Engineering cytochrome P450 BM3 of Bacillus megaterium for terminal oxidation of palmitic acid

Journal of Biotechnology

Volumn 184, Issue , 2014, Pages 17-26

  Brühlmann, Fredi ^a   Fourage, Laurent ^b,c   Ullmann, Christophe ^b   Haefliger, Olivier P ^a   Jeckelmann, Nicolas ^a   Dubois, Cédric ^a   Wahler, Denis ^b,d  

^a Analysis and Perception Department   (Switzerland)

^b Protéus Parc Georges Besse ^*  (France)

^c TOTAL   (France)

^d SEPPIC   (France)

Author keywords

Bacillus megaterium; Cytochrome P450; Directed evolution; Palmitic acid; Terminal oxidation

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; OXIDATION; PALMITIC ACID; REGIOSELECTIVITY; FATTY ACIDS; SATURATED FATTY ACIDS;

BACILLUS MEGATERIUM; CRYSTALLOGRAPHIC INFORMATION; CYTOCHROME P450; DIRECTED EVOLUTION; FATTY ACID HYDROXYLASE; HIGH-THROUGHPUT ASSAYS; SECONDARY OXIDATION PRODUCTS; SIMULTANEOUS DETECTION;

SATURATED FATTY ACIDS; PALMITIC ACID;

BACTERIAL PROTEIN; CYTOCHROME P450 BM3; PALMITIC ACID; CYTOCHROME P450; FLAVOCYTOCHROME P450 BM3 MONOXYGENASES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; AMINO ACID; HYDROGEN PEROXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS MEGATERIUM; CONTROLLED STUDY; ENZYME ACTIVE SITE; FATTY ACID OXIDATION; GAS CHROMATOGRAPHY; HIGH THROUGHPUT SCREENING; LIMIT OF DETECTION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; GENETIC ENGINEERING; GENETICS; METABOLISM; MUTAGENESIS; OXIDATION REDUCTION REACTION; CRYSTALLOGRAPHY; ENZYME ENGINEERING; HYDROXYLATION; MOLECULAR CLONING; SEQUENCE ANALYSIS; THERMOSTABILITY; TURNOVER TIME;

AMINO ACID SUBSTITUTION; BACILLUS MEGATERIUM; BACTERIAL PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; DIRECTED MOLECULAR EVOLUTION; GENETIC ENGINEERING; HIGH-THROUGHPUT SCREENING ASSAYS; MUTAGENESIS; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDATION-REDUCTION; PALMITIC ACID;

BACILLUS MEGATERIUM;

EID: 84901396944     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.05.002     Document Type: Article

References (60)

