Cytochrome P450-mediated metabolic engineering: Current progress and future challenges

Current Opinion in Plant Biology

Volumn 19, Issue , 2014, Pages 27-34

  Renault, Hugues ^a,b   Bassard, Jean Etienne ^c   Hamberger, Björn ^c   Werck Reichhart, Danièle ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISINIC ACID; ARTEMISININ DERIVATIVE; CYTOCHROME P450;

COLOR; FLOWER; METABOLIC ENGINEERING; METABOLISM;

ARTEMISININS; COLOR; CYTOCHROME P-450 ENZYME SYSTEM; FLOWERS; METABOLIC ENGINEERING;

EID: 84897553187     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.03.004     Document Type: Review

References (65)

1. Nebert D.W., Wikvall K., Miller W.L. Human cytochromes P450 in health and disease. Philos Trans R Soc Lond B: Biol Sci 2013, 368:20120431.
2. Newman D.J., Cragg G.M. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 2012, 75:311-335.
3. Rischer H., Hakkinen S.T., Ritala A., Seppanen-Laakso T., Miralpeix B., Capell T., Christou P., Oksman-Caldentey K.M. Plant cells as pharmaceutical factories. Curr Pharm Des 2013, 19:5640-5660.
4. Bak S., Beisson F., Bishop G., Hamberger B., Hofer R., Paquette S., Werck-Reichhart D. Cytochromes P450. Arabidopsis Book 2011, 9:e0144.
5. Guengerich F.P., Isin E.M. Unusual cytochrome P450 enzymes and reactions. Handbook of Metabolic Pathways of Xenobiotics 2014, vol 1. John Wiley and Sons.
6. Hamberger B., Bak S. Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos Trans R Soc Lond B: Biol Sci 2013, 368:20120426.
7. Kumar S. Engineering cytochrome P450 biocatalysts for biotechnology, medicine and bioremediation. Expert Opin Drug Metab Toxicol 2010, 6:115-131.
8. Powles S.B., Yu Q. Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 2010, 61:317-347.
9. Didierjean L., Gondet L., Perkins R., Lau S.M., Schaller H., O'Keefe D.P., Werck-Reichhart D. Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol 2002, 130:179-189.
10. Rylott E.L., Jackson R.G., Sabbadin F., Seth-Smith H.M., Edwards J., Chong C.S., Strand S.E., Grogan G., Bruce N.C. The explosive-degrading cytochrome P450 XplA: biochemistry, structural features and prospects for bioremediation. Biochim Biophys Acta 2011, 1814:230-236.
11. Zhang Y., Liu J., Zhou Y., Gong T., Wang J., Ge Y. Enhanced phytoremediation of mixed heavy metal (mercury)-organic pollutants (trichloroethylene) with transgenic alfalfa co-expressing glutathione S-transferase and human P450 2E1. J Hazard Mater 2013, 260:1100-1107.
12. Shimazu S., Inui H., Ohkawa H. Phytomonitoring and phytoremediation of agrochemicals and related compounds based on recombinant cytochrome P450s and aryl hydrocarbon receptors (AhRs). J Agric Food Chem 2011, 59:2870-2875.
13. Li J., Yu H., Zhang F., Lin C., Gao J., Fang J., Ding X., Shen Z., Xu X. A built-in strategy to mitigate transgene spreading from genetically modified corn. PLOS ONE 2013, 8:e81645.
14. Paddon C.J., Westfall P.J., Pitera D.J., Benjamin K., Fisher K., McPhee D., Leavell M.D., Tai A., Main A., Eng D., et al. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496:528-532.
15. Teoh K.H., Polichuk D.R., Reed D.W., Nowak G., Covello P.S. Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett 2006, 580:1411-1416.
16. Ro D.K., Paradise E.M., Ouellet M., Fisher K.J., Newman K.L., Ndungu J.M., Ho K.A., Eachus R.A., Ham T.S., Kirby J., et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440:940-943.
17. Westfall P.J., Pitera D.J., Lenihan J.R., Eng D., Woolard F.X., Regentin R., Horning T., Tsuruta H., Melis D.J., Owens A., et al. Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin. Proc Natl Acad Sci U S A 2012, 109:E111-E118.
18. Keasling J.D. Synthetic biology and the development of tools for metabolic engineering. Metab Eng 2012, 14:189-195.
19. Tanaka Y., Brugliera F. Flower colour and cytochromes P450. Philos Trans R Soc Lond B: Biol Sci 2013, 368:20120432.
20. de Vetten N., ter Horst J., van Schaik H.P., de Boer A., Mol J., Koes R. A cytochrome b5 is required for full activity of flavonoid 3',5'-hydroxylase, a cytochrome P450 involved in the formation of blue flower colors. Proc Natl Acad Sci U S A 1999, 96:778-783.
21. Noda N., Aida R., Kishimoto S., Ishiguro K., Fukuchi-Mizutani M., Tanaka Y., Ohmiya A. Genetic engineering of novel bluer-colored chrysanthemums produced by accumulation of delphinidin-based anthocyanins. Plant Cell Physiol 2013, 54:1684-1695.
