CYP82Y1 is n-methylcanadine 1-hydroxylase, a key noscapine biosynthetic enzyme in opium poppy

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2013-2026

  Dang, Thu Thuy T ^a   Facchini, Peter J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHETIC ENZYMES; NOSCAPINE; OPIUM POPPY;

BIOCHEMISTRY; BIOSYNTHESIS;

ENZYMES;

7 METHYLCANADINE; CANADINE; CYTOCHROME P450; CYTOCHROME P450 CYP82Y1; NARCOTOLINE; NOSCAPINE; PLANT MEDICINAL PRODUCT; RECOMBINANT ENZYME; SCOULERINE; SECOBERBINE; TETRAHYDROCOLUMBAMINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOACCUMULATION; BIOCHEMICAL COMPOSITION; BIOSYNTHESIS; CATALYSIS; CONTROLLED STUDY; CYP82Y1 GENE; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME REPRESSION; ENZYME SPECIFICITY; GENE SILENCING; HYDROXYLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPAVER SOMNIFERUM; PLANT GENE; PLANT STEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURE ANALYSIS;

BIOSYNTHESIS; CYTOCHROME P-450; ENZYME CATALYSIS; GENE SILENCING; METABOLISM; PLANT BIOCHEMISTRY; SECONDARY METABOLISM;

CYTOCHROME P-450 ENZYME SYSTEM; NOSCAPINE; PAPAVER; PLANT PROTEINS; RECOMBINANT PROTEINS;

EID: 84893122130     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505099     Document Type: Article

References (39)