1. Boddupalli S.S., Pramanik B.C., Slaughter C.A., Estabrook R.W., Peterson J.A. Fatty acid monoxygenation by P450BM-3: Product identification and proposed mechanisms for the sequential hydroxylation reactions. Arch. Biochem. Biophys. 1992, 292:20-28.
2. Capdevila J.H., Shozou W., Helvig C., Falck J.R., Belosludtsev Y., Truan G., Graham-Lorence S.E., Peterson J.A. The highly stereoselective oxidation of polyunsaturated fatty acids by cytochrome P450BM-3. J. Biol. Chem. 1996, 271:22663-22671.
3. Carmichael A.B., Wong L.L. Protein engineering of Bacillus megaterium CYP102. Eur. J. Biochem. 2001, 268:3117-3125.
4. Castelfranco P.A., Jones O.T.G. Protoheme turnover and chlorophyll synthesis in greening barley tissue. Plant Physiol. 1975, 55:485-490.
5. Chen C-K.J., Shokhireva T.K., Berry R.E., Zhang H., Walker F.A. The effect of mutation F87 on the properties of CYP102A1-CYP4C7 chimeras: altered regiospecificity and substrate selectivity. J. Biol. Inorg. Chem. 2008, 13:813-824.
6. Chen C-K.J., Shokhireva T.K., Berry R.E., Shokhireva T.K., Murataliev M.B., Zhang H., Walker F.A. Scanning chimeragenesis: the approach used to change the substrate selectivity of fatty acid monooxygenase CYP102A1 to that of terpene Ω-hydroxylase CYP4C7. J. Biol. Inorg. Chem. 2010, 15:159-174.
7. Chodorge M., Fourage L., Ullmann C., Duvivier V., Masson J.M., Lefèvre F. Rational strategies for directed evolution of biocatalysts-application to Candida antarctica lipase B (CALB). Adv. Synth. Catal. 2005, 347:1022-1026.
8. Cirino P.C., Arnold F.H. Regioselectivity and activity of cytochrome P450 BM-3 and mutant F87A in reactions driven by hydrogen peroxide. Adv. Synth. Catal. 2002, 344:932-937.
9. Cirino P.C., Arnold F.H. A self-sufficient peroxide-driven hydroxylation biocatalyst. Angew. Chem. Int. Ed. 2003, 42:3299-3301.
10. Cowart L.A., Falck J.R., Capdevilla J.H. Structural determinants of active site binding affinity and metabolism by cytochrome P450 BM-3. Arch. Biochem. Biophys. 2001, 387:117-124.
11. BM-3 (CYP102). Arch. Biochem. Biophys. 1996, 328:35-42.
12. de Beer S.B.A., van Bergen L.A.H., Keijzer K., Rea V., Venkataraman H., Fonseca Guerra C., Bickelhaupt M., Vermeulen N.P.E., Commandeur J.N.M., Geerke D.P. The role of protein plasticity in computational rationalization studies on regioselectivity in testosterone hydroxylation by cytochrome P450 BM3 mutants. Curr. Drug Metabol. 2012, 13:155-166.
13. BM3. Chem. Biol. 2009, 4:261-267.
14. Dietrich M., Do T.A., Schmid R.D., Pleiss J., Urlacher V.B. Altering the regioselectivity of the subterminal fatty acid hydroxylase P450 BM-3 towards (- and (-positions. J. Biotechnol. 2009, 139:115-117.
15. Di Nardo G., Fantuzzi A., Sideri A., Panicco P., Sassone C., Giunta C., Gilardi G. Wild-type CYP102A1 as a biocatalyst: turnover of drugs usually metabolised by human liver enzymes. J. Biol. Inorg. Chem. 2007, 12:313-323.
16. Eiben S., Bartelmäs H., Urlacher V.B. Construction of a thermostable cytochrome P450 chimera derived from self-sufficient mesophilic parents. Appl. Microbiol. Biotechnol. 2007, 75:1055-1061.
17. BM3 exhibiting native like catalytic properties. Angew. Chem. Int. Ed. 2007, 46:8414-8418.
18. Girvan H.M., Dunford A.J., Neeli R., Ekanem I.S., Waltham T.N., Joyce M.G., Leys D., Curtis R.A., Fisher K., Voice M.W., Munro A.W. Arch. Biochem. Biophys. 2011, 507:75-85.
19. Haines D.C., Tomchick D.R., Machius M., Peterson J.A. Pivotal role of water in the mechanism of P450BM-3. Biochemistry 2001, 40:13456-13465.
