Isolation and characterization of a cDNA encoding (S)-cis-N-methylstylopine 14-hydroxylase from opium poppy, a key enzyme in sanguinarine biosynthesis

Biochemical and Biophysical Research Communications

Volumn 431, Issue 3, 2013, Pages 597-603

  Beaudoin, Guillaume A W ^a   Facchini, Peter J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Benzo c phenenthridine alkaloid; Benzylisoquinoline alkaloid; Cytochrome P450; Plant specialized metabolism; Protopine alkaloid; Sanguinarine biosynthesis

Indexed keywords

BENZYLISOQUINOLINE DERIVATIVE; COMPLEMENTARY DNA; N METHYLSTYLOPINE 14 HYDROXYLASE; OPIATE; OXYGENASE; PROTOPINE 6 HYDROXYLASE; SANGUINARINE; STYLOPINE; UNCLASSIFIED DRUG;

ARTICLE; CELL SUSPENSION; CONTROLLED STUDY; DRUG ISOLATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

BENZOPHENANTHRIDINES; CYTOCHROME P-450 ENZYME SYSTEM; DNA, COMPLEMENTARY; ISOQUINOLINES; OPIUM; PAPAVER; PHYLOGENY; PLANT PROTEINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

PAPAVER SOMNIFERUM; PAPAVERACEAE; SACCHAROMYCES CEREVISIAE;

EID: 84873735095     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.129     Document Type: Article

References (36)

