Internal binding of halogenated phenols in dehaloperoxidase-hemoglobin inhibits peroxidase function

Biophysical Journal

Volumn 99, Issue 5, 2010, Pages 1586-1595

  Thompson, Matthew K ^a   Davis, Michael F ^a,b,c   Serrano, Vesna De ^a   Nicoletti, Francesco P ^d   Howes, Barry D ^d   Smulevich, Giulietta ^d   Franzen, Stefan ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

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

^d UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHITRITE ORNATA; ANNELIDA;

EID: 77955257385     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.05.041     Document Type: Article

References (53)

1. Lebioda, L., M. W. LaCount., S. A. Woodin. 1999. An enzymatic globin from a marine worm. Nature. 401:445. (Pubitemid 129515774)
2. Weber, R. E., C. Mangum., J. Bonaventura. 1977. Hemoglobins of two terebellid polychaetes: Enoplobranchus sanguineus and Amphitrite ornata. Comp. Biochem. Physiol. Comp. Physiol. 56:179-187.
3. Chen, Y. P., S. A. Woodin., C. R. Lovell. 1996. An unusual dehalogenating peroxidase from the marine terebellid polychaete Amphitrite ornata. J. Biol. Chem. 271:4609-4612.
4. Reference deleted in proof.
5. Han, K., S. A. Woodin., B. Ely. 2001. Amphitrite ornata, a marine worm, contains two dehaloperoxidase genes. Mar. Biotechnol. 3:287-292.
6. de Sorrano, V., J. D'Antonio., R. A. Ghiladi. 2010. Crystal structure of dehaloperoxidase B at 1.58 A and characterization of the A/B dimer from Amphitrite ornata. Acta Crystallogr. D Biol. Crystallogr. 66:529-538.
7. Goodin, D. B., and D. E. McRee. 1993. The Asp-His-Fe triad of cytochrome c peroxidase controls the reduction potential, electronic structure, and coupling of the tryptophan free radical to the heme. Biochemistry. 32:3313-3324.
8. Spiro, T. G., G. Smulevich, and C. Su. 1990. Probing protein structure and dynamics with resonance Raman spectroscopy: cytochrome c peroxidase and hemoglobin. Biochemistry. 29:4497-4508.
9. Perutz, M. F., A. J. Wilkinson., G. G. Dodson. 1998. The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27:1-34.
10. Chen, Y. R., L. J. Deterding., R. P. Mason. 2000. Nature of the inhibition of horseradish peroxidase and mitochondrial cytochrome c oxidase by cyanyl radical. Biochemistry. 39:4415-4422.
11. Zatón, A. M., and E. Ochoa de Aspuru. 1995. Horseradish peroxidase inhibition by thiouracils. FEBS Lett. 374:192-194.
12. Ziemys, A., and J. Kulys. 2005. Heme peroxidase clothing and inhibition with polyphenolic substances revealed by molecular modeling. Comput. Biol. Chem. 29:83-90.
13. de Serrano, V., Z. Chen., S. Franzen. 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. D Biol. Crystallogr. 63:1094-1101.
14. Chen, Z., V. de Serrano., S. Franzen. 2009. Distal histidine conformational flexibility in dehaloperoxidase from Amphitrite ornata. Acta Crystallogr. D Biol. Crystallogr. 65:34-40.
15. Yang, F., and G. N. Phillips, Jr. 1996. Crystal structures of CO-, deoxyand met-myoglobins at various pH values. J. Mol. Biol. 256:762-774.
16. Nicoletti, F. P., M. K. Thompson., G. Smulevich. 2010. New insights into the role of distal histidine flexibility in ligand stabilization of dehaloperoxidase-hemoglobin from Amphitrite ornata. Biochemistry. 49:1903-1912.
17. Davis, M. F., H. Gracz., S. Franzen. 2009. Different modes of binding of mono-, di-, and trihalogenated phenols to the hemoglobin dehaloperoxidase from Amphitrite ornata. Biochemistry. 48:2164-2172.
18. Davis, M. F., B. G. Bobay, and S. Franzen. 2010. Determination of separate inhibitor and substrate binding sites in the dehaloperoxidase- hemoglobin from Amphitrite ornata. Biochemistry. 49:1199-1206.
19. Tippett, P. S., and K. E. Neet. 1982. An allosteric model for the inhibition of glucokinase by long chain acyl coenzyme A. J. Biol. Chem. 257:12846-12852.
20. Hu, D. D., C. A. White., J. W. Smith. 1999. A new model of dual interacting ligand binding sites on integrin αIIbβ3. J. Biol. Chem. 274:4633-4639.
21. Tran, K. L., P. A. Aronov., C. Morisseau. 2005. Lipid sulfates and sulfonates are allosteric competitive inhibitors of the N-terminal phosphatase activity of the mammalian soluble epoxide hydrolase. Biochemistry. 44:12179-12187.
22. Horton, H. R., L. A. Morton., D. Rawn. 2006. Principles of Biochemistry. Pearson Prentice Hall, Upper Saddle River, NJ.
23. Johnson, J. B., D. C. Lamb., R. D. Young. 1996. Ligand binding to heme proteins. VI. Interconversion of taxonomic substates in carbonmonoxymyoglobin. Biophys. J. 71:1563-1573.
