Role of polarity of the distal pocket in the control of inhibitor binding in dehaloperoxidase-hemoglobin

Biochemistry

Volumn 52, Issue 13, 2013, Pages 2218-2227

  Plummer, Ashlee ^a   Thompson, Matthew K ^b   Franzen, Stefan ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ,4 ,6-TRIBROMOPHENOL; AROMATIC SUBSTRATES; HORSERADISH PEROXIDASE; HYDROPHOBIC AMINO ACIDS; PEROXIDASE ACTIVITIES; SINGLE ELECTRON TRANSFER; STERIC INTERFERENCE; X RAY CRYSTAL STRUCTURES;

AMINO ACIDS; BIOREMEDIATION; BIOTECHNOLOGY; PHENOLS; PORPHYRINS; SUBSTRATES;

ENZYMES;

4 BROMOPHENOL; AROMATIC COMPOUND; DEHALOPEROXIDASE; HALOPHENOL; HEMOGLOBIN; HORSERADISH PEROXIDASE; LEUCINE; PEROXIDASE; UNCLASSIFIED DRUG;

AMPHITRITE ORNATA; ANNELID; ARTICLE; BINDING AFFINITY; BIOREMEDIATION; CATALYSIS; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HEMOGLOBINS; MODELS, MOLECULAR; PEROXIDASES; PHENOLS; POINT MUTATION; POLYCHAETA; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

AMPHITRITE ORNATA; ANNELIDA; ARMORACIA RUSTICANA;

EID: 84875796365     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301509r     Document Type: Article

References (47)

