Characterization of Cupriavidus metallidurans CYP116B1 - A thiocarbamate herbicide oxygenating P450-phthalate dioxygenase reductase fusion protein

FEBS Journal

Volumn 279, Issue 9, 2012, Pages 1675-1693

  Warman, Ashley J ^a   Robinson, Jacob W ^b   Luciakova, Dominika ^b   Lawrence, Andrew D ^c   Marshall, Ker R ^a   Warren, Martin J ^c   Cheesman, Myles R ^d   Rigby, Stephen E J ^b   Munro, Andrew W ^b   McLean, Kirsty J ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF KENT   (United Kingdom)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

CYP116B1 cytochrome P450 (116B1) from Cupriavidus metallidurans; fusion enzyme; phthalate dioxygenase reductase; potentiometry

Indexed keywords

ARACHIDONIC ACID; CYTOCHROME C; CYTOCHROME P450 116A1; CYTOCHROME P450 116B1; CYTOCHROME P450 REDUCTASE; DIPROPYLTHIOCARBAMIC ACID S ETHYL ESTER; FERRICYANIDE; HERBICIDE; IRON; IRON SULFUR PROTEIN; MYRISTOLEIC ACID; PALMITOLEIC ACID; PROPYLDIPROPYLTHIOCARBAMATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ARTICLE; CATALYSIS; CUPRIAVIDUS; CUPRIAVIDUS METALLIDURANS; DEALKYLATION; ELECTRON SPIN RESONANCE; ENZYME BINDING; ENZYME METABOLISM; ENZYME STRUCTURE; HYDROXYLATION; LIGHT SCATTERING; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; RAMAN SPECTROMETRY; REDUCTION; RHODOCOCCUS ERYTHROPOLIS;

BACTERIAL PROTEINS; CLONING, MOLECULAR; CUPRIAVIDUS; CYANIDES; CYTOCHROME P-450 ENZYME SYSTEM; ELECTRON SPIN RESONANCE SPECTROSCOPY; HERBICIDES; IMIDAZOLES; IRON-SULFUR PROTEINS; LASERS; NADP; NITRIC OXIDE; OXIDOREDUCTASES; RECOMBINANT FUSION PROTEINS; RHODOCOCCUS; SCATTERING, RADIATION; SPECTROPHOTOMETRY, ULTRAVIOLET; THERMODYNAMICS; THIOCARBAMATES;

CUPRIAVIDUS METALLIDURANS; ERYTHROPOLIS; ESCHERICHIA COLI;

EID: 84860223425     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08543.x     Document Type: Article

References (66)

