Structural insight into the dioxygenation of nitroarene compounds: The crystal structure of nitrobenzene dioxygenase

Journal of Molecular Biology

Volumn 348, Issue 5, 2005, Pages 1139-1151

  Friemann, Rosmarie ^a   Ivkovic Jensen, Maja M ^b   Lessner, Daniel J ^b   Yu, Chi Li ^b   Gibson, David T ^b   Parales, Rebecca E ^c   Eklund, Hans ^a   Ramaswamy, S ^d  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Crystal structure; Nitroarene; Nitrobenzene dioxygenase; Rieske non heme dioxygenase; Substrate specificity

Indexed keywords

3 NITROTOLUENE; AROMATIC NITRO COMPOUND; ASPARAGINE; CARBON; HYDROGEN; IRON; IRON SULFUR PROTEIN; NITROBENZENE; NITROBENZENE DIOXYGENASE; NITROGEN; NONHEME IRON PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATOM; CRYSTAL STRUCTURE; DIOXYGENATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE; HYDROGEN BOND; MOLECULE; NUCLEOTIDE SEQUENCE; OXYGENATION; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

EID: 18044377439     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.03.052     Document Type: Article

References (59)

1. D.R. Hartter The use and importance of nitroaromatic chemicals in the chemical industry D.E. Rickert Toxicity of Nitroaromatic Compounds. Chemical Industry Institute of Toxicology Series 1985 Hemisphere Washington, DC 1 14
2. T. Bruning, R. Thier, and H.M. Bolt Nephrotoxicity and nephrocarcinogenicity of dinitrotoluene: new aspects to be considered Rev. Environ. Health 17 2002 163 172
3. D.B. Couch, P.F. Allen, and D.J. Abernethy The mutagenicity of dinitrotoluenes in Salmonella typhimurium Mutat. Res. 90 1981 373 383
4. J.C. Mirsalis, and B.E. Butterworth Induction of unscheduled DNA synthesis in rat hepatocytes following in vivo treatment with dinitrotoluene Carcinogenesis 3 1982 241 245
5. H. Tokiwa, and Y. Ohnishi Mutagenicity and carcinogenicity of nitroarenes and their sources in the environment Crit. Rev. Toxicol. 17 1986 23 60
6. J.C. Spain Biodegradation of nitroaromatic compounds Annu. Rev. Microbiol. 49 1995 523 555
7. Z. He, and J.C. Spain Studies of the catabolic pathway of degradation of nitrobenzene by Pseudomonas pseudoalcaligenes JS45: removal of the amino group from 2-aminomuconic semialdehyde Appl. Environ. Microbiol. 63 1997 4839 4843
8. Z. He, J.K. Davis, and J.C. Spain Purification, characterization, and sequence analysis of 2-aminomuconic 6-semialdehyde dehydrogenase from Pseudomonas pseudoalcaligenes JS45 J. Bacteriol. 180 1998 4591 4595
9. Z. He, and J.C. Spain A novel 2-aminomuconate deaminase in the nitrobenzene degradation pathway of Pseudomonas pseudoalcaligenes JS45 J. Bacteriol. 180 1998 2502 2506
10. S.F. Nishino, and J.C. Spain Degradation of nitrobenzene by a Pseudomonas pseudoalcaligenes Appl. Environ. Microbiol. 59 1993 2520 2525
11. H.S. Park, and H.S. Kim Identification and characterization of the nitrobenzene catabolic plasmids pNB1 and pNB2 in Pseudomonas putida HS12 J. Bacteriol. 182 2000 573 580
12. C.C. Somerville, S.F. Nishino, and J.C. Spain Purification and characterization of nitrobenzene nitroreductase from Pseudomonas pseudoalcaligenes JS45 J. Bacteriol. 177 1995 3837 3842
13. D.J. Lessner, G.R. Johnson, R.E. Parales, J.C. Spain, and D.T. Gibson Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765 Appl. Environ. Microbiol. 68 2002 634 641
14. D.T. Gibson, and R.E. Parales Aromatic hydrocarbon dioxygenases in environmental biotechnology Curr. Opin. Biotechnol. 11 2000 236 243
15. S.F. Nishino, and J.C. Spain Oxidative pathway for the biodegradation of nitrobenzene by Comamonas sp. strain JS765 Appl. Environ. Microbiol. 61 1995 2308 2313
