Synthesis of morphinan alkaloids in Saccharomyces cerevisiae

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Fossati, Elena ^a   Narcross, Lauren ^a   Ekins, Andrew ^a   Falgueyret, Jean Pierre ^a   Martin, Vincent J J ^a  

^a Dept of Electrical and Computer Engineering   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID; CODEINE; CODEINE O DEMETHYLASE; CODEINONE; METHYLTRANSFERASE; MORPHINAN DERIVATIVE; MORPHINE; NEOPINE; RETICULINE; SALUTARIDINE REDUCTASE; SALUTARIDINE SYNTHASE; SALUTARIDINOL; SALUTARIDINOL 7 O ACETATE; SALUTARIDINOL ACETYLTRANSFERASE; TETRAHYDROPAPAVERINE; THEBAINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG STRUCTURE; DRUG SYNTHESIS; ENANTIOSELECTIVITY; ENZYME ACTIVITY; ENZYME SUBSTRATE; FEASIBILITY STUDY; NONHUMAN; PH; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; YEAST CELL; CHEMISTRY; FOURIER ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; STEREOISOMERISM;

PAPAVER SOMNIFERUM; SACCHAROMYCES CEREVISIAE;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FOURIER ANALYSIS; MASS SPECTROMETRY; MORPHINANS; SACCHAROMYCES CEREVISIAE; STEREOISOMERISM;

EID: 84928393363     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124459     Document Type: Article

References (36)

