Semi-rational engineering of cytochrome CYP153A from Marinobacter aquaeolei for improved ω-hydroxylation activity towards oleic acid

Applied Microbiology and Biotechnology

Volumn 100, Issue 20, 2016, Pages 8779-8788

  Duan, Yan ^a   Ba, Lina ^a,b   Gao, Jianwei ^a   Gao, Xianxing ^a   Zhu, Dunming ^c   de Jong, René M ^d   Mink, Daniel ^e   Kaluzna, Iwona ^e   Lin, Zhanglin ^a  

^a TSINGHUA UNIVERSITY   (China)

^b INSTITUTE OF EDIBLE FUNGI   (China)

^c Chinese Academy of Sciences   (China)

^d DSM BIOTECHNOLOGY CENTER   (Netherlands)

^e DSM RESOLVE   (Netherlands)

Author keywords

Cytochrome CYP153A; Electron transfer; Iterative saturation mutagenesis; Oleic acid; Site directed saturation mutagenesis

Indexed keywords

BINDING SITES; ELECTRON TRANSITIONS; HYBRID SYSTEMS; HYDROXYLATION; INTERFACES (MATERIALS); MUTAGENESIS; TISSUE CULTURE;

96-WELL FORMAT; ELECTRON TRANSFER; INTERACTION INTERFACE; KINETIC ANALYSIS; REDOX PARTNERS; SATURATION MUTAGENESIS; SUBSTRATE BINDING; WHOLE CELL TRANSFORMATIONS;

OLEIC ACID;

BACTERIAL ENZYME; CYTOCHROME P450; CYTOCHROME P450 153A; HYDROXY FATTY ACID; OLEIC ACID; OXIDOREDUCTASE; PUTIDAREDOXIN; UNCLASSIFIED DRUG; CYTOCHROME P-450 CYP153 (ACINETOBACTER); FERREDOXIN; MUTANT PROTEIN; PUTIDAREDOXIN REDUCTASE;

BACTERIUM; BIOENGINEERING; BIOTRANSFORMATION; CYTOCHROME; ELECTRON; ENZYME ACTIVITY; ESTER; FATTY ACID; GENE EXPRESSION; GENETIC ANALYSIS; MUTATION; POLYMER; PROTEIN;

ARTICLE; CELL TRANSFORMATION; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME SUBSTRATE; HYDROXYLATION; ITERATIVE SATURATION MUTAGENESIS; MARINOBACTER HYDROCARBONOCLASTICUS; MUTAGENESIS; NONHUMAN; PROTEIN EXPRESSION; PSEUDOMONAS PUTIDA; SITE DIRECTED MUTAGENESIS; WHOLE CELL; ENZYMOLOGY; GENETICS; MARINOBACTER; METABOLISM; PROTEIN ENGINEERING;

MARINOBACTER HYDROCARBONOCLASTICUS;

CYTOCHROME P-450 ENZYME SYSTEM; ELECTRON TRANSPORT; FERREDOXINS; HYDROXYLATION; MARINOBACTER; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; NADH, NADPH OXIDOREDUCTASES; OLEIC ACID; PROTEIN ENGINEERING;

EID: 84971012987     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-016-7634-1     Document Type: Article

References (40)