20. Haines D.C., Hedge A., Chen B., Zhao W., Bondlela M., Humphreys J.M., Mullin D.A., Tomchick D.R., Machius M., Peterson J.A. A single active site mutation of P450BM-3 dramatically enhances substrate binding and rate of product formation. Biochemistry 2011, 50:8333-8341.
21. Heckmann K.L., Pease L.R. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Prot. 2007, 2:924-932.
22. Huang W-C., Westlake A.C.G., Maréchal J.D., Joyce M.G., Moody P.C.E., Roberts G.C.K. Filling a hole in cytochrome P450 BM3 improves substrate binding and catalytic efficiency. J. Mol. Biol. 2007, 373:633-651.
23. Huang W-C., Cullis P.M., Raven E.L., Roberts G.C.K. Control of the stereo-selectivity of styrene Epoxidation by cytochrome P450 BM3 using structure-based mutagenesis. Metallomics 2011, 3:410-416.
24. Jung S.T., Lauchli R., Arnold F.H. Cytochrome P450: taming a wild type enzyme. Curr. Opin. Biotechnol. 2011, 22:1-9.
25. Kille S., Zilly F.E., Acevedo J.P., Reetz M.F. Regio- and stereoselectivity of P450-catalyzed hydroxylation of steroids controlled by laboratory evolution. Nat. Chem. 2003, 3:738-743.
26. Lentz O., Feenstra A., Habicher T., Hauer B., Schmid R.D., Urlacher V.B. Altering the regioselectivity of cytochrome P450 CYP102A3 of Bacillus subtilis by using a new versatile assay system. ChemBioChem 2006, 7:345-350.
27. Lewis C., Arnold F.H. Catalysts on demand: selective oxidations by laboratory-evolved cytochrome P450 BM3. Chimia 2009, 63:309-312.
28. Li H., Poulos T.L. The structure of the cytochrome P450BM-3 haem domain complexed with the fatty acid substrate, palmitoleic acid. Nat. Struct. Biol. 1997, 4:140-146.
29. BM-3. Biochim. Biophys. Acta 1999, 1441:141-149.
30. Li Y., Drummond D.A., Sawayama A.M., Snow C.D., Bloom J.D., Arnold F.H. A diverse family of thermostable cytochrome P450s created by recombinantion of stabilizing fragments. Nat. Biotechnol. 2007, 25:1051-1056.
31. Loida P.J., Sligar S.G. Molecular recognition in cytochrome P-450: mechanisms for the control of decoupling reactions. Biochemistry 1993, 32:11530-11538.
32. Macheroux P., Massey V., Thiele D.J. Expression of spinach glyolate oxidase in Saccharomyces cerevisiae: purification and characterization. Biochemistry 1991, 30:4612-4619.
33. Malca S.H., Scheps D., Kühnel L., Venegas-Venegas E., Seifert A., Nestl B.M., Hauer B. Bacterial CYP153A monooxygenases for the synthesis of omega-hydroxylated fatty acids. Chem. Commun. 2012, 48:5115-5117.
34. Meinhold P., Peters M.W., Hartwick A., Hernandez A.R., Arnold F.H. Engineering cytochrome P450 for terminal alkane hydroxylation. Adv. Synth. Catal. 2006, 348:763-772.
35. Mestres J. Structure conservation in cytochrome P450. Prot. Struct. Funct. Bioinform. 2005, 58:596-609.
36. Meunier B., deVisser S.P., Shaik S. Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem. Rev. 2004, 104:3947-3980.
37. Miura K.I. Preparation of bacterial DNA by the phenol-pH 9-RNases method. Meth. Enzymol. 1967, 12:543-545.
38. Miura Y., Fulco A. Ω-1, Ω-2 and Ω-3 hydroxylation of long-chain fatty acids, amides and alcohols by a soluble enzyme system from Bacillus megaterium. Biochim. Biophys. Acta 1975, 388:305-317.
39. Modi S., Sutcliffe M.J., Primrose W.U., Lian L.Y., Roberts G.C.K. The catalytic mechanism of cytochrome P450 BM3 involves a 6Å movement of the bound substrate on reduction. Nat. Struct. Biol. 1996, 3:414-417.
40. Nazor J., Dannemann S., Adjei R.O., Fordjour Y.B., Ghampson I.T., Blanusa M., Roccatano D., Schwaneberg U. Laboratory evolution of P450 BM3 for mediated electron transfer yielding an activity-improved and reductase-independent variant. Prot. Eng. Des. Sel. 2008, 21:29-35.
