Observation of an unusual electronically distorted semiquinone radical of PCB metabolites in the active site of prostaglandin H synthase-2

Chemosphere

Volumn 81, Issue 11, 2010, Pages 1501-1508

  Wangpradit, Orarat ^a   Moman, Edelmiro ^b   Nolan, Kevin B ^c   Buettner, Garry R ^a   Robertson, Larry W ^a   Luthe, Gregor ^a,d  

^a UNIVERSITY OF IOWA   (United States)

^b ProSciens   (Luxembourg)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d SAXION UNIVERSITY OF APPLIED SCIENCES   (Netherlands)

Author keywords

Ab initio; Airborne polychlorinated biphenyls (PCBs); Electron paramagnetic resonance (EPR) spectroscopy; Human recombinant prostaglandin H synthase 2 (hPGHS 2); In silico molecular docking model; Semiquinone radicals

Indexed keywords

BIOMOLECULES; CHEMICAL ACTIVATION; ELECTRON RESONANCE; ELECTRON SPIN RESONANCE SPECTROSCOPY; LIPIDS; METABOLITES; MOLECULAR MODELING; PARAMAGNETIC RESONANCE; PARAMAGNETISM; POLYCHLORINATED BIPHENYLS; PRINTED CIRCUIT BOARDS; QUANTUM THEORY;

AB INITIO; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DOCKING; POLYCHLORINATED BIPHENYL (PCBS); SEMIQUINONE RADICALS; SYNTHASES;

ORGANIC POLLUTANTS;

4 CHLOROBIPHENYL 2',5' HYDROQUINONE; 4 CHLOROBIPHENYL 2',5'SEMIQUINONE RADICAL; ARACHIDONATE POTASSIUM; ARACHIDONIC ACID; CARBOXYLIC ACID; FLUORINE; FLURBIPROFEN; FREE RADICAL; GLYCEROL; HEMATIN; PEROXIDASE; POLYCHLORINATED BIPHENYL; PRONASE; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE 2; SEMIQUINONE; UNCLASSIFIED DRUG;

CARBOXYLIC ACID; ELECTROKINESIS; ELECTRON; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; FLUORINE; METABOLITE; MOLECULAR ANALYSIS; NUMERICAL MODEL; OBSERVATIONAL METHOD; OXIDATION; PCB; PERTURBATION; RADICAL; RECOMBINATION; VISCOSITY;

ARTICLE; BIOCATALYSIS; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ELECTRONICS; ENZYME ACTIVE SITE; METABOLIC ACTIVATION; METABOLITE; MOLECULAR DOCKING; OXIDATION; QUANTUM MECHANICS; STEREOSPECIFICITY; VISCOSITY;

EID: 78249244466     PISSN: 00456535     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2010.08.041     Document Type: Article

References (63)