22. Nakamura N., Fukuchi-Mizutani M., Fukui Y., Ishiguro K., Suzuki K., Suzuki H., Okazaki K., Shibata D., Tanaka Y. Generation of pink flower varieties from blue Torenia hybrida by redirecting the flavonoid biosynthetic pathway from delphinidin to pelargonidin. Plant Biotechnol 2010, 27:375-383.
23. Boase M.R., Lewis D.H., Davies K.M., Marshall G.B., Patel D., Schwinn K.E., Deroles S.C. Isolation and antisense suppression of flavonoid 3',5'-hydroxylase modifies flower pigments and colour in cyclamen. BMC Plant Biol 2010, 10:107.
24. Munro A.W., Girvan H.M., Mason A.E., Dunford A.J., McLean K.J. What makes a P450 tick?. Trends Biochem Sci 2013, 38:140-150.
25. Guengerich F.P., Munro A.W. Unusual cytochrome P450 enzymes and reactions. J Biol Chem 2013, 288:17065-17073.
26. Park S., Kim Y.S., Rupasinghe S.G., Schuler M.A., Back K. Rice P450 reductases differentially affect P450-mediated metabolism in bacterial expression systems. Bioprocess Biosyst Eng 2013, 36:325-331.
27. Neunzig I., Widjaja M., Peters F.T., Maurer H.H., Hehn A., Bourgaud F., Bureik M. Coexpression of CPR from various origins enhances biotransformation activity of human CYPs in S. pombe. Appl Biochem Biotechnol 2013, 170:1751-1766.
28. Brugliera F., Tao G.Q., Tems U., Kalc G., Mouradova E., Price K., Stevenson K., Nakamura N., Stacey I., Katsumoto Y., et al. Violet/blue chrysanthemums-metabolic engineering of the anthocyanin biosynthetic pathway results in novel petal colors. Plant Cell Physiol 2013, 54:1696-1710.
29. Bassard J.E., Mutterer J., Duval F., Werck-Reichhart D. A novel method for monitoring the localization of cytochromes P450 and other endoplasmic reticulum membrane associated proteins: a tool for investigating the formation of metabolons. FEBS J 2012, 279:1576-1583.
30. Ajikumar P.K., Xiao W.H., Tyo K.E., Wang Y., Simeon F., Leonard E., Mucha O., Phon T.H., Pfeifer B., Stephanopoulos G. Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science 2010, 330:70-74.
31. Schuckel J., Rylott E.L., Grogan G., Bruce N.C. A gene-fusion approach to enabling plant cytochromes p450 for biocatalysis. Chembiochem 2012, 13:2758-2763.
32. Ba L., Li P., Zhang H., Duan Y., Lin Z. 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 2013, 110:2815-2825.
33. Jensen K., Johnston J.B., de Montellano P.R., Moller B.L. Photosystem I from plants as a bacterial cytochrome P450 surrogate electron donor: terminal hydroxylation of branched hydrocarbon chains. Biotechnol Lett 2012, 34:239-245.
34. Nielsen A.Z., Ziersen B., Jensen K., Lassen L.M., Olsen C.E., Moller B.L., Jensen P.E. Redirecting photosynthetic reducing power toward bioactive natural product synthesis. ACS Synth Biol 2013, 2:308-315.
35. Tran N.H., Nguyen D., Dwaraknath S., Mahadevan S., Chavez G., Nguyen A., Dao T., Mullen S., Nguyen T.A., Cheruzel L.E. An efficient light-driven P450 BM3 biocatalyst. J Am Chem Soc 2013, 135:14484-14487.
36. Lee S.H., Kwon Y.C., Kim D.M., Park C.B. Cytochrome P450-catalyzed O-dealkylation coupled with photochemical NADPH regeneration. Biotechnol Bioeng 2013, 110:383-390.
37. Norholm M.H., Toddo S., Virkki M.T., Light S., von Heijne G., Daley D.O. Improved production of membrane proteins in Escherichia coli by selective codon substitutions. FEBS Lett 2013, 587:2352-2358.
38. Goodman D.B., Church G.M., Kosuri S. Causes and effects of N-terminal codon bias in bacterial genes. Science 2013, 342:475-479.
39. Gavira C., Hofer R., Lesot A., Lambert F., Zucca J., Werck-Reichhart D. Challenges and pitfalls of P450-dependent (+)-valencene bioconversion by Saccharomyces cerevisiae. Metab Eng 2013, 18:25-35.
40. Höfer R., Dong L., Andre F., Ginglinger J.F., Lugan R., Gavira C., Grec S., Lang G., Memelink J., Van Der Krol S., 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, 20C:221-232.
41. Dai Z., Liu Y., Zhang X., Shi M., Wang B., Wang D., Huang L., Zhang X. Metabolic engineering of Saccharomyces cerevisiae for production of ginsenosides. Metab Eng 2013, 20:146-156.
42. Guo J., Zhou Y.J., Hillwig M.L., Shen Y., Yang L., Wang Y., Zhang X., Liu W., Peters R.J., Chen X., et al. CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc Natl Acad Sci U S A 2013, 110:12108-12113.