1. Chen, Y. P., Woodin, S. A., Lincoln, D. E., and Lovell, C. R. (1996) An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata J. Biol. Chem. 271, 4609-4612
2. Dunford, B. H. (1999) Heme Peroxidases, John Wiley and Sons, New York.
3. Weber, R. E., Mangum, C., Steinman, H., Bonaventura, C., Sullivan, B., and Bonaventura, J. (1977) Hemoglobins of two terebellid polychaetes: Enoplobranchus sanuineus and Amphitrite ornata Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 179-187
4. Argese, E., Bettiol, C., Giurin, G., and Miana, P. (1999) Quantitative structure-activity relationships for the toxicity of chlorophenols to mammalian submitochondrial particles Chemosphere 38, 2281-2292
5. Godoy, F., Zenteno, P., Cerda, F., Gonzalez, B., and Martinez, M. (1999) Tolerance to trichlorophenols in microorganisms from a polluted and a pristine site of a river Chemosphere 38, 655-662
6. Osborne, R. L., Raner, G. M., Hager, L. P., and Dawson, J. H. (2006) C. fumago Chloroperoxidase is also a Dehaloperoxidase: Oxidative Dehalogenation of Halophenols J. Am. Chem. Soc. 128, 1036-1037
7. Lincoln, D. E., Fielman, K. T., Marinelli, R. L., and Woodin, S. A. (2005) Bromophenol accumulation and sediment contamination by the marine annelids Notomastus lobatus and Thelepus crispus Biochem. Syst. Ecol. 33, 559-570
8. Thompson, M. K., Davis, M. F., de Serrano, V., Nicoletti, F. P., Howes, B. D., Smulevich, G., and Franzen, S. (2010) Internal Binding of Halogenated Phenols in Dehaloperoxidase-Hemoglobin Inhibits Peroxidase Function Biophys. J. 99, 1586-1595
9. Thompson, M. K., Franzen, S., Davis, M. F., Oliver, R. C., and Krueger, J. K. (2011) Dehaloperoxidase-Hemoglobin from Amphitrite ornata Is Primarily a Monomer in Solution J. Phys. Chem. B 115, 4266-4272
10. Han, K., Woodin, S. A., Lincoln, D. E., Fielman, K. T., and Ely, B. (2001) Amphitrite ornata, a marine worm, contains two dehaloperoxidase genes Mar. Biotechnol. 3, 287-292
11. de Serrano, V., D'Antonio, J., Franzen, S., and Ghiladi, R. A. (2010) Structure of dehaloperoxidase B at 1.58 angstrom resolution and structural characterization of the AB dimer from Amphitrite ornata Acta Crystallogr. D66, 529-538
12. D'Antonio, J., D'Antonio, E. L., Thompson, M. K., Bowden, E. F., Franzen, S., Smirnova, T., and Ghiladi, R. A. (2010) Spectroscopic and Mechanistic Investigations of Dehaloperoxidase B from Amphitrite ornata Biochemistry 49, 6600-6616
13. Lebioda, L., LaCount, M. W., Zhang, E., Chen, Y. P., Han, K., Whitton, M. M., Lincoln, D. E., and Woodin, S. A. (1999) An enzymatic globin from a marine worm Nature 401, 445
14. de Serrano, V., D'Antonio, J., Franzen, S., and Ghiladi, R. A. (2010) Crystal structure of dehaloperoxidase B at 1.58 Å and characterization of the A/B dimer from Amphitrite ornata Acta Crystallogr. D66, 529-538
15. LaCount, M. W., Zhang, E. L., Chen, Y. P., Han, K. P., Whitton, M. M., Lincoln, D. E., Woodin, S. A., and Lebioda, L. (2000) The crystal structure and amino acid sequence of dehaloperoxidase from Amphitrite ornata indicate common ancestry with globins J. Biol. Chem. 275, 18712-18716
16. de Serrano, V., Chen, Z. X., Davis, M. F., and Franzen, S. (2007) X-ray crystal structural analysis of the binding site in the ferric and oxyferrous forms of the recombinant heme dehaloperoxidase cloned from Amphitrite ornata Acta Crystallogr. D63, 1094-1101
17. Davis, M. F., Bobay, B. G., and Franzen, S. (2010) Determination of Separate Inhibitor and Substrate Binding Sites in the Dehaloperoxidase- Hemoglobin from Amphitrite ornata Biochemistry 49, 1199-1206
18. Nienhaus, K., Nickel, E., Davis, M. F., Franzen, S., and Nienhaus, G. U. (2008) Determinants of Substrate Internalization in the Distal Pocket of Dehaloperoxidase Hemoglobin of Amphitrite ornata Biochemistry 47, 12985-12994
19. de Serrano, V. and Franzen, S. (2012) Structural Evidence for Stabilization of Inhibitor Binding by a Protein Cavity in the Dehaloperoxidase-Hemoglobin from Amphitrite ornata Biopolymers 98, 27-35
20. Franzen, S., Thompson, M. K., and Ghiladi, R. A. (2012) The Dehaloperoxidase Paradox Biochim. Biophys. Acta 1824, 578-588
21. Thompson, M. K., Franzen, S., Ghiladi, R. A., Reeder, B. J., and Svistunenko, D. A. (2010) Compound ES of Dehaloperoxidase Decays via Two Alternative Pathways Depending on the Conformation of the Distal Histidine J. Am. Chem. Soc. 132, 17501-17510