24. Tian, W. D., J. T. Sage, and P. M. Champion. 1993. Investigations of ligand association and dissociation rates in the "open" and "closed" states of myoglobin. J. Mol. Biol. 233:155-166.
25. Otwinowski, Z., and W. Minor. 1997. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
26. McCoy, A. J., R. W. Grosse-Kunstleve., R. J. Read. 2007. Phaser crystallographic software. J. Appl. Cryst. 40:658-674.
27. Krissinel, E. B., M. D. Winn., P. Emsley. 2004. The new CCP4 Coordinate Library as a toolkit for the design of coordinate-related applications in protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 60:2250-2255.
28. Potterton, L., S. McNicholas., M. Noble. 2004. Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60:2288-2294.
29. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
30. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
31. Collaborative Computational Project, Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
32. Brünger, A. T., P. D. Adams., G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
33. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD-Visual Molecular Dynamics. J. Mol. Graph. 14:33-38.
34. Fermi, G., M. F. Perutz., R. Fourme. 1984. The crystal structure of human deoxyhaemoglobin at 1.74 A resolution. J. Mol. Biol. 175:159-174.
35. Harrington, D. J., K. Adachi, and W. E. Royer, Jr. 1997. The high resolution crystal structure of deoxyhemoglobin S. J. Mol. Biol. 272:398-407.
36. Schlichting, I., J. Berendzen., R. M. Sweet. 1994. Crystal structure of photolysed carbonmonoxy-myoglobin. Nature. 371:808-812.
37. Nienhaus, K., P. Deng., G. U. Nienhaus. 2006. Spectroscopic study of substrate binding to the carbonmonoxy form of dehaloperoxidase from Amphitrite ornata. J. Phys. Chem. B. 110:13264-13276.
38. Smirnova, T. I., R. T. Weber., S. Franzen. 2008. Substrate binding triggers a switch in the iron coordination in dehaloperoxidase from Amphitrite ornata: HYSCORE experiments. J. Am. Chem. Soc. 130:2128-2129.
39. Feducia, J., R. Dumarieh., R. A. Ghiladi. 2009. Characterization of dehaloperoxidase compound ES and its reactivity with trihalophenols. Biochemistry. 48:995-1005.
40. Sivaraja, M., D. B. Goodin., B. M. Hoffman. 1989. Identification by ENDOR of Trp191 as the free-radical site in cytochrome c peroxidase compound ES. Science. 245:738-740.
41. Tilton, Jr., R. F., I. D. Kuntz, Jr., and G. A. Petsko. 1984. Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 A. Biochemistry. 23:2849-2857.
42. Franzen, S., J. Belyea., S. A. Lommel. 2006. Proximal cavity, distal histidine, and substrate hydrogen-bonding mutations modulate the activity of Amphitrite ornata dehaloperoxidase. Biochemistry. 45:9085-9094.
43. Franzen, S., L. B. Gilvey, and J. L. Belyea. 2007. The pH dependence of the activity of dehaloperoxidase from Amphitrite ornata. Biochim. Biophys. Acta. 1774:121-130.
44. Dodgson, K. S., J. N. Smith, and R. T. Williams. 1950. Studies in detoxication. 29. The orientation of glucuronic acid conjugation in chloroquinol. Biochem. J. 46:124-128.
45. Kortum, G., W. Vogel, and K. Andrussow. 1961. Dissociation constants of organic acids in aqueous solution. Pure Appl. Chem. 1:190-536.
46. Varadarajan, R., T. E. Zewert., S. G. Boxer. 1989. Effects of buried ionizable amino acids on the reduction potential of recombinant myoglobin. Science. 243:69-72.
47. Gilvey, L. B. 2006. Kinetic studies of dehaloperoxidase-hemoglobin from Amphitrite ornata. MS thesis. North Carolina State University, Raleigh, North Carolina.
48. Dawson, J. H. 1988. Probing structure-function relations in heme-containing oxygenases and peroxidases. Science. 240:433-439.
49. Poulos, T. L. 1988. Heme enzyme crystal structures. Adv. Inorg. Biochem. 7:1-36.
50. Poulos, T. L., and J. Kraut. 1980. The stereochemistry of peroxidase catalysis. J. Biol. Chem. 255:8199-8205.
51. Belyea, J., L. B. Gilvey., S. Franzen. 2005. Enzyme function of the globin dehaloperoxidase from Amphitrite ornata is activated by substrate binding. Biochemistry. 44:15637-15644.
52. Lincoln, D. E., K. T. Fielman., S. A. Woodin. 2005. Bromophenol accumulation and sediment contamination by the marine annelids Notomastus lobatus and Thelepus crispus. Biochem. Syst. Ecol. 33:559-570.
53. Chen, Y. P., D. E. Lincoln., C. R. Lovell. 1991. Purification and properties of a unique flavin-containing chloroperoxidase from the capitellid polychaete Notomastus lobatus. J. Biol. Chem. 266:23909-23915.