Application of a new versatile electron transfer system for cytochrome P450-based Escherichia coli whole-cell bioconversions

Applied Microbiology and Biotechnology

Volumn 97, Issue 17, 2013, Pages 7741-7754

  Ringle, Michael ^a   Khatri, Yogan ^a   Zapp, Josef ^a   Hannemann, Frank ^a   Bernhardt, Rita ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Adrenodoxin; Biotechnology; CYP106A1; CYP264A1; Cytochromes P450; Escherichia coli reductase; Redox chain; Whole cell system

Indexed keywords

BACTERIOLOGY; BIOTECHNOLOGY; CYTOLOGY; ELECTRON TRANSITIONS; ENZYMES; ESCHERICHIA COLI;

ADRENODOXIN; CYP106A1; CYP264A1; CYTOCHROMES P450; WHOLE CELL;

CELLS;

ADRENODOXIN; CYTOCHROME P450; CYTOCHROME P450 26A1;

BIOTECHNOLOGY; CATALYST; CELL ORGANELLE; COLIFORM BACTERIUM; ELECTRON; ENZYME ACTIVITY; REDOX POTENTIAL; STEROID;

ARTICLE; BACILLUS MEGATERIUM; BIOTECHNOLOGY; BIOTRANSFORMATION; CONTROLLED STUDY; ELECTRON TRANSPORT; ESCHERICHIA COLI; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SORANGIUM CELLULOSUM; WHOLE CELL;

BACILLUS MEGATERIUM; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; POLYANGIUM CELLULOSUM;

ADRENODOXIN; ANIMALS; BIOTRANSFORMATION; CATTLE; CYTOCHROME P-450 ENZYME SYSTEM; ELECTRON TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METABOLIC ENGINEERING; MYXOCOCCALES; OXIDATION-REDUCTION;

EID: 84892590749     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4612-0     Document Type: Article

References (74)