22. Davis, M. F., Gracz, H., Vendeix, F. A., de Serrano, V., Somasundaram, A., Decatur, S. M., and Franzen, S. (2009) Different Modes of Binding of Mono-, Di-, and Trihalogenated Phenols to the Hemoglobin Dehaloperoxidase from Amphitrite ornata Biochemistry 48, 2164-2172
23. Ferrari, R. P., Laurenti, E., and Trotta, F. (1999) Oxidative 4-dechlorination of 2,4,6-trichlorophenol catalyzed by horseradish peroxidase JBIC, J. Biol. Inorg. Chem. 4, 232-237
24. Laurenti, E., Ghibaudi, E., Ardissone, S., and Ferrari, R. P. (2003) Oxidation of 2,4-dichlorophenol catalyzed by horseradish peroxidase: Characterization of the reaction mechanism by UV-visible spectroscopy and mass spectrometry J. Inorg. Biochem. 95, 171-176
25. de Serrano, V. S., Zhao, J., and Franzen, S. (2013) Structural and kinetic study of an internal substrate binding site of dehaloperoxidase- hemoglobin A from Amphitrite ornata Biochemistry 52, DOI: 10.1021/bi301307f
26. Ma, H., Thompson, M. K., Gaff, J., and Franzen, S. (2010) Kinetic Analysis of a Naturally Occurring Bioremediation Enzyme: Dehaloperoxidase- Hemoglobin from Amphitrite ornata J. Phys. Chem. B 114, 13823-13829
27. Chen, Z., de Serrano, V., Betts, L., and Franzen, S. (2009) Distal histidine conformation flexibility in dehaloperoxidase from Amphitrite ornata Acta Crystallogr. D65, 34-40
28. Sage, J. T., Li, P., and Champion, P. M. (1991) Spectroscopic studies at low pH: Heme ligation kinetics Biochemistry 30, 1237-1247
29. Tian, W. D., Sage, J. T., Srajer, V., and Champion, P. M. (1992) Relaxation dynamics of myoglobin in solution Phys. Rev. Lett. 68, 408-411
30. Heering, H. A., Smith, A. T., and Smulevich, G. (2002) Spectroscopic characterization of mutations at the Phe41 position in the distal haem pocket of horseradish peroxidase C: Structural and functional consequences Biochem. J. 363, 571-579
31. Du, J., Huang, X., Sun, S., Wang, C., Lebioda, L., and Dawson, J. H. (2011) Amphitrite ornata Dehaloperoxidase (DHP): Investigations of Structural Factors That Influence the Mechanism of Halophenol Dehalogenation Using "Peroxidase-like" Myoglobin Mutants and "Myoglobin-like" DHP Mutants Biochemistry 50, 8172-8180
32. Belyea, J., Gilvey, L. B., Davis, M. F., Godek, M., Sit, T. L., Lommel, S. A., and Franzen, S. (2005) Enzyme Function of the Globin Dehaloperoxidase from Amphitrite ornate Is Activated by Substrate Binding Biochemistry 44, 15637-15644
33. Nelson, M. T., Humphrey, W., Gursoy, A., Dalke, A., Kale, L. V., Skeel, R. D., and Schulten, K. (1996) NAMD: A parallel, object oriented molecular dynamics program International Journal of Supercomputer Applications and High Performance Computing 10, 251-268
34. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802
35. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14, 33-38
36. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
37. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
38. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
39. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
40. 2 Occurs by a Radical Mechanism J. Phys. Chem. B 116, 1666-1676
41. Franzen, S., Belyea, J., Gilvey, L. B., Davis, M. F., Chaudhary, C. E., Sit, T. L., and Lommel, S. A. (2006) Proximal cavity, distal histidine and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase Biochemistry 45, 9085-9094
42. Lente, G. and Espenson, J. H. (2004) Unusual Kinetic Role of a Water-Soluble Iron(III) Porphyrin Catalyst in the Oxidation of 2,4,6-Trichlorophenol by Hydrogen Peroxide Int. J. Chem. Kinet. 36, 449-455
43. Nicoletti, F. P., Thompson, M. K., Howes, B. D., Franzen, S., and Smulevich, G. (2010) New Insights into the Role of Distal Histidine Flexibility in Ligand Stabilization of Dehaloperoxidase-Hemoglobin from Amphitrite ornata Biochemistry 49, 1903-1912
44. Nicoletti, F. P., Thompson, M. K., Franzen, S., and Smulevich, G. (2011) Degradation of sulfide by dehaloperoxidase-hemoglobin from Amphitrite ornata JBIC, J. Biol. Inorg. Chem. 16, 611-619
45. Belyea, J., Belyea, C. M., Lappi, S., and Franzen, S. (2006) Resonance Raman Study of Ferric Heme Adducts of Dehaloperoxidase from Amphitrite ornata Biochemistry 45, 14275-14284
46. de Serrano, V. S., Davis, M. F., Gaff, J. F., Zhang, Q., Chen, Z., D'Antonio, E. L., Bowden, E. F., Rose, R., and Franzen, S. (2010) X-ray structure of the metcyano form of dehaloperoxidase from Amphitrite ornata: Evidence for photoreductive dissociation of the iron-cyanide bond Acta Crystallogr. D66, 770-782
47. Laskowski, R. A. (1995) SURFNET: A program for visualizing molecular surfaces, cavities, and intermolecular interactions J. Mol. Graphics 13, 307-308, 323-330