43. Fukushima E.O., Seki H., Sawai S., Suzuki M., Ohyama K., Saito K., Muranaka T. Combinatorial biosynthesis of legume natural and rare triterpenoids in engineered yeast. Plant Cell Physiol 2013, 54:740-749.
44. Moses T., Pollier J., Thevelein J.M., Goossens A. Bioengineering of plant (tri)terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol 2013, 200:27-43.
45. 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.
46. Wollenberg L.A., Jett J.E., Wu Y., Flora D.R., Wu N., Tracy T.S., Gannett P.M. Selective filling of nanowells in nanowell arrays fabricated using polystyrene nanosphere lithography with cytochrome P450 enzymes. Nanotechnology 2012, 23:385101.
47. Wollenberg L.A., Kabulski J.L., Powell M.J., Chen J., Flora D.R., Tracy T.S., Gannett P.M. The use of immobilized cytochrome P4502C9 in PMMA-based plug flow bioreactors for the production of drug metabolites. Appl Biochem Biotechnol 2013, 1-14.
48. Bayburt T.H., Sligar S.G. Membrane protein assembly into nanodiscs. FEBS Lett 2010, 584:1721-1727.
49. Laursen T., Naur P., Moller B.L. Amphipol trapping of a functional CYP system. Biotechnol Appl Biochem 2013, 60:119-127.
50. Tissier A. Glandular trichomes: what comes after expressed sequence tags?. Plant J 2012, 70:51-68.
51. Lange B.M., Turner G.W. Terpenoid biosynthesis in trichomes-current status and future opportunities. Plant Biotechnol J 2013, 11:2-22.
52. Ginglinger J.F., Boachon B., Hofer R., Paetz C., Kollner T.G., Miesch L., Lugan R., Baltenweck R., Mutterer J., Ullmann P., et al. Gene coexpression analysis reveals complex metabolism of the monoterpene alcohol linalool in arabidopsis flowers. Plant Cell 2013.
53. Nguyen T.D., MacNevin G., Ro D.K. De novo synthesis of high-value plant sesquiterpenoids in yeast. Methods Enzymol 2012, 517:261-278.
54. Siriphongphaew A., Pisnupong P., Wongkongkatep J., Inprakhon P., Vangnai A.S., Honda K., Ohtake H., Kato J., Ogawa J., Shimizu S., et al. Development of a whole-cell biocatalyst co-expressing P450 monooxygenase and glucose dehydrogenase for synthesis of epoxyhexane. Appl Microbiol Biotechnol 2012, 95:357-367.
55. Janocha S., Bernhardt R. Design and characterization of an efficient CYP105A1-based whole-cell biocatalyst for the conversion of resin acid diterpenoids in permeabilized Escherichia coli. Appl Microbiol Biotechnol 2013, 97:7639-7649.
56. Jensen K., Jensen P.E., Moller B.L. Light-driven cytochrome P450 hydroxylations. ACS Chem Biol 2011, 6:533-539.
57. van der Felt C., Hindoyan K., Choi K., Javdan N., Goldman P., Bustos R., Star A.G., Hunter B.M., Hill M.G., Nersissian A., et al. Electron-transfer rates govern product distribution in electrochemically-driven P450-catalyzed dioxygen reduction. J Inorg Biochem 2011, 105:1350-1353.
58. Sadeghi S.J., Fantuzzi A., Gilardi G. Breakthrough in P450 bioelectrochemistry and future perspectives. Biochim Biophys Acta 2011, 1814:237-248.
59. Schneider E., Clark D.S. Cytochrome P450 (CYP) enzymes and the development of CYP biosensors. Biosens Bioelectron 2013, 39:1-13.
60. Alonso-Gutierrez J., Chan R., Batth T.S., Adams P.D., Keasling J.D., Petzold C.J., Lee T.S. Metabolic engineering of Escherichia coli for limonene and perillyl alcohol production. Metab Eng 2013, 19:33-41.
61. Tattersall D.B., Bak S., Jones P.R., Olsen C.E., Nielsen J.K., Hansen M.L., Hoj P.B., Moller B.L. Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science 2001, 293:1826-1828.
62. Jung S.T., Lauchli R., Arnold F.H. Cytochrome P450: taming a wild type enzyme. Curr Opin Biotechnol 2011, 22:809-817.
63. McIntosh J.A., Coelho P.S., Farwell C.C., Wang Z.J., Lewis J.C., Brown T.R., Arnold F.H. Enantioselective intramolecular C-H amination catalyzed by engineered cytochrome P450 enzymes in vitro and in vivo. Angew Chem Int Ed Engl 2013, 52:9309-9312.
64. Dietrich J.A., Yoshikuni Y., Fisher K.J., Woolard F.X., Ockey D., McPhee D.J., Renninger N.S., Chang M.C., Baker D., Keasling J.D. A novel semi-biosynthetic route for artemisinin production using engineered substrate-promiscuous P450(BM3). ACS Chem Biol 2009, 4:261-267.
65. Koopman F., Beekwilder J., Crimi B., van Houwelingen A., Hall R.D., Bosch D., van Maris A.J., Pronk J.T., Daran J.M. De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae. Microb Cell Fact 2012, 11:155.