Chapter 13
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Model Studies of Vanadium-Dependent Haloperoxidation: Structural and Functional Lessons Synthetic and Computational Models of Supramolecular Interactions and the Formation of Peroxo Species Winfried Plass, Masroor Bangesh, Simona Nica, and Axel Buchholz Institut fur Anorganische und Analytische Chemie der Friedrich-SchillerUniversität Jena, Carl-Zeiss-Promenade 10, D-07745 Jena, Germany
Vanadate is the prosthetic group of vanadium haloperoxidases and fixed in the active site cavity by just one coordinative bond to a histidine residue and embedded in an environment of extensive hydrogen bonds. Density functional theory has been used to investigate the structure of the resting state of the prosthetic group in the enzyme pocket and to elucidate the mechanism of the formation of its peroxo complex. The role of the protein environment and in particular that of the amino acid residues Ser402 and His404 for the catalytic action of the prosthetic group is discussed and a catalytic mechanism proposed. The relevance of vanadium complexes derived from the versatile tridentate N-salicylidene hydrazide ligand system with a broad variation of the carbonic acid moiety introducing different functional groups in the side chain is presented. This includes supramolecular assemblies with chiral hosts.
© 2007 American Chemical Society
In Vanadium: The Versatile Metal; Kustin, Kenneth, et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2007.
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Introduction Vanadium dependent haloperoxidases are enzymes capable of catalyzing the oxidation of halide ions by hydrogen peroxide to the corresponding hypohalous acids and their catalytic properties have been extensively investigated in recent years (/). Crystal structures of vanadium-containing chloroperoxidases (VCPO) (2) and bromoperoxidases (VBPO) (J, 4) have been determined and reveal that an orthovanadate is coordinatively bound to a histidine residue and surrounded by several other amino acid residues forming hydrogen bonds to the anionic oxygen atoms. A schematic drawing of the active site including the prosthetic group of the V C P O from the fungus C. inaequalis is depicted in Figure 1. Nevertheless structural uncertainties concerning the prosthetic group still remain. This is related to the general resolution problem of protein crystallographic data (2.03 A for the native V C P O and 2.24 A for the peroxo form) which leads to an estimated mean positional error of the atoms of about ±0.23 A (5).
Figure 1. Structure of the active site of vanadium dependent chloroperoxidase from the fungus C. inaequalis.
The active site structure of vanadium haloperoxidase enzymes is the same for V C P O and VBPOs and, moreover, is observed to be rather rigid as the structure of the apo protein is compared with the vanadate and tungstate derivatives of the V C P O (
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Figure 12. Proposed catalytic cycle for the halide oxidation by vanadium haloperoxidases, charges at the vanadate not schown; emphasizing the specific role of the amino acid residues Lys353, Ser402 and His404 (see Figure I).
In Vanadium: The Versatile Metal; Kustin, Kenneth, et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2007.
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Acknowledgment
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We thank the Deutsche Forschungsgemeinschaft for financial support by a generous research grant and the John von Neumann Institute for Computing (NIC) at the Forschungszentrum JUlich for the generous supply of computational time on the J U M P supercomputer.
References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.
15. 16.
17. 18.
