Structural basis for regioselectivity and stereoselectivity of product formation by naphthalene 1,2-dioxygenase

Journal of Bacteriology

Volumn 188, Issue 19, 2006, Pages 6986-6994

  Ferraro, Daniel J ^a   Okerlund, Adam L ^b   Mowers, Jonathan C ^a   Ramaswamy, S ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b University of Iowa   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTOLUENE; ANTHRACENE; AROMATIC COMPOUND; DIOXYGENASE; NAPHTHALENE 1,2 DIOXYGENASE; NITROBENZENE DIOXYGENASE; OXYGENASE; PHENANTHRENE; PHENYLALANINE; RIESKE OXYGENASE; UNCLASSIFIED DRUG; VALINE;

ARTICLE; BACTERIAL STRAIN; CHIRALITY; COMPLEX FORMATION; DEGRADATION; ENZYME ACTIVE SITE; ENZYME ENGINEERING; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; MUTATION; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; PSEUDOMONAS; SOIL POLLUTION; STEREOCHEMISTRY; STRUCTURE ANALYSIS; TECHNIQUE; WILD TYPE;

ANTHRACENES; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MULTIENZYME COMPLEXES; MUTATION; OXYGENASES; PHENANTHRENES; PROTEIN STRUCTURE, QUATERNARY; PSEUDOMONAS; STEREOISOMERISM; SUBSTRATE SPECIFICITY; TOLUENE;

PSEUDOMONAS SP.;

EID: 33749347047     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00707-06     Document Type: Article

References (41)

