Determination of separate inhibitor and substrate binding sites in the dehaloperoxidase-hemoglobin from Amphitrite ornata

Biochemistry

Volumn 49, Issue 6, 2010, Pages 1199-1206

  Davis, Michael F ^a,c   Bobay, Benjamin G ^a,b   Franzen, Stefan ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b North Carolina Research Campus ^*  (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

[CARBONYL; BINDING POCKETS; BROMINATED PHENOLS; DIMER INTERFACE; DISTAL HISTIDINE; DUAL FUNCTION; HALOPHENOLS; MUDFLATS; RESONANCE ASSIGNMENTS; SUBSTRATE-BINDING SITES; X RAY CRYSTAL STRUCTURES;

AMIDES; BINDING ENERGY; BIOCHEMISTRY; HEMOGLOBIN; LOCATION; PHENOLS; PHOSPHATASES; TITRATION;

BINDING SITES;

9 (2,3 DIHYDROXYPROPYL)ADENINE; AMIDE; BROMINE DERIVATIVE; CARBON 13; DEHALOPEROXIDASE HEMOGLOBIN; HALOPHENOL; HEMOGLOBIN; HISTIDINE; PHENOL DERIVATIVE; PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMPHITRITE ORNATA; ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; DEHALOGENATION; ENZYME ASSAY; ESCHERICHIA COLI; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYCHAETA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; TITRIMETRY;

ANIMALS; BENZOMORPHANS; BINDING SITES; CATALYTIC DOMAIN; CHLOROPHENOLS; HEMOGLOBINS; HYDROCARBONS, HALOGENATED; MAGNETIC RESONANCE SPECTROSCOPY; PEROXIDASES; PHENOLS; POLYCHAETA; SPECTROPHOTOMETRY, ULTRAVIOLET; SUBSTRATE SPECIFICITY;

AMPHITRITE ORNATA; ANNELIDA; POLYCHAETA;

EID: 76749095979     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9018576     Document Type: Article

References (44)

