Expanding P450 catalytic reaction space through evolution and engineering

Current Opinion in Chemical Biology

Volumn 19, Issue 1, 2014, Pages 126-134

  McIntosh, John A ^a   Farwell, Christopher C ^a   Arnold, Frances H ^a  

^a California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CYTOCHROME P450; HYDROGEN;

BIOCATALYSIS; COVALENT BOND; ENZYME ENGINEERING; ENZYME KINETICS; ENZYME METABOLISM; HUMAN; MOLECULAR EVOLUTION; REVIEW; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN ENGINEERING;

BIOCATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; OXIDATION-REDUCTION; PROTEIN ENGINEERING;

EID: 84896520980     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2014.02.001     Document Type: Review

References (46)

1. Keasling J.D., Mendoza A., Baran P.S. Synthesis: a constructive debate. Nature 2012, 492:188-189.
2. Blomberg R., Kries H., Pinkas D.M., Mittl P.R., Grütter M.G., Privett H.K., Mayo S.L., Hilvert D. Precision is essential for efficient catalysis in an evolved Kemp eliminase. Nature 2013, 503:418-421.
3. Siegel J.B., Zanghellini A., Lovick H.M., Kiss G., Lambert A.R., St Clair J.L., Gallaher J.L., Hilvert D., Gelb M.H., Stoddard B.L., Houk K.N., et al. Computational design of an enzyme catalyst for a stereoselective bimolecular Diels-Alder reaction. Science 2010, 329:309-313.
4. Gerlt J.A., Babbitt P.C. Enzyme (re)design: lessons from natural evolution and computation. Curr Opin Chem Biol 2009, 13:10-18.
5. Glasner M.E., Gerlt J.A., Babbitt P.C. Evolution of enzyme superfamilies. Curr Opin Chem Biol 2006, 10:492-497.
6. Dellus-Gur E., Toth-Petroczy A., Elias M., Tawfik D.S. What makes a protein fold amenable to functional innovation? Fold polarity and stability trade-offs. J Mol Biol 2013, 425:2609-2621.
7. Guengerich F.P., Munro A.W. Unusual cytochrome P450 enzymes and reactions. J Biol Chem 2013, 288:17065-17073.
8. Guengerich F.P. Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 2001, 14:611-650.
9. Podust L.M., Sherman D.H. Diversity of P450 enzymes in the biosynthesis of natural products. Nat Prod Rep 2012, 29:1251-1266.
10. Whitehouse C.J., Bell S.G., Wong L.L. P450BM3 (CYP102A1): connecting the dots. Chem Soc Rev 2012, 41:1218-1260.
11. Krest C.M., Onderko E.L., Yosca T.H., Calixto J.C., Karp R.F., Livada J., Rittle J., Green M.T. Reactive intermediates in cytochrome P450 catalysis. J Biol Chem 2013, 288:17074-17081.
12. Green M.T. CH bond activation in heme proteins: the role of thiolate ligation in cytochrome P450. Curr Opin Chem Biol 2009, 13:84-88.
13. Fasan R. Tuning P450 enzymes as oxidation catalysts. ACS Catal 2012, 2:647-666.
14. De Voss J.J., Cryle M.J. Is the ferric hydroperoxy species responsible for sulfur oxidation in cytochrome P450s?. Angew Chem Int Ed Engl 2006, 45:8221-8223.
15. Jin S., Markris T.M., Bryson T.A., Sligar S.G., Dawson J.H. Epoxidation of olefins by hydroperoxo-ferric cytochrome P450. J Am Chem Soc 2003, 125:3406-3407.
16. Barry S.M., Kers J.A., Johnson E.G., Song L., Aston P.R., Patel B., Krasnoff S.B., Crane B.R., Gibson D.M., Loria R., Challis G.L. Cytochrome P450-catalyzed l-tryptophan nitration in thaxtomin phytotoxin biosynthesis. Nat Chem Biol 2012, 8:814-816.
17. He J., Muller M., Hertweck C. Formation of the aureothin tetrahydrofuran ring by a bifunctional cytochrome P450 monooxygenase. J Am Chem Soc 2004, 126:16742-16743.
18. Henrot M., Richter M.E., Maddaluno J., Hertweck C., De Paolis M. Convergent asymmetric synthesis of (+)-aureothin employing an oxygenase-mediated resolution step. Angew Chem Int Ed Engl 2012, 51:9587-9591.
19. Richter M., Busch B., Ishida K., Moore B.S., Hertweck C. Pyran formation by an atypical CYP-mediated four-electron oxygenation-cyclization cascade in an engineered aureothin pathway. ChemBioChem 2012, 13:2196-2199.
20. Zocher G., Richter M.E., Mueller U., Hertweck C. Structural fine-tuning of a multifunctional cytochrome P450 monooxygenase. J Am Chem Soc 2011, 133:2292-2302.
21. Zhang Q., Li H., Li S., Zhu Y., Zhang G., Zhang H., Zhang W., Shi R., Zhang C. Carboxyl formation from methyl via triple hydroxylations by XiaM in xiamycin A biosynthesis. Org Lett 2012, 14:6142-6145.
22. Höfer R., Dong L., Andre F., Ginglinger J.F., Lugan R., Gavira C., Grec S., Lang G., Memelink J., Van Der Krol S., Bouwmeester H., et al. Geraniol hydroxylase and hydroxygeraniol oxidase activities of the CYP76 family of cytochrome P450 enzymes and potential for engineering the early steps of the (seco)iridoid pathway. Metab Eng 2013.