1. Amaro A.R., Oakley G.G., Bauer U., Spielmann H.P., Robertson L.W. Metabolic activation of PCBs to quinones: reactivity toward nitrogen and sulfur nucleophiles and influence of superoxide dismutase. Chem. Res. Toxicol. 1996, 9:623-629.
2. Bader R.F.W. Atoms in Molecules: A Quantum Theory 1982, Oxford University Press, Oxford.
3. Biegler-Konig F.W., Bader R.F.W., Tang T.H. Calculation of the average properties of atoms in molecules II. J. Comput. Chem. 1982, 13:317-328.
4. Blinder S.M. An exactly solvable model for the Fermi contact interaction. Theor. Chim. Acta. 1979, 53:159-163.
5. Bolton J.L., Trush M.A., Penning T.M., Dryhurst G., Monks T.J. Role of quinones in toxicology. Chem. Res. Toxicol. 2000, 13:135-160.
6. Brown J.R. Structure of bovine serum albumin. Fed. Proc. 1975, 34:591.
7. Carabaza A., Cabre F., Rotllan E., Gomez M., Gutierrez M., Garcia M.L., Mauleon D. Stereoselective inhibition of inducible cyclooxygenase by chiral nonsteroidal antiinflammatory drugs. J. Clin. Pharmacol. 1996, 36:505-512.
8. Carter C.D., Ho J.X. Structure of serum albumin. Advances in Protein Chemistry 1994, 153-203. Academic Press, NY. V.N. Schumacker (Ed.).
9. Chubb A.J., Fitzgerald D.J., Nolan K.B., Moman E. The productive conformation of prostaglandin G2 at the peroxidase site of prostaglandin endoperoxide H synthase: docking, molecular dynamics, and site-directed mutagenesis studies. Biochemistry 2006, 45:811-820.
10. Duan Y., Wu C., Chowdhury S., Lee M.C., Xiong G., Zhang W., Yang R., Cieplak P., Luo R., Lee T., Caldwell J., Wang J., Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 2003, 24:1999-2012.
11. Duling D.R. Simulation of multiple isotropic spin-trap EPR spectra. J. Magn. Reson. 1994, 104:105-110.
12. Dunbrack R.L. Rotamer libraries in the 21st century. Curr. Opin. Struct. Biol. 2002, 12:431-440.
13. Fernandez M.F., Kiviranta H., Molina-Molina J.M., Laine O., Lopez-Espinosa M.J., Vartiainen T., Olea N. Polychlorinated biphenyls (PCBs) and hydroxy-PCBs in adipose tissue of women in Southeast Spain. Chemosphere 2008, 71:1196-1205.
14. Freed J.H. Theory of slow tumbling ESR spectra for nitroxides. Spin Labeling: Theory and Applications 1976, 53-132. Academic Press, NY. L.J. Berliner (Ed.).
15. Gordon M.S., Schmidt M.W. Advances in electronic structure theory: GAMESS a decade later. Theory and Applications of Computational Chemistry, the First Forty Years 2005, 1167-1189. Elsevier, Amsterdam, The Netherlands. C.E. Dykstra, G. Frenking, K.S. Kim, G.E. Scuseria (Eds.).
16. Gupta K., Selinsky B.S., Kaub C.J., Katz A.K., Loll P.J. The 2.0 A resolution crystal structure of prostaglandin H2 synthase-1: structural insights into an unusual peroxidase. J. Mol. Biol 2004, 335:503-518.
17. Gutowsky H.S., Holm C. Rate processes and nuclear magnetic resonance spectra, II: hindered internal rotation of amides. Chem. Phys. 1956, 25:1228-1234.
18. Halgren T.A. Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J. Comput. Chem. 1996, 17:490-519.
19. Hansen L.G. The ortho Side of PCBs: Occurence and Disposition 1999, Kluwer Academic Publishers, Norwell, MA.
20. Hsia L.C., Wong L.T., Tan C.T., Kharouba S.S., Balaskas E., Tinker D.O., Feldhoff R.C. Bovine serum albumin: characterization of a fatty acid binding site on the N-terminal peptic fragment using a new spin-label. Biochemistry 1984, 23:5930-5932.
21. Hsuanyu Y.C., Dunford H.B. Reduction of prostaglandin H synthase compound II by phenol and hydroquinone, and the effect of indomethacin. Arch. Biochem. Biophys. 1992, 292:213-220.
22. Huey R., Morris G.M., Olson A.J., Goodsell D.S. A semiempirical free energy force field with charge-based desolvation. J. Comput. Chem. 2007, 28:1145-1152.
23. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 1996, 14(33-38):27-38.