1. Han, K. P., 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.
2. de Serrano, V., D'Antonio, J., Thompson, M. K., Franzen, S., and Ghiladi, R. A. (2010) Crystal structure of dehaloperoxidase B at 1.58 Å and structural characterization of the A/B dimer from Amphitrite ornata, J. Biol. Chem. (submitted for publication).
3. D'Antonio, J., D'Antonio, E. L., Bowden, E. F., Smirnova, T. S., Franzen, S. F., and Ghiladi, R. A. (2010) Spectroscopic and mechanistic investigations of dehaloperoxidase B from Amphitrite ornata, J. Biol. Chem. (submitted for publication).
4. Chen, Z., De Serrano, V., Betts, L., and Franzen, S. (2009) Distal histidine conformational flexibility in dehaloperoxidase from Amphitrite ornata. Acta Crystallogr., Sect. D: Biol. Crystallogr. 65, 34-40.
5. 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., Sect. D: Biol. Crystallogr. 63, 1094-1101.
6. 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.
7. Weber, R. E., Mnum, C. P., Steinman, H., Bonaventura, C., Sullivan, B., and Bonaventura, J. (1977) Hemoglobins of two terebellid polychaetes: Enoplobranchus sanuigneus and Amphitire ornata. Comp. Biochem. Physiol. 56A, 179-187.
8. 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 ornata is activated by substrate binding. Biochemistry 44, 15637-15644.
9. Franzen, S., Gilvey, L. B., and Belyea, J. L. (2007) The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata. Biochim. Biophys. Acta 1774, 121-130.
10. Franzen, S., Chaudhary, C., Belyea, J., Gilvey, L., Davis, M. F., 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.
11. 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.
12. Nienhaus, K., Deng, P. C., Belyea, J., Franzen, S., and Nienhaus, G. U. (2006) Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata. J. Phys. Chem. B 110, 13264-13276.
13. Davis, M. F., Gracz, H., Vendeix, F. A. P., 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.
14. Zhang, E., Chen, Y. P., Roach, M. P., Lincoln, D. E., Lovell, C. R., Woodin, S. A., Dawson, J. H., and Lebioda, L. (1996) Crystallization and initial spectroscopic characterization of the heme-containing dehaloperoxidase from the marine polychaete Amphitrite ornata. Acta Crystallogr., Sect. D 52, 1191-1193.
15. 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 (DOI: 10.1021/bi9020567).
16. 2 bonding in myoglobin and hemoglobin: A new molecular paradigm. Prog. Biophys. Mol. Biol. 91, 83-162.
17. Fielman, K. T., Woodin, S. A., and Lincoln, D. E. (2001) Polychaete indicator species as a source of natural halogenated organic compounds in marine sediments. Environ. Toxicol. Chem. 20, 738-747.
18. Fielman, K. T., Woodin, S. A., Walla, M. D., and Lincoln, D. E. (1999) Widespread occurrence of natural halogenated organics among temperate marine infauna. Mar. Ecol.: Prog. Ser. 181, 1-12.
19. Woodin, S. A., Lindsay, S. M., and Lincoln, D. E. (1997) Biogenic bromophenols as negative recruitment cues. Mar. Ecol.: Prog. Ser. 157, 303-306.
20. 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. Systemat. Ecol. 33, 559-570.
21. Osborne, R. L., Taylor, L. O., Han, K. P., Ely, B., and Dawson, J. H. (2004) Amphitrite ornata dehaloperoxidase: Enhanced activity for the catalytically active globin using MCPBA. Biochem. Biophys. Res. Commun. 324, 1194-1198.
22. Feducia, J., Dumarieh, R., Gilvey, L. B. G., Smirnova, T., Franzen, S., and Ghiladi, R. A. (2009) Characterization of dehaloperoxidase compound ES and its reactivity with trihalophenols. Biochemistry 48, 995-1005.
23. Smirnova, T. I., Weber, R. T., Davis, M. F., and Franzen, S. (2008) Substrate binding triggers a switch in the iron coordination in dehaloperoxidase from Amphitrite ornata: HYSCORE experiments. J. Am. Chem. Soc. 130, 2128-2129.
24. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
25. Goddard, T. D., and Kneller, D. G. SPARKY 3, University of California, San Francisco.
26. Kordys, D. R., Bobay, B. G., Thompson, R. J., Venters, R. A., and Cavanah, J. (2007) Peptide binding proclivities of calcium loaded calbindin-D28k. FEBS Lett. 581, 4778-4782.
27. Palmer, S. M., Schaller, M. D., and Campbell, S. L. (2008) Vinculin tail conformation and self-association is independent of pH and H906 protonation. Biochemistry 47, 12467-12475.
28. Chaudhary, C. (2003) Functional studies of the push-pull mechanism in dehaloperoxidase from Amphitrite ornata, Master's Thesis, North Carolina State University.
29. Ator, M. A., and Ortiz de Montellano, P. R. (1987) Protein control of prosthetic heme reactivity: Reaction of substrates with the heme edge of horseradish peroxidase. J. Biol. Chem. 262, 1542-1551.
30. Pogni, R., Baratto, M. C., Giansanti, S., Teutloff, C., Verdin, J., Valderrama, B., Lendzian, F., Lubitz, W., Vazquez-Duhalt, R., and Basosi, R. (2005) Tryptophan-based radical in the catalytic mechanism of versatile peroxidase from Bjerkandera adusta. Biochemistry 44, 4267-4274.
31. Royer, W. E., Hendrickson, W. A., and Chiancone, E. (1990) Structural transitions upon ligand-binding in a cooperative dimeric hemoglobin. Science 249, 518-521.
32. Royer, W. E., Pardanani, A., Gibson, Q. H., Peterson, E. S., and Friedman, J. M. (1996) Ordered water molecules as key allosteric mediators in a cooperative dimeric hemoglobin. Proc. Natl. Acad. Sci. U.S.A. 93, 14526-14531.
33. Knapp, J. E., Bonham, M. A., Gibson, Q. H., Nichols, J. C., and Royer, W. E. (2005) Residue F4 plays a key role in modulating oxygen affinity and cooperativity in Scapharca dimeric hemoglobin. Biochemistry 44, 14419-14430.
34. Doyle, W. A., Blodig, W., Veitch, N. C., Piontek, K., and Smith, A. T. (1998) Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis. Biochemistry 37, 15097-15105.
35. Perez-Boada, M., Ruiz-Duenas, F. J., Pogni, R., Basosi, R., Choinowski, T., Martinez, M. J., Piontek, K., and Martinez, A. T. (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: Site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways. J. Mol. Biol. 354, 385-402.
36. Ruiz-Duenas, F. J., Pogni, R., Morales, M., Giansanti, S., Mate, M. J., Romero, A., Martinez, M. J., Basosi, R., and Martinez, A. T. (2009) Protein radicals in fungal versatile peroxidase: Catalytic tryptophan radical in both compound I and compound II and studies on W164Y, W164H, and W164S variants. J. Biol. Chem. 284, 7986-7994.
37. Sivaraja, M., Goodin, D. B., Smith, M., and Hoffman, B. M. (1989) Identification by ENDOR of Trp191 as the free-radical site in cytochrome-c peroxidase compound ES. Science 245, 738-740.
38. Gunther, M. R. (2004) Probing the free radicals formed in the metmyoglobin-hydrogen peroxide reaction. Free Radical Biol. Med. 36, 1345-1354.
39. Mason, R. P. (2004) Using anti-5,5-dimethyl-1-pyrroline N-oxide to detect protein radicals in time and space with immuno-spin trapping. Free Radical Biol. Med. 36, 1214-1223.
40. Bhattacharjee, S., Deterding, L. J., Jiang, J., Bonini, M. G., Tomer, K. B., Ramirez, D. C., and Mason, R. P. (2007) Electron transfer between a tyrosyl radical and a cysteine residue in hemoproteins: Spin trapping analysis. J. Am. Chem. Soc. 129, 13493-13501.
41. La Mar, G. N., and de Ropp, J. S. (1993) in Biological Magnetic Resonance, pp 1-73, Plenum Press, New York.
42. La Mar, G. N. (2007) Application of the paramagnetic dipole field for solution NMR active site structure determination in low-spin, cyanide-inhibited ferric hemoproteins. IUBMB Life 59, 513-527.
43. La Mar, G. N., Chen, Z., Vyas, K., and McPherson, A. D. (1995) An interpretive bases of the hyperfine shifts in cyanide-inhibited horse-radish peroxidase based on the magnetic axes and ligand tilt. Influence of substrate binding and extensions to other peroxidases. J. Am. Chem. Soc. 117, 411-419.
44. Zhu, W., Li, Y., Wang, J., Ortiz de Montellano, P. R., and La Mar, G. N. (2006) Solution NMR study of environmental effects on substrate seating in human heme oxygenase: Influence of polypeptide truncation, substrate modification and axial ligand. J. Inorg. Biochem. 100, 97-107.