41. Noble M.A., Miles C.S., Chapman S.K., Lysek D.A., Mackay A.C., Reid G.A., Hanzlik R.P., Munro A.W. Roles of key active site residues in flavocytochrome P450 BM3. Biochem. J. 1999, 339:371-379.
42. Oliver C.F., Modi S., Sutcliffe M.J., Primrose W.U., Lian L-Y., Roberts G.C.K. A single mutation in cytochrome P450 BM3 changes substrate orientation in a catalytic intermediate and the regiospecificity of hydroxylation. Biochemistry 1997, 36:1567-1572.
43. Omura T., Sato R. The carbon monoxide-binding pigment of liver microsomes. J. Biol. Chem. 1964, 239:2370-2378.
44. O'Reilly E., Köhler V., Flitsch S.L., Turner N.J. Cytochromes P450 as useful biocatalysts: addressing the limitations. Chem. Commun. 2011, 47:2490-2501.
45. Peters M.W., Meinhold A., Glieder A., Arnold F.H. Regio- and enantioselective alkane hydroxylation with engineered cytochrome p450 BM-3. J. Am. Chem. Soc. 2003, 125:13442-13450.
46. Ravot G., Masson J.-M., Lefèvre F. Application of extremophiles: the industrial screening of extremophiles for valuable biomolecules. Meth. Miocrobiol. 2006, 35:785-813.
47. Ravichandran K.G., Boddupalli S.S., Hasemann C.A., Peterson J.A., Deisenhofer J. Crystal structure of hemeprotein domain of P450BM-3, a prototype for microsomal P450's. Science 1993, 261:731-736.
48. BM3 (CYP102A1). Prot. Cell 2011, 2:656-671.
49. Ruettinger R.T., Fulco A.J. Epoxidation of unsaturated fatty acids by a soluble cytochrome P-450-dependent system from Bacillus megaterium. J. Biol. Chem. 1981, 256:5728-5734.
50. Sambrook J., Russell D.W. Molecular cloning: a laboratory manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 3rd edition.
51. BM-3 monooxygenase: oxidation of 16-hydroxy-hexadecanoic acid to α,ω-hexadecanedioic acid. Biocatal. Biotransfor. 1999, 17:163-178.
52. Seifert A., Pleiss J. Identification of selectivity-determining residues in cytochrome P450 monooxygenases: a systematic analysis of the substrate recognition site 5. Proteins 2008, 74:1028-1035.
53. Seifert A., Vomund S., Grohmann K., Kriening S., Urlacher V.B., Laschat S., Pleiss J. Rational design of a minimal and highly enriched CYP102A1 mutant library with improved regio, stereo, and chemoselectivity. ChemBioChem 2009, 10:853-861.
54. Seifert A., Antonovici M., Hauer B., Pleiss J. An efficient route to selective bio-oxidation catalysts: an iterative approach comprising modeling, diversification and screening, based on CYP102A1. ChemBioChem 2011, 12:1346-1351.
55. Seifert A., Pleiss J. Identification of selectivity determinants in CYP monooxygenases by modeling at systematic analysis of sequence and structure. Curr. Drug Metabol. 2012, 13:197-202.
56. Shehzad A., Panneerselvam S., Linow M., Bocola M., Roccatano D., Mueller-Dieckmann J., Wilmanns M., Schwaneberg U. P450 BM3 crystal structures reveal the role of the charged surface residue Lys/Arg184 in inversion of enantioselective styrene oxidation. Chem. Commun. 2013, 49:4694-4696.
57. Truan G., Komandla M.R., Falck J.R., Peterson J.A. P450BM-3: Absolute configuration of the primary metabolites of palmitic acid. Arch. Biochem. Biophys. 1999, 366:192-198.
58. Vottero E., Rea V., Lastdrager J., Honing M., Vermeulen N.P.E., Commandeur J.N.M. Role of residue 87 in substrate selectivity and regioselectivity of drug-metabolizing cytochrome P450 CYP102A1 M11. J. Biol. Inorg. Chem. 2011, 16:899-912.
59. Whitehouse C.J.C., Bell S.G., Wong L.L. P450BM3 (CYP102A1): connecting the dots. Chem. Soc. Rev. 2012, 41:1218-1260.
60. Wong T.S., Arnold F.H., Schwaneberg U. Laboratory evolution of cytochrome P450 BM-3 monooxygenase for organic cosolvents. Biotechnol. Bioeng. 2004, 85:351-385.