16. B. Kauppi, K. Lee, E. Carredano, R.E. Parales, D.T. Gibson, H. Eklund, and S. Ramaswamy Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase Structure 6 1998 571 586
17. A. Karlsson, J.V. Parales, R.E. Parales, D.T. Gibson, H. Eklund, and S. Ramaswamy Crystal structure of naphthalene dioxygenase: side-on binding of dioxygen to iron Science 299 2003 1039 1042
18. 2 activation by the oxygenase component of naphthalene 1,2-dioxygenase J. Biol. Chem. 276 2001 1945 1953
19. D.T. Gibson, S.M. Resnick, K. Lee, J.M. Brand, D.S. Torok, and L.P. Wackett Desaturation, dioxygenation, and monooxygenation reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain 9816-4 J. Bacteriol. 177 1995 2615 2621
20. J.V. Parales, A. Kumar, R.E. Parales, and D.T. Gibson Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42 Gene 181 1996 57 61
21. W.C. Suen, B.E. Haigler, and J.C. Spain 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase J. Bacteriol. 178 1996 4926 4934
22. A. Karlsson, J.V. Parales, R.E. Parales, D.T. Gibson, H. Eklund, and S. Ramaswamy The reduction of the Rieske iron-sulfur cluster in naphthalene dioxygenase by X-rays J. Inorg. Biochem. 78 2000 83 87
23. Y. Furusawa, V. Nagarajan, M. Tanokura, E. Masai, M. Fukuda, and T. Senda Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1 J. Mol. Biol. 342 2004 1041 1052
24. 2+/calmodulin- dependent kinase II Mol. Cell 11 2003 1241 1251
25. T. Lundqvist, J. Rice, C.N. Hodge, G.S. Basarab, J. Pierce, and Y. Lindqvist Crystal structure of scytalone dehydratase: a disease determinant of the rice pathogen, Magnaporthe grisea Structure 2 1994 937 944
26. T.L. Bullock, W.D. Clarkson, H.M. Kent, and M. Stewart The 1.6 Å resolution crystal structure of nuclear transport factor 2 (NTF2) J. Mol. Biol. 260 1996 422 431
27. 5-3-ketosteroid isomerase with and without a reaction intermediate analogue Biochemistry 36 1997 14030 14036
28. D. Lim, and N.C. Strynadka Structural basis for the beta lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus Nature Struct. Biol. 9 2002 870 876
29. M. Arand, B.M. Hallberg, J. Zou, T. Bergfors, F. Oesch, and M.J. van der Werf Structure of Rhodococcus erythropolis limonene-1,2-epoxide hydrolase reveals a novel active site EMBO J. 22 2003 2583 2592
30. C.A. Kerfeld, M.R. Sawaya, V. Brahmandam, D. Cascio, K.K. Ho, and C.C. Trevithick-Sutton The crystal structure of a cyanobacterial water-soluble carotenoid binding protein Structure (Camb.) 11 2003 55 65
31. J. Hirose, A. Suyama, S. Hayashida, and K. Furukawa Construction of hybrid biphenyl (bph) and toluene (tod) genes for functional analysis of aromatic ring dioxygenases Gene 138 1994 27 33
32. S. Harayama, M. Rekik, and K.N. Timmis Genetic analysis of a relaxed substrate specificity aromatic ring dioxygenase, toluate 1,2-dioxygenase, encoded by TOL plasmid pWW0 of Pseudomonas putida Mol. Gen. Genet. 202 1986 226 234
33. J.V. Parales, R.E. Parales, S.M. Resnick, and D.T. Gibson Enzyme specificity of 2-nitrotoluene 2,3-dioxygenase from Pseudomonas sp. strain JS42 is determined by the C-terminal region of the alpha subunit of the oxygenase component J. Bacteriol. 180 1998 1194 1199
34. H.M. Tan, and C.M. Cheong Substitution of the ISP alpha subunit of biphenyl dioxygenase from Pseudomonas results in a modification of the enzyme activity Biochem. Biophys. Res. Commun. 204 1994 912 917
35. H. Jiang, R.E. Parales, and D.T. Gibson The alpha subunit of toluene dioxygenase from Pseudomonas putida F1 can accept electrons from reduced FerredoxinTOL but is catalytically inactive in the absence of the beta subunit Appl. Environ. Microbiol. 65 1999 315 318