24. Hyde J.S., Thomas D.D. New EPR methods for the study of very slow motion: application to spin-labeled hemoglobin. Ann. N. Y. Acad. Sci. 1973, 222:680-692.
25. Jakalian A., Jack D.B., Bayly C.I. Fast, efficient generation of high-quality atomic charges. AM1-BCC model: II. Parameterization and validation. J. Comput. Chem. 2002, 23:1623-1641.
26. James M.O. Polychlorinated biphenyls: metabolism and metabolites. PCBs: Recent Advances in Environmental Toxicology and Health Effects 2001, 35-46. University Press of Kentucky, Lexington, KY. L.W. Robertson, L.G. Hansen (Eds.).
27. Karasek L., Hajslova J., Rosmus J., Huhnerfuss H. Methylsulfonyl PCB and DDE metabolites and their enantioselective gas chromatographic separation in human adipose tissues, seal blubbler and pelican muscle. Chemosphere 2007, 67:S22-S27.
28. Keith, T.A., 2009. AIMII (version 09.02.01). http://aim.tkgristmill.com.
29. Kulmacz R.J. Prostaglandin H synthase and hydroperoxides: peroxidase reaction and inactivation kinetics. Arch. Biochem. Biophys. 1986, 249:273-285.
30. Kurumbail R.G., Stevens A.M., Gierse J.K., McDonald J.J., Stegeman R.A., Pak J.Y., Gildehaus D., Miyashiro J.M., Penning T.D., Seibert K., Isakson P.C., Stallings W.C. Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 1996, 384:644-648.
31. Luthe G., Garcia Boy R., Jacobus J., Smith B.J., Rahaman A., Robertson L.W., Ludewig G. Xenobiotic geometry and media pH determine cytotoxicity through solubility. Chem. Res. Toxicol. 2008, 21:1017-1027.
32. Luthe G., Swenson D.C., Robertson L.W. Influence of fluoro-substitution on the planarity of 4-chlorobiphenyl (PCB 3). Acta. Cryst. 2007, B63:319-327.
33. Marnett L.J. Cyclooxygenase mechanisms. Curr. Opin. Chem. Biol. 2000, 4:545-552.
34. Marnett L.J., Johnson J.T., Bienkowski M.J. Arachidonic acid-dependent metabolism of 7,8-dihydroxy-7,8-dihydro-benzo[a]pyrene by ram seminal vesicles. FEBS Lett. 1979, 106:13-16.
35. Marnett L.J., Rowlinson S.W., Goodwin D.C., Kalgutkar A.S., Lanzo C.A. Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. J. Biol. Chem. 1999, 274:22903-22906.
36. Mayer M., Mayer B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew. Chem. Int. Ed. 1999, 38:1784-1788.
37. McLean M.R., Bauer U., Amaro A.R., Robertson L.W. Identification of catechol and hydroquinone metabolites of 4-monochlorobiphenyl. Chem. Res. Toxicol. 1996, 9:158-164.
38. Monks T.J., Jones D.C. The metabolism and toxicity of quinones, quinonimines, quinone methides, and quinone-thioethers. Curr. Drug Metab. 2002, 3:425-438.
39. Morris G.M., Goodsell D.S., Halliday R.S., Huey R., Hart W.E., Belew R.K., Olson A.J. Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 1998, 19:1639-1662.
40. NIEHS EPR-WinSim 2002. Public Electron Paramagnetic Resonance Software Tools 2002, National Institute of Environmental Health Sciences, Research Triangle Park, NC.
41. Nilsson K., Hersleth H.P., Rod T.H., Andersson K.K., Ryde U. The protonation status of compound II in myoglobin, studied by a combination of experimental data and quantum chemical calculations: quantum refinement. Biophys. J. 2004, 87:3437-3447.
42. O'Brien P.J. Molecular mechanisms of quinone cytotoxicity. Chem. Biol. Interact. 1991, 80:1-41.
43. Oakley G.G., Devanaboyina U., Robertson L.W., Gupta R.C. Oxidative DNA damage induced by activation of polychlorinated biphenyls (PCBs): implications for PCB-induced oxidative stress in breast cancer. Chem. Res. Toxicol. 1996, 9:1285-1292.
44. Oakley G.G., Robertson L.W., Gupta R.C. Analysis of polychlorinated biphenyl-DNA adducts by 32P-postlabeling. Carcinogenesis 1996, 17:109-114.
45. Park J.S., Bergman A., Linderholm L., Athanasiadou M., Kocan A., Petrik J., Drobna B., Trnovec T., Charles M.J., Hertz-Picciotto I. Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia. Chemosphere 2008, 70:1676-1684.
46. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