1. Denisov IG, Makris TM, Sligar SG, &, Schlichtling I, (2005) Structure and chemistry of cytochrome P450. Chem Rev 105, 2253-2277. (Pubitemid 40951784)
2. Munro AW, Girvan HM, &, McLean KJ, (2007) Variations on a (t)heme-novel mechanisms, redox partners and catalytic functions in the cytochrome P450 superfamily. Nat Prod Rep 24, 585-609. (Pubitemid 46848711)
3. Rittle J, &, Green MT, (2010) Cytochrome P450 compound I: capture, characterization, and C-H bond activation kinetics. Science 330, 933-937.
4. Cryle MJ, &, De Voss JJ, (2006) Is the ferric hydroperoxy species responsible for sulfur oxidation in cytochrome P450s? Angew Chem Int Ed 45, 8221-8223. (Pubitemid 44974169)
5. Shaik S, de Visser SP, &, Kumar D, (2004) One oxidant, many pathways: a theoretical perspective of monooxygenation mechanisms by cytochrome P450 enzymes. JBiol Inorg Chem 9, 661-668. (Pubitemid 39279245)
6. Guengerich FP, (2001) Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 14, 611-650. (Pubitemid 32565712)
7. Rylott EL, Jackson RG, Sabbadin F, Seth-Smith HM, Edwards J, Chong CS, Strand SE, Grogan G, &, Bruce NC, (2011) The explosive-degrading cytochrome P450 XplA: biochemistry, structural features and prospects for bioremediation. Biochim Biophys Acta 1814, 230-236.
8. Song W-C, Baertschis SW, Boeglin WE, Harris TM, &, Brash AR, (1993) Formation of epoxyalcohols by a purified allene oxide synthase. Implications for the mechanism of allene oxide synthase. J Biol Chem 268, 6293-6298. (Pubitemid 23099322)
9. Poulos TL, Finzel BC, &, Howard AJ, (1987) High-resolution crystal structure of cytochrome P450cam. J Mol Biol 195, 687-700.
10. Sevrioukova IF, Poulos TL, &, Churbanova IY, (2010) Crystal structure of the putidaredoxin reductase-putidaredoxin electron transfer complex. J Biol Chem 285, 13616-13620.
11. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS, &, Kim JJ, (1997) Three dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94, 8411-8416. (Pubitemid 27335052)
12. Munro AW, Girvan HM, &, McLean KJ, (2007) Cytochrome P450-redox partner fusion enzymes. Biochim Biophys Acta 1770, 345-359. (Pubitemid 46136745)
13. Daiber A, Shoun H, &, Ullrich V, (2005) Nitric oxide reductase (P450nor) from Fusarium oxysporum. J Inorg Biochem 99, 185-193. (Pubitemid 39642978)
14. Shoji O, Fujishiro T, Nakajima H, Kim M, Nagano S, Shiro Y, &, Watanabe Y, (2007) Hydrogen peroxide dependent monooxygenations by tricking the substrate recognition of cytochrome P450BSbeta. Angew Chem Int Ed 46, 3656-3659. (Pubitemid 46981241)
15. Hannemann F, Bichet A, Ewen KM, &, Bernhardt R, (2007) Cytochrome P450 systems-biological variations of electron transport chains. Biochim Biophys Acta 1770, 330-344. (Pubitemid 46157074)
16. Warman AJ, Roitel O, Neeli R, Girvan HM, Seward HE, Murray SA, McLean KJ, Joyce MG, Toogood H, Holt RA, et al. (2005) Flavocytochrome P450 BM3: an update on structure and mechanism of a biotechnologically important enzyme. Biochem Soc Trans 33, 747-753. (Pubitemid 41160856)
17. Narhi LO, &, Fulco AJ, (1987) Identification and characterization of two functional domains in cytochrome P-450BM-3, a catalytically self-sufficient monooxygenase induced by barbiturates in Bacillus megaterium. J Biol Chem 262, 6683-6690.
18. Noble MA, Miles CS, Chapman SK, Lysek DA, MacKay AC, Reid GA, Hanzlik RP, &, Munro AW, (1999) Roles of key active-site residues in flavocytochrome P450 BM3. Biochem J 339, 371-379. (Pubitemid 29209968)