36. R.E. Parales, M.D. Emig, N.A. Lynch, and D.T. Gibson Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems J. Bacteriol. 180 1998 2337 2344
37. S. Beil, J.R. Mason, K.N. Timmis, and D.H. Pieper Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5-tetrachlorobenzene J. Bacteriol. 180 1998 5520 5528
38. C.L. Colbert, M.M. Couture, L.D. Eltis, and J.T. Bolin A cluster exposed: structure of the Rieske ferredoxin from biphenyl dioxygenase and the redox properties of Rieske Fe-S proteins Struct. Fold. Des. 8 2000 1267 1278
39. P.J. Ellis, T. Conrads, R. Hille, and P. Kuhn Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 A and 2.03 A Structure (Camb.) 9 2001 125 132
40. S. Iwata, M. Saynovits, T.A. Link, and H. Michel Structure of a water soluble fragment of the 'Rieske' iron-sulfur protein of the bovine heart mitochondrial cytochrome bc1 complex determined by MAD phasing at 1.5 Å resolution Structure 4 1996 567 579
41. S. Iwata, J.W. Lee, K. Okada, J.K. Lee, M. Iwata, and B. Rasmussen Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex Science 281 1998 64 71
42. C.J. Carrell, H. Zhang, W.A. Cramer, and J.L. Smith Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein Structure 5 1997 1613 1625
43. L.M. Iyer, E.V. Koonin, and L. Aravind Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily Proteins: Struct. Funct. Genet. 43 2001 134 144
44. M.J. Romanowski, R.E. Soccio, J.L. Breslow, and S.K. Burley Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain Proc. Natl Acad. Sci. USA 99 2002 6949 6954
45. M.D. Yoder, L.M. Thomas, J.M. Tremblay, R.L. Oliver, L.R. Yarbrough, and G.M. Helmkamp Jr Structure of a multifunctional protein. Mammalian phosphatidylinositol transfer protein complexed with phosphatidylcholine J. Biol. Chem. 276 2001 9246 9252
46. Y. Tsujishita, and J.H. Hurley Structure and lipid transport mechanism of a StAR-related domain Nature Struct. Biol. 7 2000 408 414
47. S.M. Resnick, K. Lee, and D.T. Gibson Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp strain ncib 9816 J. Ind. Microbiol. Biotechnol. 17 1996 438 457
48. R.E. Parales, R. Huang, C.-L. Yu, J. Parales, F.K.N. Lee, and D.J. Lessner Purification, characterization, and crystallization of the components of the nitrobenzene and 2-nitrotoluene dioxygenase enzyme systems Appl. Environ. Microbiol. 2005 in the press
49. A. Hadfield, and J. Hajdu A fast and portable microspectrophotometer for protein crystallography J. Appl. Crystallog. 26 1993 839 842
50. H.R. Powell The Rossmann Fourier autoindexing algorithm in MOSFLM Acta Crystallog. sect. D 55 1999 1690 1695
51. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
52. A. Vagin, and A. Teplyakov MOLREP: an automated program for molecular replacement J. Appl. Crystallog. 30 1997 1022 1025
53. G.N. Murshudov Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallog. sect. D 53 1997 240 255
54. T.A. Jones, J.Y. Zou, S.W. Cowan, and Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta. Crystallogr. sect. A 47 1991 110 119
55. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucl. Acids Res. 28 2000 235 242
56. G.J. Barton ALSCRIPT a tool to formate multiple sequence alignment Protein Engng. 6 1993 37 40
57. D.J. Lessner, G.R. Johnson, R.E. Parales, J.C. Spain, and D.T. Gibson Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765 Appl. Environ. Microbiol. 68 2002 634 641
58. A.M. Jeffrey, H.J. Yeh, D.M. Jerina, T.R. Patel, J.F. Davey, and D.T. Gibson Initial reactions in the oxidation of naphthalene by Pseudomonas putida Biochemistry 14 1975 575 584
59. D.M. Jerina, J.W. Daly, A.M. Jeffrey, and D.T. Gibson Cis-1,2-dihydroxy-1,2-dihydronaphthalene: a bacterial metabolite from naphthalene Arch. Biochem. Biophys. 142 1971 394 396