1. Biancofiore G. Oxycodone controlled release in cancer pain management. Ther Clin Risk Manag. 2006; 2: 229-234. PMID: 18360598
2. Millgate AG, Pogson BJ, Wilson IW, Kutchan TM, Zenk MH, Gerlach WL, et al. Analgesia: morphine-pathway block in top1 poppies. Nature. 2004; 431: 413-414. PMID: 15386001
3. INCB Supply of opiate raw materials and demand for opiates for medical and scientific purposes. Estim World Requir 2014 - Stat 2012: 2013; 3: 92-10. Available: http://www.incb.org/documents/Narcotic-Drugs/Technical-Publications/2012/NDR-2012-Part3-Supply-E.pdf. Accessed 30 September 2014.
4. Fossati E, Ekins A, Narcross L, Zhu Y, Falgueyret J-P, Beaudoin GAW, et al. Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat Commun. 2014; 5: 3283. Available: doi: 10.1038/ncomms4283 Accessed 27 July 2014. PMID: 24513861
5. Thodey K, Galanie S, Smolke CD. A microbial biomanufacturing platform for natural and semisynthetic opioids. Nat Chem Biol 2014; 10: 837-844. Available: doi: 10.1038/nchembio.1613 PMID: 25151135
6. Nakagawa A, Minami H, Kim J-S, Koyanagi T, Katayama T, Sato F, et al. Bench-top fermentative production of plant benzylisoquinoline alkaloids using a bacterial platform. Bioeng Bugs. 2012; 3: 49-53. doi: 10.1038/ncomms1327 PMID: 22179145
7. De Luca V, Salim V, Atsumi SM, Yu F. Mining the biodiversity of plants: a revolution in the making. Science. 2012; 336: 1658-1661. doi: 10.1126/science.1217410 PMID: 22745417
8. Hagel JM, Facchini PJ. Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol. 2013; 54: 647-672. doi: 10.1093/pcp/pct020 PMID: 23385146
9. Beaudoin GAW, Facchini PJ. Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta. 2014; 240: 19-32. doi: 10.1007/s00425-014-2056-8 PMID: 24671624
10. Ilari A, Franceschini S, Bonamore A, Arenghi F, Botta B, Macone A, et al. Structural basis of enzymatic (S)-norcoclaurine biosynthesis. J Biol Chem. 2009; 284: 897-904. doi: 10.1074/jbc.M803738200 PMID: 19004827
11. Hirata K, Poeaknapo C, Schmidt J, Zenk MH. 1,2-Dehydroreticuline synthase, the branch point enzyme opening the morphinan biosynthetic pathway. Phytochemistry. 2004; 65: 1039-1046. PMID: 15110683
12. De-Eknamkul W, Zenk MH. Purification and properties of 1,2-dehydroreticuline reductase from Papaver somniferum seedlings. Phytochemistry. 1992; 31: 813-821.
13. Hawkins KM, Smolke CD. Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol. 2008; 4: 564-573. doi: 10.1038/nchembio.105 PMID: 18690217
14. Nakagawa A, Matsuzaki C, Matsumura E, Koyanagi T, Katayama T, Yamamoto K, et al. (R,S)-Tetrahydropapaveroline production by stepwise fermentation using engineered Escherichia coli. Sci Rep. 2014; 4: 6695. Available: doi: 10.1038/srep06695 Accessed 12 November 2014. PMID: 25331563
15. Jansen G, Wu C, Schade B, Thomas DY, Whiteway M. Drag&Drop cloning in yeast. Gene. 2005; 344: 43-51. PMID: 15656971
16. Shao Z, Zhao H, Zhao H. DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res. 2009; 37: e16. Available: doi: 10.1093/nar/gkn991 Accessed 24 July 2014. PMID: 19074487
17. Gietz RD, Schiestl RH. Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007; 2: 1-4. PMID: 17401330
18. Nakagawa A, Minami H, Kim J-S, Koyanagi T, Katayama T, Sato F, et al. A bacterial platform for fermentative production of plant alkaloids. Nat Commun. 2011; 2: 326-328. Available: http://dx.doi.org/10.1038/ncomms1327. Accessed 30 September, 2014. doi: 10.1038/ncomms1327 PMID: 21610729
19. Gesell A, Rolf M, Ziegler J, Díaz Chávez ML, Huang F-C, Kutchan TM. CYP719B1 is salutaridine synthase, the C-C phenol-coupling enzyme of morphine biosynthesis in opium poppy. J Biol Chem. 2009; 284: 24432-24442. doi: 10.1074/jbc.M109.033373 PMID: 19567876
20. Facchini PJ, Penzes C, Johnson AG, Bull D. Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol. 1996; 112: 1669-1677. PMID: 8972604
21. Fisinger U, Grobe N, Zenk MH. Thebaine synthase: a new enzyme in the morphine pathway in P. somniferum. Nat Prod Commun. 2007; 2: 249-253.
22. Theuns HG, Lenting HBM, Salemink CA, Tanaka H, Shibata M, Ito K, et al. Neodihydrothebaine and bractazonine, two dibenz[d,f]azonine alkaloids of Papaver bracteatum. Phytochemistry. 1984; 23: 1157-1166.
23. Gerardy R, Zenk MH. Purification and characterization of salutaridine: NADPH 7-oxidoreductasefrom papaver somniferum. Phytochemistry. 1993; 34: 125-132.
24. Hagel JM, Facchini PJ. Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat Chem Biol. 2010; 6: 273-275. doi: 10.1038/nchembio.317 PMID: 20228795
25. Facchini PJ, Bohlmann J, Covello PS, De Luca V, Mahadevan R, Page GE, et al. Synthetic biosystems for the production of high-value plant metabolites. Trends Biotechnol. 2012; 30: 127-131. doi: 10.1016/j.tibtech.2011.10.001 PMID: 22209518
26. Kraus PF, Kutchan TM. Molecular cloning and heterologous expression of a cDNA encoding berbamunine synthase, a C-O phenol-coupling cytochrome P450 from the higher plant Berberis stolonifera. Proc Natl Acad Sci USA. 1995; 92: 2071-2075. PMID: 7892226
27. Sabarna K. Approaches to isolating a cDNA encoding thebaine synthase of morphine biosynthesis from opium poppy Papaver somniferum. PhD thesis, Martin Luther University Halle-Wittenberg. 2006. Available: http://www.dart-europe.eu/full.php?id=44110. Accessed: 26 August 2014.
28. Aabo T, Glückstad J, Siegumfeldt H, Arneborg N. Intracellular pH distribution as a cell health indicator in Saccharomyces cerevisiae. J R Soc Interface. 2011; 8: 1635-1643. Available: doi: 10.1098/rsif.2011.0148 Accessed 8 March 2014. PMID: 21527496
29. Ziegler J, Brandt W, Geissler R, Facchini PJ. Removal of substrate inhibition and increase in maximal velocity in the short chain dehydrogenase/reductase salutaridine reductase involved in morphine biosynthesis. J Biol Chem. 2009; 284: 26758-26767. doi: 10.1074/jbc.M109.030957 PMID: 19648114
30. Weng J-K, Philippe RN, Noel JP. The rise of chemodiversity in plants. Science. 2012; 336: 1667-1670. doi: 10.1126/science.1217411 PMID: 22745420
31. Farrow SC, Facchini PJ. Dioxygenases catalyze O-demethylation and O,O-demethylenation with widespread roles in benzylisoquinoline alkaloid metabolism in opium poppy. J Biol Chem. 2013; 288: 28997-29012. doi: 10.1074/jbc.M113.488585 PMID: 23928311
32. Unterlinner B, Lenz R, Kutchan TM. Molecular cloning and functional expression of codeinone reductase: the penultimate enzyme in morphine biosynthesis in the opium poppy Papaver somniferum. Plant J. 1999; 18: 465-475. PMID: 10417697
33. Ziegler J, Facchini PJ. Alkaloid biosynthesis: metabolism and trafficking. Annu Rev Plant Biol. 2008; 59: 735-769. doi: 10.1146/annurev.arplant.59.032607.092730 PMID: 18251710
34. Kim EY, Tullman-Ercek D. A rapid flow cytometry assay for the relative quantification of protein encapsulation into bacterial microcompartments. Biotechnol J. 2014; 9: 348-354. doi: 10.1002/biot.201300391 PMID: 24323373
35. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, et al. Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol. 2009; 27: 753-759. doi: 10.1038/nbt.1557 PMID: 19648908
36. Xiao M, Zhang Y, Chen X, Lee E-J, Barber CJS, Chakrabarty R, et al. Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J Biotechnol. 2013; 166: 122-134. doi: 10.1016/j.jbiotec.2013.04.004 PMID: 23602801