23. Bell S.G., Zhou R., Yang W., Tan A.B., Gentleman A.S., Wong L.L., Zhou W. Investigation of the substrate range of CYP199A4: modification of the partition between hydroxylation and desaturation activities by substrate and protein engineering. Chemistry 2012, 18:16677-16688.
24. Rude M.A., Baron T.S., Brubaker S., Alibhai M., Del Cardayre S.B., Schirmer A. Terminal olefin (1-alkene) biosynthesis by a novel P450 fatty acid decarboxylase from jeotgalicoccus species. Appl Environ Microbiol 2011, 77:1718-1727.
25. Li Z., Rupasinghe S.G., Schuler M.A., Nair S.K. Crystal structure of a phenol-coupling P450 monooxygenase involved in teicoplanin biosynthesis. Proteins 2011, 79:1728-1738.
26. Cryle M.J., Staaden J., Schlichting I. Structural characterization of CYP165D3, a cytochrome P450 involved in phenolic coupling in teicoplanin biosynthesis. Arch Biochem Biophys 2011, 507:163-173.
27. Schmartz P.C., Wolfel K., Zerbe K., Gad E., El Tamany el S., Ibrahim H.K., Abou-Hadeed K., Robinson J.A. Substituent effects on the phenol coupling reaction catalyzed by the vancomycin biosynthetic P450 enzyme OxyB. Angew Chem Int Ed Engl 2012, 51:11468-11472.
28. 2) complex as a highly efficient oxidant in sulfoxidation reactions: revival of an underrated oxidant in cytochrome P450. J Chem Theory Comput 2013, 9:2519-2525.
29. Li C., Zhang L., Zhang C., Hirao H., Wu W., Shaik S. Which oxidant is really responsible for sulfur oxidation by cytochrome P450?. Angew Chem Int Ed Engl 2007, 46:8168-8170.
30. Gregory M., Mak P.J., Sligar S.G., Kincaid J.R. Differential hydrogen bonding in human CYP17 dictates hydroxylation versus lyase chemistry. Angew Chem Int Ed Engl 2013, 52:5342-5345.
31. Qiu Y., Tittiger C., Wicker-Thomas C., Le Goff G., Young S., Wajnberg E., Fricaux T., Taquet N., Blomquist G.J., Feyereisen R. An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci USA 2012, 109:14858-14863.
32. 2. Proc Natl Acad Sci U S A 1994, 91:10000-10004.
33. Breslow R., Gellman S.H. Tosylamidation of cyclohexane by a cytochrome P-450 model. J Chem Soc Chem Commun 1982, 1400-1401.
34. Svastits E.W., Dawson J.H., Breslow R., Gellman S.H. Functionalized nitrogen atom transfer catalyzed by cytochrome P450. J Am Chem Soc 1985, 107:6427-6428.
35. Wolf J.R., Hamaker C.G., Djukic J.P., Kodadek T., Woo L.K. Shape and stereoselective cyclopropanation of alkenes catalyzed by iron porphyrins. J Am Chem Soc 1995, 117:9194-9199.
36. Coelho P.S., Brustad E.M., Kannan A., Arnold F.H. Olefin cyclopropanation via carbene transfer catalyzed by engineered cytochrome P450 enzymes. Science 2013, 339:307-310.
37. Coelho P.S., Wang Z.J., Ener M.E., Baril S.A., Kannan A., Arnold F.H., Brustad E.M. A serine-substituted P450 catalyzes highly efficient carbene transfer to olefins in vivo. Nat Chem Biol 2013, 9:485-487.
38. McIntosh J.A., Coelho P.S., Farwell C.C., Wang Z.J., Lewis J.C., Brown T.R., Arnold F.H. Enantioselective intramolecular CH amination catalyzed by engineered cytochrome P450 enzymes in vitro and in vivo. Angew Chem Int Ed Engl 2013, 52:9309-9312.
39. Ruppel J.V., Kamble R.M., Zhang X.P. Cobalt-catalyzed intramolecular CH amination with arylsulfonyl azides. Org Lett 2007, 9:4889-4892.
40. Wang Z.J., Peck N.E., Renata H., Arnold F.H. Cytochrome P450 catalysed insertion of carbenoids into NH bonds. Chem Sci 2014, [Epub ahead of print].
41. Lewis J.C., Coelho P.S., Arnold F.H. Enzymatic functionalization of carbon-hydrogen bonds. Chem Soc Rev 2011, 40:2003-2021.
42. Muller A., Sturmer R., Hauer B., Rosche B. Stereospecific alkyne reduction: novel activity of old yellow enzymes. Angew Chem Int Ed Engl 2007, 46:3316-3318.
43. Hasnaoui-Dijoux G., Majeric Elenkov M., Lutje Spelberg J.H., Hauer B., Janssen D.B. Catalytic promiscuity of halohydrin dehalogenase and its application in enantioselective epoxide ring opening. ChemBioChem 2008, 9:1048-1051.
44. Savile C.K., Magloire V.P., Kazlauskas R.J. Subtilisin-catalyzed resolution of N-acyl arylsulfinamides. J Am Chem Soc 2005, 127:2104-2113.
45. Huisman G.W., Collier S.J. On the development of new biocatalytic processes for practical pharmaceutical synthesis. Curr Opin Chem Biol 2013, 17:284-292.
46. Harris D.C., Jewett M.C. Cell-free biology: exploiting the interface between synthetic biology and synthetic chemistry. Curr Opin Biotechnol 2012, 23:672-678.