1. Agematu H, Matsumoto N, Fujii Y, Kabumoto H, Doi S, Machida K, Ishikawa J, Arisawa A (2006) Hydroxylation of testosterone by bacterial cytochromes P450 using the Escherichia coli expression system. Biosci Biotechnol Biochem 70:307-311
2. Bell SG, Harford-Cross CF, Wong L-L (2001) Engineering the CYP101 system for in vivo oxidation of unnatural substrates. Protein Eng 14:797-802
3. Bell SG, Hoskins N, Xu F, Caprotti D, Rao Z, Wong LL (2006) Cytochrome P450 enzymes from the metabolically diverse bacterium Rhodopseudomonas palustris. Biochem Biophys Res Commun 342:191-196
4. Bell S, Dale A, Rees N, Wong L-L (2010) A cytochrome P450 class I electron transfer system from Novosphingobium aromaticivorans. Appl Microbiol Biotechnol 86:163-175
5. Berg A, Gustafsson JA, Ingelman-SundbergM(1976) Characterization of a cytochrome P-450-dependent steroid hydroxylase system present in Bacillus megaterium. J Biol Chem 251:2831-2838
6. Berg A, Ingelman-Sundberg M, Gustafsson JA (1979) Isolation and characterization of cytochrome P-450meg. Acta Biol Med Ger 38:333-344
7. Bernhardt R (1996) Cytochrome P450: structure, function, and generation of reactive oxygen species. Rev Physiol Biochem Pharmacol 127:137-221
8. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124:128-145
9. Bleif S, Hannemann F, Lisurek M, von Kries JP, Zapp J, Dietzen M, Antes I, Bernhardt R (2011) Identification of CYP106A2 as a regioselective allylic bacterial diterpene hydroxylase. ChemBioChem 12:576-582
10. Bleif S, Hannemann F, Zapp J, Hartmann D, Jauch J, Bernhardt R (2012) A new Bacillus megaterium whole-cell catalyst for the hydroxylation of the pentacyclic triterpene 11-keto-beta-boswellic acid (KBA) based on a recombinant cytochrome P450 system. Appl Microbiol Biotechnol 93:1135-1146
11. Botsford JL, DeMoss RD (1971) Catabolite repression of tryptophanase in Escherichia coli. J Bacteriol 105:303-312
12. Cao PR, Bulow H, Dumas B, Bernhardt R (2000) Construction and characterization of a catalytic fusion protein system: P-450(11beta)-adrenodoxin reductase-adrenodoxin. Biochim Biophys Acta 1476:253-264
13. Chefson A, Auclair K (2006) Progress towards the easier use of P450 enzymes. Mol Biosyst 2:462-469
14. Chun YJ, Shimada T, Waterman MR, Guengerich FP (2006) Understanding electron transport systems of Streptomyces cytochrome P450. Biochem Soc Trans 34:1183-1185
15. Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Structure and chemistry of cytochrome P450. Chem Rev 105:2253-2278
16. Ensley BD, Ratzkin BJ, Osslund TD, Simon MJ, Wackett LP, Gibson DT (1983) Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222:167-169
17. Ewen KM, Schiffler B, Uhlmann-Schiffler H, Bernhardt R, Hannemann F (2008) The endogenous adrenodoxin reductaselike flavoprotein arh1 supports heterologous cytochrome P450-dependent substrate conversions in Schizosaccharomyces pombe. FEMS Yeast Res 8:432-441
18. Ewen KM, Hannemann F, Khatri Y, Perlova O, Kappl R, Krug D, Hüttermann J, Müller R, Bernhardt R (2009) Genome mining in Sorangium cellulosum So ce56-identification and characterization of the homologous electron transfer proteins of a myxobacterial cytochrome P450. J Biol Chem 284:28590-28598
19. Ewen KM, Hannemann F, Iametti S, Morleo A, Bernhardt R (2011) Functional characterization of Fdx1: evidence for an evolutionary relationship between P450-type and ISC-type ferredoxins. J Mol Biol 413:940-951
20. Ewen KM, Ringle M, Bernhardt R (2012) Adrenodoxin-a versatile ferredoxin. IUBMB Life 64:506-512
21. Faro M, Schiffler B, Heinz A, Nogues I, Medina M, Bernhardt R, Gomez-Moreno C (2003) Insights into the design of a hybrid system between Anabaena ferredoxin-NADP+ reductase and bovine adrenodoxin. Eur J Biochem 270:726-735
22. Fischer F, Raimondi D, Aliverti A, Zanetti G (2002) Mycobacterium tuberculosis FprA, a novel bacterial NADPH-ferredoxin reductase. Eur J Biochem 269:3005-3013
23. Frank LH, Demoss RD (1957) Specific enzymic method for the estimation of l-tryptophan. Arch Biochem Biophys 67:387-397
24. Gillam EMJ, Guengerich FP (2001) Exploiting the versatility of human cytochrome P450 enzymes: the promise of blue roses from biotechnology. IUBMB Life 52:271-277
25. Gillam EMJ, Notley LM, Cai H, De Voss JJ, Guengerich FP (2000) Oxidation of indole by cytochrome P450 enzymes. Biochemistry (Mosc) 39:13817-13824