19. Munro AW, Daff S, Coggins JR, Lindsay JG, &, Chapman SK, (1996) Probing electron transfer in flavocytochrome P450 BM3 and its component domains. Eur J Biochem 239, 403-409. (Pubitemid 26246547)
20. Gustafsson MC, Roitel O, Marshall KR, Noble MA, Chapman SK, Pessegueiro A, Fulco AJ, Cheesman MR, von Wachenfeldt C, &, Munro AW, (2004) Expression, purification and characterization of Bacillus subtilis cytochromes P450 CYP102A2 and CYP102A3: flavocytochrome homologues of P450 BM3 from Bacillus megaterium. Biochemistry 43, 5474-5487. (Pubitemid 38620939)
21. Kitazume T, Takaya N, Nakayama N, &, Shoun H, (2000) Fusarium oxysporum fatty-acid subterminal hydroxylase (CYP505) is a membrane-bound eukaryotic counterpart of Bacillus megaterium cytochrome P450 BM3. J Biol Chem 275, 39734-39740. (Pubitemid 32059002)
22. Neeli R, Girvan HM, Lawrence A, Warren MJ, Leys D, Scrutton NS, &, Munro AW, (2005) The dimeric form of flavocytochrome P450 BM3 is catalytically functional as a fatty acid hydroxylase. FEBS Lett 579, 5582-5588. (Pubitemid 41455634)
23. Kitazume T, Haines DC, Estabrook RW, Chen B, &, Peterson JA, (2007) Obligatory intermolecular electron transfer from FAD to FMN in dimeric P450 BM-3. Biochemistry 46, 11892-11901. (Pubitemid 47623757)
24. Girvan HM, Dunford AJ, Neeli R, Ekanem IS, Waltham TN, Joyce MG, Leys D, Curtis RA, Williams P, Fisher K, et al. (2011) Flavocytochrome P450 BM3 mutant W1046A is a NADH-dependent fatty acid hydroxylase: implications for the mechanism of electron transfer in the P450 BM3 dimer. Arch Biochem Biophys 507, 75-85.
25. Ost TW, Miles CS, Murdoch J, Cheung Y, Reid GA, Chapman SK, &, Munro AW, (2000) Rational re-design of the substrate binding site of flavocytochrome P450 BM3. FEBS Lett 486, 173-177.
26. Peters MW, Meinhold P, Glieder A, &, Arnold FH, (2005) Regio- and enantioselective alkane hydroxylation with engineered cytochromes P450 BM-3. J Am Chem Soc 125, 13442-13450. (Pubitemid 37352128)
27. Kille S, Zilly FE, Acevedo JP, &, Reetz MT, (2011) Regio- and stereoselectivity of P450-catalysed hydroxylation of steroids controlled by laboratory evolution. Nat Chem 14, 738-743.
28. Whitehouse CJ, Bell SG, &, Wong LL, (2012) P450 BM3 (CYP102A1): connecting the dots. Chem Soc Rev 41, 1218-1260.
29. De Mot R, &, Parret AH, (2002) A novel class of self-sufficient cytochrome P450 monooxygenases in prokaryotes. Trends Microbiol 10, 502-508. (Pubitemid 35284796)
30. Gassner GT, Ludwig ML, Gatti DL, Correll CC, &, Ballou DP, (1995) Structure and mechanism of the iron-sulfur flavoprotein phthalate dioxygenase reductase. FASEB J 9, 1411-1418.
31. Batie CJ, &, Ballou DP, (1990) Phthalate dioxygenase. Methods Enzymol 188, 61-70. (Pubitemid 20384879)
32. Roberts GA, Celik A, Hunter DJ, Ost TW, White JH, Chapman SK, Turner NJ, &, Flitsch SL, (2003) A self-sufficient cytochrome P450 with a primary structural organization that includes a flavin domain and a [2Fe-2S] redox center. J Biol Chem 278, 48914-48920.
33. Hunter DJ, Roberts GA, Ost TW, White JH, Müller S, Turner NJ, Flitsch SL, &, Chapman SK, (2005) Analysis of the domain properties of the novel cytochrome P450 RhF. FEBS Lett 579, 2215-2220. (Pubitemid 40469695)
34. Nagy I, Schoofs G, Compornolle F, Proost P, Vanderleyden J, &, de Mot R, (1995) Degradation of the thiocarbamate herbicide EPTC (S-ethyl dipropylcarbamothioate) and biosafening by Rhodococcus sp. Strain NI86/21 involve an inducible cytochrome P-450 system and aldehyde dehydrogenase. J Bacteriol 177, 676-687.
