Jr.; Watanabe, Y. J. Biol. Chem. 1999, 274, 2838-2844 10.1074/jbc.274.5.2838
12. Hernandez-Ruiz, J.; Arnao, M. B.; Hiner, A. N.; Garcia-Canovas, F.; Acosta, M. Biochem. J. 2001, 354, 107-114 10.1042/0264-6021:3540107
13. Matsunaga, I.; Shiro, Y. Curr. Opin. Chem. Biol. 2004, 8, 127-132 10.1016/j.cbpa.2004.01.001
14. Nastri, F.; Lista, L.; Ringhieri, P.; Vitale, R.; Faiella, M.; Andreozzi, C.; Travascio, P.; Maglio, O.; Lombardi, A.; Pavone, V. Chem.-Eur. J. 2011, 17, 4444-4453 10.1002/chem.201003485
15. Vlasits, J.; Jakopitsch, C.; Bernroitner, M.; Zamocky, M.; Furtmuller, P. G.; Obinger, C. Arch. Biochem. Biophys. 2010, 500, 74-81 10.1016/j.abb.2010.04.018
16. Dawson, J. H. Science 1988, 240, 433-439 10.1126/science.3358128
17. de Visser, S. P.; Shaik, S.; Sharma, P. K.; Kumar, D.; Thiel, W. J. Am. Chem. Soc. 2003, 125, 15779-15788 10.1021/ja0380906
18. Chelikani, P.; Fita, I.; Loewen, P. C. Cell. Mol. Life Sci. 2004, 61, 192-208 10.1007/s00018-003-3206-5
19. Alfonso-Prieto, M.; Vidossich, P.; Rovira, C. Arch. Biochem. Biophys. 2012, 525, 121-130 10.1016/j.abb.2012.04.004
20. Vidossich, P.; Alfonso-Prieto, M.; Carpena, X.; Fita, I.; Loewen, P. C.; Rovira, C. Arch. Biochem. Biophys. 2010, 500, 37-44 10.1016/j.abb.2010.04.021
21. Takahashi, A.; Kurahashi, T.; Fujii, H. Inorg. Chem. 2009, 48, 2614-2625 10.1021/ic802123m
22. Robert, A.; Loock, B.; Momenteau, M.; Meunier, B. Inorg. Chem. 1991, 30, 706-711 10.1021/ic00004a021
23. Silaghi-Dumitrescu, R. J. Porphyrins Phthalocyanines 2010, 14, 371-374 10.1142/S1088424610002161
24. Vidossich, P.; Alfonso-Prieto, M.; Rovira, C. J. Inorg. Biochem. 2012, 117, 292-297 10.1016/j.jinorgbio.2012.07.002
25. Alfonso-Prieto, M.; Biarnés, X.; Vidossich, P.; Rovira, C. J. Am. Chem. Soc. 2009, 131, 11751-11761 10.1021/ja9018572
26. Fita, I.; Rossmann, M. G. J. Mol. Biol. 1985, 185, 21-37 10.1016/0022-2836(85)90180-9
27. Loewen, P. C.; Carpena, X.; Vidossich, P.; Fita, I.; Rovira, C. J. Am. Chem. Soc. 2014, 136, 7249-7252 10.1021/ja502794e
28. Berglund, G. I.; Carlsson, G. H.; Smith, A. T.; Szoke, H.; Henriksen, A.; Hajdu, J. Nature 2002, 417, 463-468 10.1038/417463a
29. Olsson, M. H. M.; Søndergaard, C. R.; Rostkowski, M.; Jensen, J. H. J. Chem. Theory Comput. 2011, 7, 525-537 10.1021/ct100578z
30. Søndergaard, C. R.; Olsson, M. H. M.; Rostkowski, M.; Jensen, J. H. J. Chem. Theory Comput. 2011, 7, 2284-2295 10.1021/ct200133y
31. Derat, E.; Shaik, S. J. Am. Chem. Soc. 2006, 128, 13940-13949 10.1021/ja065058d
32. Casadei, C. M.; Gumiero, A.; Metcalfe, C. L.; Murphy, E. J.; Basran, J.; Concilio, M. G.; Teixeira, S. C.; Schrader, T. E.; Fielding, A. J.; Ostermann, A.; Blakeley, M. P.; Raven, E. L.; Moody, P. C. Science 2014, 345, 193-197 10.1126/science.1254398
33. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J. Am. Chem. Soc. 1995, 117, 5179-5197 10.1021/ja00124a002
34. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J. Chem. Phys. 1983, 79, 926-935 10.1063/1.445869
35. Banci, L.; Gori-Savellini, G.; Turano, P. Eur. J. Biochem. 1997, 249, 716-723 10.1111/j.1432-1033.1997.t01-1-00716.x
36. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. J. Chem. Phys. 1995, 103, 8577-8593 10.1063/1.470117
37. Kubo, R.; Hashitsume, N.; Toda, M. Statistical Physics II: Nonequilibrium Statistical Mechanics, 2 nd ed.; Springer: Berlin, 1995.