26. Girhard M, Machida K, Itoh M, Schmid RD, Arisawa A, Urlacher VB (2009) Regioselective biooxidation of (+)-valencene by recombinant E. coli expressing CYP109B1 from Bacillus subtilis in a two-liquid-phase system. Microb Cell Fact 8:36
27. Girhard M, Klaus T, Khatri Y, Bernhardt R, Urlacher VB (2010) Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis. Appl Microbiol Biotechnol 87:595-607
28. Gudiminchi R, Randall C, Opperman D, Olaofe O, Harrison SL, Albertyn J, Smit M (2012) Whole-cell hydroxylation of noctane by Escherichia coli strains expressing the CYP153A6 operon. Appl Microbiol Biotechnol 96:1507-1516
29. Guengerich FP (2001) Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 14:611-650
30. Guzov VM, Unnithan GC, Chernogolov AA, Feyereisen R (1998) CYP12A1, a mitochondrial cytochrome P450 from the house fly. Arch Biochem Biophys 359:231-240
31. Hannemann F, Virus C, Bernhardt R (2006) Design of an Escherichia coli system for whole cell mediated steroid synthesis and molecular evolution of steroid hydroxylases. J Biotechnol 124:172-181
32. Hannemann F, Bichet A, Ewen KM, Bernhardt R (2007) Cytochrome P450 systems-biological variations of electron transport chains. Biochim Biophys Acta Gen Subj 1770:330-344
33. Hawkes DB, Slessor KE, Bernhardt PV, De Voss JJ (2010) Cloning, expression and purification of cindoxin, an unusual Fmncontaining cytochrome P450 redox partner. ChemBioChem 11:1107-1114
34. Isin EM, Guengerich FP (2007) Complex reactions catalyzed by cytochrome P450 enzymes. Biochim Biophys Acta Gen Subj 1770:314-329
35. Jenkins CM, Waterman MR (1994) Flavodoxin and NADPHflavodoxin reductase from Escherichia coli support bovine cytochrome P450c17 hydroxylase activities. J Biol Chem 269:27401-27408
36. Jenkins CM, Waterman MR (1998) NADPH-flavodoxin reductase and flavodoxin from Escherichia coli: characteristics as a soluble microsomal P450 reductase. Biochemistry (Mosc) 37:6106-6113
37. Khatri Y, Girhard M, Romankiewicz A, Ringle M, Hannemann F, Urlacher V, Hutter M, Bernhardt R (2010a) Regioselective hydroxylation of norisoprenoids by CYP109D1 from Sorangium cellulosum So ce56. Appl Microbiol Biotechnol 88:485-495
38. Khatri Y, Hannemann F, Ewen KM, Pistorius D, Perlova O, Kagawa N, Brachmann AO, Müller R, Bernhardt R (2010b) The CYPome of Sorangium cellulosum So ce56 and identification of CYP109D1 as a new fatty acid hydroxylase. Chem Biol 17:1295-1305
39. Kille S, Zilly FE, Acevedo JP, Reetz MT (2011) Regio- and stereoselectivity of P450-catalysed hydroxylation of steroids controlled by laboratory evolution. Nat Chem 3:738-743
40. Kyung-Hwan J (2006) Continuous production of recombinant interferon-α in Escherichia coli via the derepression of trp promoter using casamino acid. Process Biochem 41:809-814
41. Li HM, Mei LH, Urlacher V, Schmid R (2008) Cytochrome P450 BM-3 evolved by random and saturation mutagenesis as an effective indole-hydroxylating catalyst. Appl BiochemBiotechnol 144:27-36
42. Liao WL, Dodder NG, Mast N, Pikuleva IA, Turko IV (2009) Steroid and protein ligand binding to cytochrome P450 46A1 as assessed by hydrogen-deuterium exchange and mass spectrometry. Biochemistry 48:4150-4158
43. Lisurek M, Kang MJ, Hartmann RW, Bernhardt R (2004) Identification of monohydroxy progesterones produced by CYP106A2 using comparative HPLC and electrospray ionisation collision-induced dissociation mass spectrometry. Biochem Biophys Res Commun 319:677-682
44. Ly T, Khatri Y, Zapp J, Hutter M, Bernhardt R (2012) CYP264B1 from Sorangium cellulosum So ce56: a fascinating norisoprenoid and sesquiterpene hydroxylase. Appl Microbiol Biotechnol 95:123-133
45. Manna SK, Mazumdar S (2010) Tuning the substrate specificity by engineering the active site of cytochrome P450cam: a rational approach. Dalton Trans 39:3115-3123
46. Martinez-Gomez K, Flores N, Castaneda HM, Martinez-Batallar G, Hernandez-Chavez G, Ramirez OT, Gosset G, Encarnacion S, Bolivar F (2012) New insights into Escherichia coli metabolism: carbon scavenging, acetate metabolism and carbon recycling responses during growth on glycerol. Microb Cell Fact 11:46
47. 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
48. Nelson DR (2006) Cytochrome P450 nomenclature, 2004. Methods Mol Biol 320:1-10