35. Girvan HM, Levy CW, Williams P, Fisher K, Cheesman MR, Rigby SE, &, Munro AW, (2010) Glutamate-haem ester bond formation is disfavoured in flavocytochrome P450 BM3: characterization of glutamate substitution mutants at the haem site of P450 BM3. Biochem J 427, 455-466.
36. Ost TW, Miles CS, Munro AW, Murdoch J, Red GA, &, Chapman SK, (2001) Phenylalanine 393 exerts thermodynamic control over the heme of flavocytochrome P450 BM3. Biochemistry 40, 13421-13429. (Pubitemid 33130769)
37. Perera R, Sono M, Sigman JA, Pfister TD, Lu Y, &, Dawson JH, (2003) Neutral thiol as a proximal ligand to ferrous heme iron: implications for heme proteins that lose cysteine thiolate ligation on reduction. Proc Natl Acad Sci USA 100, 3641-3646. (Pubitemid 36418085)
38. McLean KJ, Warman AJ, Seward HE, Marshall KR, Girvan HM, Cheesman MR, Waterman MR, &, Munro AW, (2006) Biophysical characterization of the sterol demethylase P450 from Mycobacterium tuberculosis, its cognate ferredoxin and their interactions. Biochemistry 45, 8427-8443. (Pubitemid 44036548)
39. McLean KJ, Cheesman MR, Rivers SL, Richmond A, Leys D, Chapman SK, Reid GA, Price NC, Kelly SM, Clarkson J, et al. (2002) Expression and purification of the cytochrome P450 CYP121 from Mycobacterium tuberculosis. J Inorg Biochem 91, 527-541. (Pubitemid 35286658)
40. Quaroni LG, Seward HE, McLean KJ, Girvan HM, Ost TW, Noble MA, Kelly SM, Price NC, Cheesman MR, Smith WE, et al. (2004) Interaction of nitric oxide with cytochrome P450 BM3. Biochemistry 43, 16416-16431. (Pubitemid 40041054)
41. Sligar SG, &, Gunsalus IC, (1976) A thermodynamic mode of regulation: modulation of redox equilbria in camphor monoxygenase. Proc Natl Acad Sci USA 73, 1078-1082.
42. Miles JS, Munro AW, Rospendowski BN, Smith WE, McKnight JE, &, Thomson AJ, (1992) Domains of the catalytically self-sufficient cytochrome P-450 BM-3. Genetic construction, overexpression, purification and spectroscopic characterization. Biochem J 288, 503-509.
43. Noble MA, Quaroni L, Chumanov GD, Turner KJ, Chapman SK, Hanzlik RP, &, Munro AW, (1998) Imidazolyl carboxylic acids as mechanistic probes of flavocytochrome P-450 BM3. Biochemistry 37, 15799-15807. (Pubitemid 28524751)
44. Morrison JF, (1969) Kinetics of the reversible inhibition of enzyme-catalysed reactions by tight-binding inhibitors. Biochim Biophys Acta 185, 269-286.
45. Alterman MA, Chaurasia CS, Lu P, Hardwick JP, &, Hanzlik RP, (1995) Fatty acid discrimination and omega hydroxylation by cytochrome P450 4A1 and a cytochrome P450 4A1/NADPH-P450 reductase fusion protein. Arch Biochem Biophys 320, 289-296.
46. Siddhanta U, Presta A, Fan B, Wolan D, Rousseau DL, &, Stuehr DJ, (1998) Domain swapping in inducible nitric-oxide synthase. Electron transfer occurs between flavin and heme groups on adjacent subunits in the dimer. J Biol Chem 273, 18950-18958. (Pubitemid 28366284)
47. Lawson RJ, Leys D, Sutcliffe MJ, Kemp CA, Cheesman MR, Smith SJ, Clarkson J, Smith WE, Haq I, Perkins JB, et al. (2004) Thermodynamic and biophysical characterisation of cytochrome P450 BioI from Bacillus subtilis. Biochemistry 43, 12410-12426. (Pubitemid 39314703)
48. Girvan HM, Marshall KR, Lawson RJ, Leys D, Joyce MG, Clarkson J, Smith WE, Cheesman MR, &, Munro AW, (2004) Flavocytochrome P450 BM3 mutant A264E undergoes substrate- dependent formation of a novel heme iron ligand set. J Biol Chem 279, 23274-23286. (Pubitemid 38685636)