47. Robertson L.W., Hansen L.G. PCBs: Recent Advances in Environmental Toxicology and Health Effects 2001, University Press of Kentucky, Lexington, KY.
48. Rouzer C.A., Marnett L.J. Mechanism of free radical oxygenation of polyunsaturated fatty acids by cyclooxygenases. Chem. Rev. 2003, 103:2239-2304.
49. Sabljic A. QSAR models for estimating properties of persistent organic pollutants required in evaluation of their environmental fate and risk. Chemosphere 2001, 43:363-375.
50. Sanner M.F. Python: a programming language for software integration and development. J. Mol. Graphics Modell. 1999, 17:57-61.
51. Schmidt M.W., Baldridge K.K., Boatz J.A., Elbert S.T., Gordon M.S., Jensen J.J., Koseki S., Matsunaga N., Nguyen K.A., Su S., Windus T.L., Dupuis M. General atomic and molecular electronic structure system. J. Comput. Chem. 1993, 14:1347-1363.
52. Seifert A., Tatzel S., Schmid R.D., Pleiss J. Multiple molecular dynamics simulations of human p450 monooxygenase CYP2C9: the molecular basis of substrate binding and regioselectivity toward warfarin. Proteins 2006, 64:147-155.
53. Shao Y., Molnar L.F., Jung Y., Kussmann J., Ochsenfeld C., Brown S.T., Gilbert A.T., Slipchenko L.V., Levchenko S.V., O'Neill D.P., DiStasio R.A., Lochan R.C., Wang T., Beran G.J., Besley N.A., Herbert J.M., Lin C.Y., Van Voorhis T., Chien S.H., Sodt A., Steele R.P., Rassolov V.A., Maslen P.E., Korambath P.P., Adamson R.D., Austin B., Baker J., Byrd E.F., Dachsel H., Doerksen R.J., Dreuw A., Dunietz B.D., Dutoi A.D., Furlani T.R., Gwaltney S.R., Heyden A., Hirata S., Hsu C.P., Kedziora G., Khalliulin R.Z., Klunzinger P., Lee A.M., Lee M.S., Liang W., Lotan I., Nair N., Peters B., Proynov E.I., Pieniazek P.A., Rhee Y.M., Ritchie J., Rosta E., Sherrill C.D., Simmonett A.C., Subotnik J.E., Woodcock H.L., Zhang W., Bell A.T., Chakraborty A.K., Chipman D.M., Keil F.J., Warshel A., Hehre W.J., Schaefer H.F., Kong J., Krylov A.I., Gill P.M., Head-Gordon M. Advances in methods and algorithms in a modern quantum chemistry program package. Phys. Chem. Chem. Phys. 2006, 8:3172-3191.
54. Smith W.L., Dewitt D.L., Garavito R.M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 2000, 69:145-182.
55. Song Y., Buettner G.R. Thermodynamic and kinetic considerations for the reaction of semiquinone radicals to form superoxide and hydrogen peroxide. Free Radical Biol. Med. 2010, 49:919-962.
56. Song Y., Wagner B.A., Lehmler H.J., Buettner G.R. Semiquinone radicals from oxygenated polychlorinated biphenyls: electron paramagnetic resonance studies. Chem. Res. Toxicol. 2008, 21:1359-1367.
57. Song Y., Wagner B.A., Witmer J.R., Lehmler H.J., Buettner G.R. Nonenzymatic displacement of chlorine and formation of free radicals upon the reaction of glutathione with PCB quinones. Proc. Natl. Acad. Sci. USA. 2009, 106:9725-9730.
58. Srinivasan A., Lehmler H.J., Robertson L.W., Ludewig G. Production of DNA strand breaks in vitro and reactive oxygen species in vitro and in HL-60 cells by PCB metabolites. Toxicol. Sci. 2001, 60:92-102.
59. Stewart, J.P., 2007. MOPAC2007. Stewart Computational Chemistry, Colorado Springs, CO. http://openmopac.net.
60. Trop M., Birk K. The specificity of proteinases from Streptomyces griseus (pronase). Biochem. J. 1970, 116:19-25.
61. Wang J., Wang W., Kollman P.A., Case D.A. Automatic atom type and bond type perception in molecular mechanical calculations. J. Mol. Graphics Modell. 2006, 25:247-260.
62. Wangpradit O., Mariappan S.V., Teesch L.M., Duffel M.W., Norstrom K., Robertson L.W., Luthe G. Oxidation of 4-chlorobiphenyl metabolites to electrophilic species by prostaglandin H synthase. Chem. Res. Toxicol. 2009, 22:64-71.
63. Wania F., Mackay D. Tracking the distribution of persistent organic pollutants. Environ. Sci. Technol. 1996, 30:390A-396A.