Crans, D. C.; Smee, J. J.; Gaidamauskas, E.; Yang, L . Chem. Rev. 2004, 104, 849-902. Messerschmidt, A . ; Wever, R. Proc. Natl. Acad. Sci. USA 1999, 93, 392396. Isupov, M . N.; Dalby, A . R.; Brindley, A . A . ; Izumi, Y . ; Tanabe, T.; Murshudov, G . N.; Littelchild, J. A. J. Mol. Biol. 2000, 299, 1035-1049. Weyand, M.; Hecht. H . J.; Kiess, M.; Liaud, M. F.; Vilter, H.; Schomburg, D. J. Mol. Biol. 1999, 293, 595-611. Messerschmidt, A . ; Prade, L.;Wever, R. Biol. Chem. 1997, 378, 309-315. Messerschmidt, A.; Wever, R. Inorg. Chim. Acta 1998, 273, 160-166. Plass, W. Angew. Chem. Int. Ed. 1999, 38, 909-912. Hemrika, W.; Renirie, R.; Macedo-Ribeiro, S.; Messerschmidt, A . ; Wever, R. J. Biol. Chem. 1999, 274, 23820-23827. Macedo-Ribeiro, S.; Hemrika, W.; Renirie, R.; Wever, R.; Messerschmidt, A. J. Biol. Inorg. Chem. 1999, 4, 209-219. Renirie, R.; Hemrika, W.; Pierma, S. R.; Wever, R. Biochemistry 2000, 39, 1133-1141. Tanaka, N.; Hasan, Z.; Wever, R. Inorg. Chim. Acta 2003, 356, 288-296. Hasan, Z.; Renirie, R.; Kerkman, R.; Ruijssenaars, H . J.; Hartog, A . F., Wever, R. J. Biol. Chem. 2006, 281, 9738-9744. Borowski, T.; Szczepanik, W.; Chruszcz, M . ; Broclawik, E. Int. J. Quant. Chem. 2004, 99, 864-875. Zampella, G.; Kravitz, J. Y . ; Webster, C. E.; Fantucci, P.; Hall, M . B . ; Carlson, H . A.; Pecoraro, V . L . ; De Gioia,L. Inorg. Chem. 2004, 43, 41274136. Plass, W.; Pohlmann, A.; Yozgatli, H . P. J. Inorg. Biochem. 2000, 80, 181183. Plass, W. In NIC Symposium 2001; Rollnik, H.; Wolf, D., Eds.; NIC Series; John von Neumann Institut für Computing: Jülich, 2002, Vol. 9, pp 103110. Bangesh, M.; Plass, W. J. Mol Struct. Theochem 2005, 725, 163-175. Zampella, G . ; Fantucci, P.; Pecoraro, V . L.; De Gioia, L. J. Am. Chem. Soc. 2005, 127, 953-960.
In Vanadium: The Versatile Metal; Kustin, Kenneth, et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2007.
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177 19. Kravitz, J. Y.; Pecoraro, V . L . ; Carlson, H. A . J. Chem. Theory Comput. 2005, 1, 1265-1274. 20. Raugei, S.; Carloni, P. J. Phys. Chem. B 2005, 110, 3747. 21. Butler, A . ; Clague,M.J.; Meister, G . E . Chem. Rev. 1994, 94, 625-638. 22. Rehder, D. Coord. Chem. Rev. 1999, 182, 297-322. 23. Ligtenbarg, A. G . J.; Hage, R.; Feringa, B . L. Coord. Chem. Rev. 2003, 237, 89-101. 24. Plass, W.; Pohlmann, A.; Yozgatli, H . P. J. Inorg. Biochem. 2000, 80, 181183. 25. Pohlmann, A.; Plass, W. J. Inorg. Biochem. 2001, 86, 381-381. 26. Plass, W.; Yozgatli, H . P. Z. Anorg. Allg. Chem. 2003, 629, 65-70. 27. Plass, W . Coord. Chem. Rew. 2003, 237, 205-212. 28. Pohlmann, A . ; Nica, S.; Luong, T. K . K.; Plass, W. Inorg. Chem. Commun. 2005, 8, 289-292. 29. Nica, S.; Pohlmann, A . ; Plass, W. Eur. J. Inorg. Chem. 2005, 2032-2036. 30. Becher, J.; Seidel, I.; Plass, W.; Klemm, D. Tetrahedron 2006, 62, 56755681. 31. Hamstra, B . J.; Colpas, G . J.; Pecoraro, V . L . Inorg. Chem. 1998, 37, 949955.
In Vanadium: The Versatile Metal; Kustin, Kenneth, et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2007.