1. Akhtar, M. N., D. R. Boyd, N. J. Thompson, M. Koreeda, D. T. Gibson, V. Mahadevan, and D. M. Jerina. 1975. Absolute stereochemistry of the dihydroanthracene-cis- and -trans-1,2-diols produced from anthracene by mammals and bacteria. J. Chem. Soc. (Perkin 1) 1975:2506-2511.
2. Anonymous. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50:760-763.
3. Boyd, D. R., and T. D. Bugg. 2006. Arene cis-dihydrodiol formation: from biology to application. Org. Biomol. Chem. 4:181-192.
4. Brown, E. N., and S. Ramaswamy. 2006. Verification of solvent molecules through composite-omit electron density maps. University of Iowa, Iowa City.
5. Carredano, E., A. Karlsson, B. Kauppi, D. Choudhury, R. E. Parales, J. V. Parales, K. Lee, D. T. Gibson, H. Eklund, and S. Ramaswamy. 2000. Substrate binding site of naphthalene 1,2-dioxygenase: functional implications of indole binding. J. Mol. Biol. 296:701-712.
6. DeLano, W. L. 2000. The PyMOL molecular graphics system, 0.98 ed. DeLano Scientific, San Carlos, Calif.
7. Eaton, R. W., and P. J. Chapman. 1992. Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions. J. Bacteriol. 174:7542-7554.
8. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60:2126-2132.
9. Ferraro, D. J., L. Gakhar, and S. Ramaswamy. 2005. Rieske business: structure-function of Rieske non-heme oxygenases. Biochem. Biophys. Res. Commun. 338:175-190.
10. Friemann, R., M. M. Ivkovic-Jensen, D. J. Lessner, C. L. Yu, D. T. Gibson, R. E. Parales, H. Eklund, and S. Ramaswamy. 2005. Structural insight into the dioxygenation of nitroarene compounds: the crystal structure of nitrobenzene dioxygenase. J. Mol. Biol. 348:1139-1151.
11. Furukawa, K., H. Suenaga, and M. Goto. 2004. Biphenyl dioxygenases: functional versatilities and directed evolution. J. Bacteriol. 186:5189-5196.
12. Furusawa, Y., V. Nagarajan, M. Tanokura, E. Masai, M. Fukuda, and T. Senda. 2004. Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J. Mol. Biol. 342:1041-1052.
13. Gakhar, L., Z. A. Malik, C. C. Allen, D. A. Lipscomb, M. J. Larkin, and S. Ramaswamy. 2005. Structure and increased thermostability of Rhodococcus sp. naphthalene 1,2-dioxygenase. J. Bacteriol. 187:7222-7231.
14. Jeffrey, A. M., H. J. Yeh, D. M. Jerina, T. R. Patel, J. F. Davey, and D. T. Gibson. 1975. Initial reactions in the oxidation of naphthalene by Pseudomonas putida. Biochemistry 14:575-584.
15. Jerina, D. M., J. W. Daly, A. M. Jeffrey, and D. T. Gibson. 1971. cis-1,2-Dihydroxy-1,2-dihydronaphthalene: a bacterial metabolite from naphthalene. Arch. Biochem. Biophys. 142:394-396.
16. Jerina, D. M., H. Selander, H. Yagi, M. C. Wells, J. F. Davey, V. Mahadevan, and D. T. Gibson. 1976. Dihydrodiols from anthracene and phenanthrene. J. Am. Chem. Soc. 98:5988-5996.
17. Jones, T. A., J. Y. Zou, S. W. Cowan, and Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47:110-119.
18. Ju, K. S., and R. E. Parales. 2006. Control of substrate specificity by active-site residues in nitrobenzene dioxygenase. Appl. Environ. Microbiol. 72:1817-1824.
19. Karlsson, A., J. V. Parales, R. E. Parales, D. T. Gibson, H. Eklund, and S. Ramaswamy. 2003. Crystal structure of naphthalene dioxygenase: side-on binding of dioxygen to iron. Science 299:1039-1042.
20. Kauppi, B., K. Lee, E. Carredano, R. E. Parales, D. T. Gibson, H. Eklund, and S. Ramaswamy. 1998. Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure 6:571-586.
21. Lamzin, V. S., and K. S. Wilson. 1993. Automated refinement of protein models. Acta Crystallogr. D 49:129-147.
22. Lee, K. 1999. Benzene-induced uncoupling of naphthalene dioxygenase activity and enzyme inactivation by production of hydrogen peroxide. J. Bacteriol. 181:2719-2725.
23. Lee, K., B. Kauppi, R. E. Parales, D. T. Gibson, and S. Ramaswamy. 1997. Purification and crystallization of the oxygenase component of naphthalene dioxygenase in native and selenomethionine-derivatized forms. Biochem. Biophys. Res. Commun. 241:553-557.
24. Lee, K. S., J. V. Parales, R. Friemann, and R. E. Parales. 2005. Active site residues controlling substrate specificity in 2-nitrotoluene dioxygenase from Acidovorax sp. strain JS42. J. Ind. Microbiol. Biotechnol. 32:465-473.
25. Lessner, D. J., G. R. Johnson, R. E. Parales, J. C. Spain, and D. T. Gibson. 2002. Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl. Environ. Microbiol. 68:634-641.
26. Martins, B. M., T. Svetlitchnaia, and H. Dobbek. 2005. 2-Oxoquinoline 8-monooxygenase oxygenase component: active site modulation by Rieske-[2Fe-2S] center oxidation/reduction. Structure 13:817-824.
27. Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53:240-255.
28. Nishino, S. F., and J. C. Spain. 1995. Oxidative pathway for the biodegradation of nitrobenzene by Comamonas sp. strain JS765. Appl. Environ. Microbiol. 61:2308-2313.
29. Parales, R. E. 2003. The role of active-site residues in naphthalene dioxygenase. J. Ind. Microbiol. Biotechnol. 30:271-278.
30. Parales, R. E., N. C. Bruce, A. Schmid, and L. P. Wackett. 2002. Biodegradation, biotransformation, and biocatalysis (b3). Appl. Environ. Microbiol. 68:4699-4709.
31. Parales, R. E., K. Lee, S. M. Resnick, H. Jiang, D. J. Lessner, and D. T. Gibson. 2000. Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J. Bacteriol. 182:1641-1649.
32. Parales, R. E., S. M. Resnick, C. L. Yu, D. R. Boyd, N. D. Sharma, and D. T. Gibson. 2000. Regioselectivity and enantioselectivity of naphthalene dioxygenase during arene cis-dihydroxylation: control by phenylalanine 352 in the alpha subunit. J. Bacteriol. 182:5495-5504.
33. Pflugrath, J. W. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr. D 55:1718-1725.
34. Que, L., Jr. 2000. One motif-many different reactions. Nat. Struct. Biol. 7:182-184.
35. Resnick, S. M., K. Lee, and D. T. Gibson. 1996. Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCBI 9816. J. Ind. Microbiol. Biotechnol. 17:438-457.
36. Stanier, R. Y., N. J. Palleroni, and M. Doudoroff. 1966. The aerobic pseudomonads: a taxonomic study. J. Gen. Microbiol. 43:159-271.
37. Suen, W. C., and D. T. Gibson. 1994. Recombinant Escherichia coli strains synthesize active forms of naphthalene dioxygenase and its individual alpha and beta subunits. Gene 143:67-71.
38. Suen, W. C., B. E. Haigler, and J. C. Spain. 1996. 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase. J. Bacteriol. 178:4926-4934.
39. Wackett, L. P. 1998. Directed evolution of new enzymes and pathways for environmental biocatalysis. Ann. N. Y. Acad. Sci. 864:142-152.
40. Wackett, L. P. 2002. Mechanism and applications of Rieske non-heme iron dioxygenases. Enzyme Microb. Technol. 31:577-587.
41. Yu, C. L., R. E. Parales, and D. T. Gibson. 2001. Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enantioselectivity. J. Ind. Microbiol. Biotechnol. 27:94-103.