1. Wittstock U., Gershenzon J. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 2002, 5:300-307.
2. Bednarek P., Osbourn A. Plant-microbe interactions: chemical diversity in plant defense. Science 2009, 324:746-748.
3. Pichersky E., Gershenzon J. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 2002, 5:237-243.
4. Ziegler J., Facchini P.J. Alkaloid biosynthesis: metabolism and trafficking. Annu. Rev. Plant Biol. 2008, 59:735-769.
5. Barken I., Geller J., Rogosnitzky M. Noscapine inhibits human prostate cancer progression and metastasis in a mouse model. Anticancer Res. 2008, 28:3701-3704.
6. Pauli H.H., Kutchan T.M. Molecular cloning and functional heterologous expression of two alleles encoding (S)-N-methylcoclaurine 3'-hydroxylase (CYP80B1), a new methyl jasmonate-inducible cytochrome P450-dependent monooxygenase of benzylisoquinoline alkaloid biosynthesis. Plant J. 1998, 53:793-801.
7. Huang F.C., Kutchan T.M. Distribution of morphinan and benzo[c]phenanthridine alkaloid gene transcript accumulation in Papaver somniferum. Phytochemistry 2000, 53:555-564.
8. Dittrich H., Kutchan T.M. Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack. Proc. Natl. Acad. Sci. USA 1991, 88:9969-9973.
9. Facchini P.J., Penzes C., Johnson A.G., Bull D. Molecular characterization of berberine bridge enzyme genes from opium poppy. Plant Physiol. 1996, 112:1669-1677.
10. Mizutani M., Sato F. Unusual P450 reactions in plant secondary metabolism. Arch. Biochem. Biophys. 2011, 507:194-203.
11. Hagel J.M., Facchini P.J. Biochemistry and occurrence of O-demethylation in plant metabolism. Front. Physiol. 2010, 1:14.
12. Ikezawa N., Iwasa K., Sato F. Molecular cloning and characterization of methylenedioxy bridge-forming enzymes involved in stylopine biosynthesis in Eschscholzia californica. FEBS J. 2007, 274:1019-1035.
13. Ikezawa N., Iwasa K., Sato F. CYP719A subfamily of cytochrome P450 oxygenases and isoquinoline alkaloid biosynthesis in Eschscholzia californica. Plant Cell Rep. 2009, 28:123-133.
14. Díaz Chávez M.L., Rolf M., Gesell A., Kutchan T.M. Characterization of two methylenedioxy bridge-forming cytochrome P450-dependent enzymes of alkaloid formation in the Mexican prickly poppy Argemone mexicana. Arch. Biochem. Biophys. 2011, 507:186-193.
15. Liscombe D.K., Facchini P.J. Molecular cloning and characterization of tetrahydroprotoberberine cis-N-methyltransferase, an enzyme involved in alkaloid biosynthesis in opium poppy. J. Biol. Chem. 2007, 282:14741-14751.
16. Rueffer M., Zenk M.H. Enzymatic formation of protopines by a microsomal cytochrome P-450 system of Corydalis vaginans. Tetrahedron Lett. 1987, 28:5307-5310.
17. T. Takemura, N. Ikezawa, K. Iwasa, F. Sato, Molecular cloning and characterization of a cytochrome P450 in sanguinarine biosynthesis from Eschscholzia californica cells, Phytochemistry, (2012), http://dx.doi.org/10.1016/j.phytochem.2012.02.013.
18. J.M. Hagel, G.A.W. Beaudoin, E. Fossati, A. Ekins, V.J.J. Martin, P.J. Facchini, Characterization of a flavoprotein oxidase from opium poppy catalyzing the final steps in sanguinarine and papaverine biosynthesis, J. Biol. Chem. 287 (2012) 42972-42983.
19. Zulak K.G., Cornish A., Daskalchuk T.E., Deyholos M.K., Goodenowe D.B., Gordon P.M.K., Klassen D., Pelcher L.E., Sensen C.W., Facchini P.J. Gene transcript and metabolite profiling of elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta 2007, 225:1085-1106.
20. Desgagné-Penix I., Facchini P.J. Systematic silencing of benzylisoquinoline alkaloid biosynthetic genes reveals the major route to papaverine in opium poppy. Plant J. 2012, 72:331-344.
21. Hagel J.M., Facchini P.J. Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat. Chem. Biol. 2010, 6:273-275.
22. Dang T.-T.T., Facchini P.J. Characterization of three O-methyltransferases involved in noscapine biosynthesis in opium poppy. Plant Physiol. 2012, 159:618-631.
23. Meisel L., Fonseca B., González S., Baeza-Yates R., Cambiazo V., Campos R., Gonzalez M., Orellana A., Retamales J., Silva H. A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol. Res. 2005, 38:83-88.
24. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T., Higgins D., Thompson J.D. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
25. Rosco A., Pauli H.H., Priesner W., Kutchan T.M. Cloning and heterologous expression of NADPH-cytochrome P450 reductases from the Papaveraceae. Arch. Biochem. Biophys. 1997, 348:369-377.
26. Nguyen D.T., Göpfert J.C., Ikezawa N., Macnevin G., Kathiresan M., Conrad J., Spring O., Ro D.K. Biochemical conservation and evolution of germacrene a oxidase in asteraceae. J. Biol. Chem. 2010, 285:16588-16598.
27. Pompon D., Louerat B., Bronine A., Urban P. Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol. 1996, 272:51-64.
28. Farrow S.C., Hagel J.M., Facchini P.J. Transcript and metabolite profiling in cell cultures of 18 plant species that produce benzylisoquinoline alkaloids. Phytochemistry 2012, 77:79-88.
29. Zulak K.G., Khan M.F., Alcantara J., Schriemer D.C., Facchini P.J. Plant defense responses in opium poppy cell cultures revealed by liquid chromatography-tandem mass spectrometry proteomics. Mol. Cell. Proteomics 2009, 8:86-98.
30. Winzer T., Gazda V., He Z., Kaminski F., Kern M., Larson T.R., Li Y., Meade F., Teodor R., Vaistij F.E., Walker C., Bowser T.A., Graham I.A. A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 2012, 336:1704-1708.
31. Kruse T., Ho K., Yoo H.D., Johnson T., Hippely M., Park J.H., Flavell R.B., Bobzin S.C. In planta biocatalysis screen identifies 8-methoxypsoralen as new substrate for the CYP82C subfamily yielding novel chemical structures. Chem. Biol. 2008, 15:149-156.
32. Lee S., Badieyan S., Bevan D.R., Herde M., Gatz C., Tholl D. Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc. Natl. Acad. Sci. USA 2010, 107:21205-21210.
33. Siminszky B., Gavilano L., Bowen S.W., Dewey R.E. Conversion of nicotine to nornicotine in Nicotiana tabacum is mediated by CYP82E4, a cytochrome P450 monooxygenase. Proc. Natl. Acad. Sci. USA 2005, 102:14919-14924.
34. Ikezawa N., Tanaka M., Nagayoshi M., Shinkyo R., Sakaki T., Inouye K., Sato F. Molecular cloning and characterization of CYP719, a methylenedioxy bridge-forming enzyme that belongs to a novel P450 family, from cultured Coptis japonica cells. J. Biol. Chem. 2003, 278:38557-38565.
35. Desgagné-Penix I., Farrow S.C., Cram D., Nowak J., Facchini P.J. Integration of deep transcript and targeted metabolite profiles for eight cultivars of opium poppy. Plant Mol. Biol. 2012, 79:295-313.
36. Nakagawa A., Minami H., Kim J.-S., Koyanagi T., Katayama T., Sato F., Kumagai H. A bacterial platform for fermentative production of plant alkaloids. Nat. Commun. 2011, 2:326.