1. Abe A, Sugiyama K (2005) Growth inhibition and apoptosis induction of human melanoma cells by ω-hydroxy fatty acids. Anti-Cancer Drugs 16:543–549. doi:10.1097/00001813-200506000-00010
2. Adas F, Salaün J, Berthou F, Picart D, Simon B, Amet Y (1999) Requirement for ω and (ω–1)-hydroxylations of fatty acids by human cytochromes P450 2E1 and 4A11. J Lipid Res 40:1990–1997
3. Axarli I, Prigipaki A, Labrou NE (2005) Engineering the substrate specificity of cytochrome P450 CYP102A2 by directed evolution: production of an efficient enzyme for bioconversion of fine chemicals. Biomol Eng 22:81–88. doi:10.1016/j.bioeng.2004.11.003
4. Ba L, Li P, Zhang H, Duan Y, Lin Z (2013a) Engineering of a hybrid biotransformation system for cytochrome P450sca-2 in Escherichia coli. Biotechnol J 8:785–793. doi:10.1002/biot.201200097
5. Ba L, Li P, Zhang H, Duan Y, Lin Z (2013b) Semi-rational engineering of cytochrome P450sca-2 in a hybrid system for enhanced catalytic activity: Insights into the important role of electron transfer. Biotechnol Bioeng 110:2815–2825. doi:10.1002/bit.24960
6. Bae JH, Park BG, Jung E, Lee P-G, Kim B-G (2014) fadD deletion and fadL overexpression in Escherichia coli increase hydroxy long-chain fatty acid productivity. Appl Microbiol Biotechnol 98:8917–8925. doi:10.1007/s00253-014-5974-2
7. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124:128–145. doi:10.1016/j.jbiotec.2006.01.026
8. Bernhardt R, Gunsalus I (1992) Reconstitution of cytochrome P4502B4 (LM2) activity with camphor and linalool monooxygenase electron donors. Biochem Biophys Res Commun 187:310–317. doi:10.1016/S0006-291X(05)81494-9
9. Bhattarai S, Liou K, Oh T-J (2013) Hydroxylation of long chain fatty acids by CYP147F1, a new cytochrome P450 subfamily protein from Streptomyces peucetius. Arch Biochem Biophys 539:63–69. doi:10.1016/j.abb.2013.09.008
10. Biermann U, Friedt W, Lang S, Lühs W, Machmüller G, Metxger JO, Ruesch M, Schaefer HJ, Schneider MP (2000) New syntheses with oils and fats as renewable raw materials for the chemical industry. Angew Chem Int Ed 39:2206–2224. doi:10.1002/9783527619849.ch25
11. Budde M, Maurer SC, Schmid RD, Urlacher VB (2004) Cloning, expression and characterisation of CYP102A2, a self-sufficient P450 monooxygenase from Bacillus subtilis. Appl Microbiol Biotechnol 66:180–186. doi:10.1007/s00253-004-1719-y
12. Fasan R, Chen MM, Crook NC, Arnold FH (2007) Engineered alkane-hydroxylating cytochrome P450BM3 exhibiting nativelike catalytic properties. Angew Chem 119:8566–8570. doi:10.1002/ange.200702616
13. Glieder A, Farinas ET, Arnold FH (2002) Laboratory evolution of a soluble, self-sufficient, highly active alkane hydroxylase. Nat Biotechnol 20:1135–1139. doi:10.1038/nbt744
14. Guengerich FP (2002a) Cytochrome P450 enzymes in the generation of commercial products. Nat Rev Drug Discov 1:359–366. doi:10.1038/nrd792
15. Guengerich FP (2002b) Rate-limiting steps in cytochrome P450 catalysis. Biol Chem 383:1553–1564. doi:10.1515/BC.2002.175
16. Hannemann F, Bichet A, Ewen KM, Bernhardt R (2007) Cytochrome P450 systems—biological variations of electron transport chains. Biochim Biophys Acta 1770:330–344. doi:10.1016/j.bbagen.2006.07.017
17. Hoch U, Zhang Z, Kroetz DL, de Montellano PRO (2000) Structural determination of the substrate specificities and regioselectivities of the rat and human fatty acid ω-hydroxylases. Arch Biochem Biophys 373:63–71. doi:10.1006/abbi.1999.1504
18. Honda Malca S, Scheps D, Kuhnel L, Venegas-Venegas E, Seifert A, Nestl BM, Hauer B (2012) Bacterial CYP153A monooxygenases for the synthesis of omega-hydroxylated fatty acids. Chem Commun (Cambridge, UK) 48:5115–5117. doi:10.1039/c2cc18103g
19. Huf S, Kruegener S, Hirth T, Rupp S, Zibek S (2011) Biotechnological synthesis of long-chain dicarboxylic acids as building blocks for polymers. Eur J Lipid Sci Technol 113:548–561. doi:10.1002/ejlt.201000112
20. Kim D, Guengerich FP (2004) Selection of human cytochrome P450 1A2 mutants with enhanced catalytic activity for heterocyclic amine N-hydroxylation. Biochemistry 43:981–988. doi:10.1021/bi035593f