49. Nguyen KT, Virus C, Günnewich N, Hannemann F, Bernhardt R (2012) Changing the regioselectivity of a P450 from C15 to C11 hydroxylation of progesterone. ChemBioChem 13:1161-1166
50. O'Keefe DP, Gibson KJ, Emptage MH, Lenstra R, Romesser JA, Litle PJ, Omer CA (1991) Ferredoxins from two sulfonylurea herbicide monooxygenase systems in Streptomyces griseolus. Biochemistry (Mosc) 30:447-455
51. Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. J Biol Chem 239:2370-2378
52. O'Reilly E, Kohler V, Flitsch SL, Turner NJ (2011) Cytochromes P450 as useful biocatalysts: addressing the limitations. Chem Commun (Camb) 47:2490-2501
53. Ortiz de Montellano P, Voss J (2005) Substrate oxidation by cytochrome P450 enzymes. Springer, New York, pp 183-245
54. Pechurskaya TA, Harnastai IN, Grabovec IP, Gilep AA, Usanov SA (2007) Adrenodoxin supports reactions catalyzed by microsomal steroidogenic cytochrome P450s. Biochem Biophys Res Commun 353:598-604
55. Perlova O, Gerth K, Kaiser O, Hans A, Müller R (2006) Identification and analysis of the chivosazol biosynthetic gene cluster from the myxobacterial model strain Sorangium cellulosum So ce56. J Biotechnol 121:174-191
56. Robin M-A, Anandatheerthavarada HK, Fang J-K, Cudic M, Otvos L, Avadhani NG (2001) Mitochondrial targeted cytochrome P450 2E1 (P450 MT5) contains an intact N terminus and requires mitochondrial specific electron transfer proteins for activity. J Biol Chem 276:24680-24689
57. Rosic N (2009) Versatile capacity of shuffled cytochrome P450s for dye production. Appl Microbiol Biotechnol 82:203-210
58. Sagara Y, Wada A, Takata Y, Waterman MR, Sekimizu K, Horiuchi T (1993) Direct expression of adrenodoxin reductase in Escherichia coli and the functional characterization. Biol Pharm Bull 16:627-630
59. Sakaki T, Kagawa N, Yamamoto K, Inouye K (2005) Metabolism of vitamin D3 by cytochromes P450. Front Biosci 10:119-134
60. Salamanca-Pinzón SG, Guengerich FP (2011) A tricistronic human adrenodoxin reductase-adrenodoxin-cytochrome P450 27A1 vector system for substrate hydroxylation in Escherichia coli. Protein Expression Purif 79:231-236
61. Schmitz D, Zapp J, Bernhardt R (2012) Hydroxylation of the triterpenoid dipterocarpol with CYP106A2 from Bacillus megaterium. FEBS J 279:1663-1674
62. Schuster I (2011) Cytochromes P450 are essential players in the vitamin D signaling system. Biochim Biophys Acta 1814:186-199
63. Seifert A, Pleiss J (2012) Identification of selectivity determinants in CYP monooxygenases by modelling and systematic analysis of sequence and structure. Curr Drug Metab 13:197-202
64. Simgen B, Contzen J, Schwarzer R, Bernhardt R, Jung C (2000) Substrate binding to 15β-hydroxylase (CYP106A2) probed by FT infrared spectroscopic studies of the iron ligand CO stretch vibration. Biochem Biophys Res Commun 269:737-742
65. Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96:2841-2888
66. Studier FW (2005) Protein production by auto-induction in highdensity shaking cultures. Protein Expr Purif 41:207-234
67. Uhlmann H, Kraft R, Bernhardt R (1994) C-terminal region of adrenodoxin affects its structural integrity and determines differences in its electron transfer function to cytochrome P-450. J Biol Chem 269:22557-22564
68. Urlacher VB, Eiben S (2006) Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol 24:324-330
69. Urlacher VB, Girhard M (2012) Cytochrome P450 monooxygenases: an update on perspectives for synthetic application. Trends Biotechnol 30:26-36
70. Virus C, Lisurek M, Simgen B, Hannemann F, Bernhardt R (2006) Function and engineering of the 15beta-hydroxylase CYP106A2. Biochem Soc Trans 34:1215-1218
71. Werck-Reichhart D, Feyereisen R (2000) Cytochromes P450: a success story. Genome Biol 1:REVIEWS3003
72. Whitehouse CJC, Yang W, Yorke JA, Tufton HG, Ogilvie LCI, Bell SG, Zhou W, Bartlam M, Rao Z, Wong L-L (2011) Structure, electronic properties and catalytic behaviour of an activityenhancing CYP102A1 (P450BM3) variant. Dalton Trans 40:10383-10396
73. Wong L-L (2011) P450BM3 on steroids: the Swiss army knife P450 enzyme just gets better. ChemBioChem 12:2537-2539
74. Zehentgruber D, Hannemann F, Bleif S, Bernhardt R, Lütz S (2010) Towards preparative scale steroid hydroxylation with cytochrome P450 monooxygenase CYP106A2. ChemBioChem 11:713-721