38. Jones, P.; Dunford, H. B. J. Inorg. Biochem. 2005, 99, 2292-2298 10.1016/j.jinorgbio.2005.08.009
39. Adamczyk, K.; Simpson, N.; Greetham, G. M.; Gumiero, A.; Walsh, M. A.; Towrie, M.; Parker, A. W.; Hunt, N. T. Chem. Sci. 2015, 6, 505-516 10.1039/C4SC02752C
40. Derat, E.; Shaik, S.; Rovira, C.; Vidossich, P.; Alfonso-Prieto, M. J. Am. Chem. Soc. 2007, 129, 6346-6347 10.1021/ja0676861
41. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. J. Comput. Chem. 2005, 26, 1781-1802 10.1002/jcc.20289
42. Humphrey, W.; Dalke, A.; Schulten, K. J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
43. VandeVondele, J.; Krack, M.; Mohamed, F.; Parrinello, M.; Chassaing, T.; Hutter, J. Comput. Phys. Commun. 2005, 167, 103-128 10.1016/j.cpc.2004.12.014
44. Laino, T.; Mohamed, F.; Laio, A.; Parrinello, M. J. Chem. Theory Comput. 2005, 1, 1176-1184 10.1021/ct050123f
45. Laio, A.; VandeVondele, J.; Rothlisberger, U. J. Chem. Phys. 2002, 116, 6941-6947 10.1063/1.1462041
46. VandeVondele, J.; Hutter, J. J. Chem. Phys. 2007, 127, 114105 10.1063/1.2770708
47. Goedecker, S.; Teter, M.; Hutter, J. Phys. Rev. B: Condens. Matter Mater. Phys. 1996, 54, 1703-1710 10.1103/PhysRevB.54.1703
48. Hartwigsen, C.; Goedecker, S.; Hutter, J. Phys. Rev. B: Condens. Matter Mater. Phys. 1998, 58, 3641-3662 10.1103/PhysRevB.58.3641
49. Becke, A. D. Phys. Rev. A: At., Mol., Opt. Phys. 1988, 38, 3098-3100 10.1103/PhysRevA.38.3098
50. Lee, C. T.; Yang, W. T.; Parr, R. G. Phys. Rev. B: Condens. Matter Mater. Phys. 1988, 37, 785-789 10.1103/PhysRevB.37.785
51. Benecky, M. J.; Frew, J. E.; Scowen, N.; Jones, P.; Hoffman, B. M. Biochemistry 1993, 32, 11929-11933 10.1021/bi00095a024
52. Bussi, G.; Donadio, D.; Parrinello, M. J. Chem. Phys. 2007, 126, 014101 10.1063/1.2408420
53. Laio, A.; Parrinello, M. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12562-12566 10.1073/pnas.202427399
54. Iannuzzi, M.; Laio, A.; Parrinello, M. Phys. Rev. Lett. 2003, 90, 238302 10.1103/PhysRevLett.90.238302
55. Laio, A.; Rodriguez-Fortea, A.; Gervasio, F. L.; Ceccarelli, M.; Parrinello, M. J. Phys. Chem. B 2005, 109, 6714-6721 10.1021/jp045424k
56. Nair, N. N.; Schreiner, E.; Marx, D. J. Am. Chem. Soc. 2008, 130, 14148-14160 10.1021/ja802370c
57. Morokuma, K.; Kitaura, K. Int. J. Quantum Chem. 1976, 10, 325-340 10.1002/qua.560100211
58. Ziegler, T.; Rauk, A. Theor. Chim. Acta. 1977, 46, 1-10 10.1007/BF02401406
59. Ess, D. H.; Houk, K. N. J. Am. Chem. Soc. 2007, 129, 10646-10647 10.1021/ja0734086
60. Usharani, D.; Lacy, D. C.; Borovik, A. S.; Shaik, S. J. Am. Chem. Soc. 2013, 135, 17090-17104 10.1021/ja408073m
61. Fernandez, I.; Bickelhaupt, F. M. Chem. Soc. Rev. 2014, 43, 4953-4967 10.1039/c4cs00055b
62. Simpson, N.; Adamczyk, K.; Hithell, G.; Shaw, D. J.; Greetham, G. M.; Towrie, M.; Parker, A. W.; Hunt, N. T. Faraday Discuss. 2015, 177, 163-179 10.1039/C4FD00161C
63. Baker, C. J.; Deahl, K.; Domek, J.; Orlandi, E. W. Arch. Biochem. Biophys. 2000, 382, 232-237 10.1006/abbi.2000.2013
64. Hiner, A. N.; Hernandez-Ruiz, J.; Williams, G. A.; Arnao, M. B.; Garcia-Canovas, F.; Acosta, M. Arch. Biochem. Biophys. 2001, 392, 295-302 10.1006/abbi.2001.2460
65. ‡ is the free energy barrier.
66. Kato, S.; Ueno, T.; Fukuzumi, S.; Watanabe, Y. J. Biol. Chem. 2004, 279, 52376-52381 10.1074/jbc.M403532200
67. Barducci, A.; Bonomi, M.; Parrinello, M. WIREs Comput. Mol. Sci. 2011, 1, 826-843 10.1002/wcms.31
68. Bader, R. F. W. Atoms in Molecules: A Quantum Theory, corrected paperback ed.; Clarendon Press: Oxford, 1994.
69. 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 10.1021/ja063660y