21. Kitazume T, Tanaka A, Takaya N, Nakamura A, Matsuyama S, Suzuki T, Shoun H (2002) Kinetic analysis of hydroxylation of saturated fatty acids by recombinant P450foxy produced by an Escherichia coli expression system. Eur J Biochem 269:2075–2082. doi:10.1046/j.1432-1033.2002.02855.x
22. Koo LS, Immoos CE, Cohen MS, Farmer PJ, Ortiz de Montellano PR (2002) Enhanced electron transfer and lauric acid hydroxylation by site-directed mutagenesis of CYP119. J Am Chem Soc 124:5684–5691. doi:10.1021/ja017174g
23. Kumar S, Sun L, Liu H, Muralidhara B, Halpert JR (2006) Engineering mammalian cytochrome P450 2B1 by directed evolution for enhanced catalytic tolerance to temperature and dimethyl sulfoxide. Protein Eng Des Sel 19:547–554. doi:10.1093/protein/gzl042
24. Kuznetsov VY, Poulos TL, Sevrioukova IF (2006) Putidaredoxin-to-cytochrome P450cam electron transfer: differences between the two reductive steps required for catalysis. Biochemistry 45:11934–11944. doi:10.1021/bi0611154
25. Labinger JA, Bercaw JE (2002) Understanding and exploiting C–H bond activation. Nature 417:507–514. doi:10.1038/417507a
26. Liu C, Liu F, Cai J, Xie W, Long TE, Turner R, Lyons A, Gross RA (2011) Polymers from fatty acids: poly(ω-hydroxyl tetradecanoic acid) synthesis and physico-mechanical studies. Biomacromolecules 12:3291–3298. doi:10.1021/bm2007554
27. Mouri T, Michizoe J, Ichinose H, Kamiya N, Goto M (2006) A recombinant Escherichia coli whole cell biocatalyst harboring a cytochrome P450cam monooxygenase system coupled with enzymatic cofactor regeneration. Appl Microbiol Biotechnol 72:514–520. doi:10.1007/s00253-005-0289-y
28. Ogura H, Nishida CR, Hoch UR, Perera R, Dawson JH, Ortiz de Montellano PR (2004) EpoK, a cytochrome P450 involved in biosynthesis of the anticancer agents epothilones A and B. Substrate-mediated rescue of a P450 enzyme. Biochemistry 43:14712–14721. doi:10.1021/bi048980d
29. Palecz B (2002) Enthalpic homogeneous pair interaction coefficients of l-α-amino acids as a hydrophobicity parameter of amino acid side chains. J Am Chem Soc 124:6003–6008. doi:10.1021/ja011937i
30. QuangáPham S (2012) Evolving P450pyr hydroxylase for highly enantioselective hydroxylation at non-activated carbon atom. Chem Commun 48:4618–4620. doi:10.1039/C2CC30779K
31. Reetz MT, Carballeira JD (2007) Iterative saturation mutagenesis (ISM) for rapid directed evolution of functional enzymes. Nat Protoc 2:891–903. doi:10.1038/nprot.2007.72
32. Reetz MT, Kahakeaw D, Lohmer R (2008) Addressing the numbers problem in directed evolution. ChemBioChem 9:1797–1804. doi:10.1002/cbic.200800298
33. Schallmey A, Den Besten G, Teune IG, Kembaren RF, Janssen DB (2011) Characterization of cytochrome P450 monooxygenase CYP154H1 from the thermophilic soil bacterium Thermobifida fusca. Appl Microbiol Biotechnol 89:1475–1485. doi:10.1007/s00253-010-2965-9
34. Scheps D, Honda Malca S, Richter SM, Marisch K, Nestl BM, Hauer B (2013) Synthesis of ω-hydroxy dodecanoic acid based on an engineered CYP153A fusion construct. Microb Biotechnol 6:694–707. doi:10.1111/1751-7915.12073
35. Scott EE, Spatzenegger M, Halpert JR (2001) A truncation of 2B subfamily cytochromes P450 yields increased expression levels, increased solubility, and decreased aggregation while retaining function. Arch Biochem Biophys 395:57–68. doi:10.1006/abbi.2001.2574
36. Tripathi S, Li H, Poulos TL (2013) Structural basis for effector control and redox partner recognition in cytochrome P450. Science 340:1227–1230. doi:10.1126/science.1235797
37. Urlacher VB, Eiben S (2006) Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol 24:324–330. doi:10.1016/j.tibtech.2006.05.002
38. Urlacher VB, Girhard M (2012) Cytochrome P450 monooxygenases: an update on perspectives for synthetic application. Trends Biotechnol 30:26–36. doi:10.1016/j.tibtech.2011.06.012
39. Xu F, Bell SG, Peng Y, Johnson EO, Bartlam M, Rao Z, Wong LL (2009) Crystal structure of a ferredoxin reductase for the CYP199A2 system from Rhodopseudomonas palustris. Proteins: Struct Funct Bioinf 77:867–880. doi:10.1002/prot.22510
40. Yang W, Bell SG, Wang H, Zhou W, Hoskins N, Dale A, Bartam M, Wong LL, Rao Z (2010) Molecular characterization of a class I P450 electron transfer system from Novosphingobium aromaticivorans DSM12444. J Biol Chem 285:27372–27384. doi:10.1074/jbc.M110.118349