49. Lipscomb JD, (1980) Electron paramagnetic resonance detectable states of cytochrome P-450cam. Biochemistry 19, 3590-3599.
50. Evans EH, Rush JD, Johnson CE, &, Evans MCW, (1979) Mossbauer spectra of Photosystem-I reaction centres from the blue-green alga Chlorogloea fritschii. Biochem J 182, 861-865. (Pubitemid 10243690)
51. Sellers VM, Wang K, Johnson MK, &, Dailey HA, (1998) Evidence that the fourth ligand to the [2Fe-2S] cluster in animal ferrochelatase is a cysteine. J Biol Chem 273, 22311-22316.
52. More C, Belle V, Asso M, Fournel A, Roger G, Guigliarelli B, &, Bertrand P, (1999) EPR spectroscopy: a powerful technique for the structural and functional investigation of metalloproteins. Biospectroscopy 5 (S5), S3-S18.
53. Batie CJ, Lahaie E, &, Ballou DP, (1987) Purification and characterization of phthalate oxygenase and phthalate oxygenase reductase from Pseudomonas cepacia. J Biol Chem 262, 1510-1518.
54. Voss I, Goss Y, Murozuka E, Altmann B, McLean KJ, Rigby SE, Munro AW, Scheibe R, Hase T, &, Hanke GT, (2011) FdC1, a novel ferredoxin protein capable of alternative electron partitioning, increases in conditions of acceptor limitation at photosystem I. J Biol Chem 286, 50-59.
55. Munro AW, &, Noble MA, (1999) Fluorescence analysis of flavoproteins. Methods Mol Biol 131, 25-48.
56. Driscoll MD, McLean KJ, Levy C, Mast N, Pikuleva IA, Lafite P, Rigby SE, Leys D, &, Munro AW, (2010) Structural and biochemical characterization of Mycobacterium tuberculosis CYP142: evidence for multiple cholesterol 27-hydroxylase activities in a human pathogen. J Biol Chem 285, 38270-38282.
57. Honeychurch MJ, Hill AO, &, Wong LL, (1999) The thermodynamics and kinetics of electron transfer in the cytochrome P450cam enzyme system. FEBS Lett 451, 351-353. (Pubitemid 29243806)
58. Daff SN, Chapman SK, Turner KL, Holt RA, Govindaraj S, Poulos TL, &, Munro AW, (1997) Redox control of the catalytic cycle of flavocytochrome P450 BM3. Biochemistry 36, 13816-13823. (Pubitemid 27494887)
59. Dutton PL, (1978) Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol 54, 411-435.
60. de Groot MJ, Ackland MJ, Horne V, Alex AA, &, Jones BC, (1999) A novel approach to predicting P450 mediated drug metabolism. CYP2D6 catalyzed N-dealkylation reactions and qualitative metabolite predictions using a combined protein and pharmacophore model for CYP2D6. J Med Chem 42, 4062-4070. (Pubitemid 29483023)
61. Kobayashi K, Yamamoto T, Chiba K, Tani M, Shimada N, Ishizaki T, &, Kuroiwa Y, (1998) Human buprenorphine N-dealkylation is catalyzed by cytochrome P450 3A4. Drug Metab Dispos 26, 818-821. (Pubitemid 28376443)
62. Janssen PJ, Van-Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, et al. (2010) The complete genome sequence of Cupriavidus metallidurans CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5, e10433.
63. Sabbadin F, Hyde R, Robin A, Hilgarth E-A, Delenn M, Flitsch S, Turner N, Grogan G, &, Bruce NC, (2010) LICRED: a versatile drop-in vector for rapid generation of redox-self-sufficient cytochrome P450s. ChemBioChem 11, 987-994.
64. Omura T, &, Sato R, (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239, 2370-2378.
65. Berry EA, &, Trumpower BL, (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161, 1-15.
66. Knight E Jr, &, Hardy RF, (1966) Isolation and characteristics of flavodoxin from nitrogen-fixing Clostridium pasteurianum. J Biol Chem 241, 2752-2756.