1. Anderson, T. (1862) On the chemistry of opium. J. Chem. Soc. Perkin Trans. I 15, 446-455
2. Battersby, A. R., Hirst, M., McCaldin, D. J., Southgate, R., and Staunton, J. (1968) Alkaloid biosynthesis. XII. The biosynthesis of narcotine. J. Chem. Soc. Perkin Trans. I 17, 2163-2172
3. Kleinschmidt, G., and Mothes, K. (1959) Physiology and biosynthesis of alkaloids of Papaver sominferum. Z. Naturforsch. 14B, 52-56
4. Battersby, A. R., Staunton, J., Wiltshire, H. R., Bircher, B. J., and Fuganti, C. (1975) Studies of enzyme-mediated reactions. Part V. Synthesis of (13S)-and (13R)-[13-3H1]scoulerine from stereospecifically labelled (S)-[α-3Hl] benzyl alcohols. Stereochemistry of enzymic reactions at saturated benzylic carbon. J. Chem. Soc. Perkin Trans. 1, 1162-1171
5. Dang, T. T., and Facchini, P. J. (2012) Characterization of three O-methyltransferases involved in noscapine biosynthesis in opium poppy. Plant Physiol. 159, 618-631
6. Dang, T. T., and Facchini, P. J. (2014) Cloning and characterization of canadine synthase involved in noscapine biosynthesis in opium. FEBS Lett. 588, 198-204
7. Sariyar, G., and Shamma, M. (1986) Six alkaloids from Papaver species. Phytochemistry 25, 2403-2406
8. Liscombe, D. K., and Facchini, P. J. (2007) Molecular cloning and characterization of tetrahydroprotoberberine cis-N-methyltransferase, an enzyme involved in alkaloid biosynthesis in opium poppy. J. Biol. Chem. 282, 14741-14751
9. Facchini, P. J., Hagel, J. M., Liscombe, D. K., Loukanina, N., MacLeod, B. P., Samanani, N., and Zulak, K. G. (2007) Opium poppy. Blueprint for an alkaloid factory. Phytochem. Rev. 6, 97-124
10. 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., and Graham, I. A. (2012) Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336, 1704-1708
11. Chen, X., and Facchini, P. J. (2014) Short-chain dehydrogenase/reductase catalyzing the final step of noscapine biosynthesis is localized to laticifers in opium poppy. Plant J. 10.1111/tpj.12379
12. Hagel, J. M., and Facchini, P. J. (2013) Benzylisoquinoline alkaloid metabolism. A century of discovery and a brave new world. Plant Cell Physiol. 54, 647-672
13. Nguyen, D. T., Göpfert, J. C., Ikezawa, N., MacNevin, G., Kathiresan, M., Conrad, J., Spring, O., Ro, D. K. (2010) Biochemical conservation and evolution of germacrene A oxidase in Asteraceae. J. Biol. Chem. 285, 16588-16598
14. Kraus, P. F., and Kutchan, T. M. (1995) 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. U.S.A. 92, 2071-2075
15. Ikezawa, N., Iwasa, K., and Sato, F. (2008) Molecular cloning and characterization of CYP80G2, a cytochrome P450 that catalyzes an intramolecular C-C phenol coupling of (S)-reticuline in magnoflorine biosynthesis, from cultured Coptis japonica cells. J. Biol. Chem. 283, 8810-8821
16. Díaz Chávez, M. L., Rolf, M., Gesell, A., and Kutchan, T. M. (2011) Characterization of two methylenedioxy bridge-forming cytochrome P450-dependent enzymes of alkaloid formation in the Mexican prickly poppy Argemone mexicana. Arch. Biochem. Biophys. 507, 186-193
17. Ikezawa,N., Tanaka, M., Nagayoshi, M., Shinkyo, R., Sakaki, T., Inouye, K., and Sato, F. (2003) 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. 278, 38557-38565
18. Ikezawa, N., Iwasa, K., and Sato, F. (2007) Molecular cloning and characterization of methylenedioxy bridge-forming enzymes involved in stylopine biosynthesis in Eschscholzia californica. FEBS J. 274, 1019-1035
19. Gesell, A., Rolf, M., Ziegler, J., Díaz Chávez, M. L., Huang, F.-C., and Kutchan, T. M. (2009) CYP719B1 is salutaridine synthase, the C-C phenol-coupling enzyme of morphine biosynthesis in opium poppy. J. Biol. Chem. 284, 24432-24442
20. Beaudoin, G. A., and Facchini, P. J. (2013) Isolation and characterization of a cDNA encoding (S)-cis-N-methylstylopine 14-hydroxylase from opium poppy, a key enzyme in sanguinarine biosynthesis. Biochem. Biophys. Res. Commun. 431, 597-603
21. Takemura, T., Ikezawa, N., Iwasa, K., and Sato, F. (2013) Molecular cloning and characterization of a cytochrome P450 in sanguinarine biosynthesis from Eschscholzia californica cells. Phytochemistry 91, 100-108
22. Desgagné-Penix, I., Khan, M. F., Schriemer, D. C., Cram, D., Nowak, J., and Facchini, P. J. (2010) Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol. 10, 252
23. Hagel, J. M., and Facchini, P. J. (2010) Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat. Chem. Biol. 6, 273-275
24. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
25. Ro, D.-K., Ouellet, M., Paradise, E. M., Burd, H., Eng, D., Paddon, C. J., Newman, J. D., and Keasling, J. D. (2008) Induction of multiple pleiotropic drug resistance genes in yeast engineered to produce an increased level of anti-malarial drug precursor, artemisinic acid. BMC Biotechnol. 8, 83
26. Pauli, H. H., and Kutchan, T. M. (1998) Molecular cloning and functional heterologous expression of two alleles encoding (S)-N-methylcoclaurine 3'-hydroxylase (CYP80B1), a new methyl jasmonate-inducible cytochrome P450-dependent mono-oxygenase of benzylisoquinoline alkaloid biosynthesis. Plant J. 13, 793-801
27. Pompon, D., Louerat, B., Bronine, A., and Urban, P. (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol. 272, 51-64
28. Dinesh-Kumar, S. P., Anandalakshmi, R., Marathe, R., Schiff, M., and Liu, Y. (2003) Virus-induced gene silencing. Methods Mol. Biol. 236, 287-294
29. Hileman, L. C., Drea, S., Martino, G., Litt, A., and Irish, V. F. (2005) Virusinduced gene silencing is an effective tool for assaying gene function in the basal eudicot species Papaver somniferum (opium poppy). Plant J. 44, 334-341
30. Desgagné-Penix, I., Farrow, S. C., Cram, D., Nowak, J., and Facchini, P. J. (2012) Integration of deep transcript and targeted metabolite profiling of eight cultivars of opium poppy. Plant Mol. Biol. 79, 295-313
31. Binutu, O. A., and Cordell, G. A. (2000) Constituents of Zanthoxylum sprucei. Pharm. Biol. 38, 210-213
32. Lee, J. K., Cho, J. G., Song, M. C, Yoo, J. S, Lee, D. Y, Yang, H. J., Han, K. M, Kim, D. H, Oh, Y. J, Jeong, T. S, and Baek, N. I. (2009) Isolation of isoquinoline alkaloids from tuber of Corydalis turtschaninovii and their inhibition activity on low density lipoprotein oxidation. J. Korean Soc. Appl. Biol. Chem. 52, 646-654
33. Le, P. M, McCooeye, M., and Windust, A. (2013) Characterization of the alkaloids in goldenseal (Hydrastis canadensis) root by high resolution Orbitrap LC-MS(n). Anal. Bioanal. Chem. 405, 4487-4498
34. Lee, S., Badieyan, S., Bevan, D. R., Herde, M., Gatz, C., and Tholl, D. (2010) Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 107, 21205-21210
35. Kruse, T., Ho, K., Yoo, H.-D., Johnson, T., Hippely, M., Park, J.-H., Flavell, R., and Bobzin, S. (2008) In planta biocatalysis screen of P450s identifies 8-methoxypsoralen as a substrate for the CYP82C subfamily, yielding original chemical structures. Chem. Biol. 15, 149-156
36. Sariyar, G., and Phillipson, D. (1977) Macrantaline and macrantoridine, new alkaloids from a Turkish sample of Papaver pseudo-orientale. Phytochemistry 16, 2009-2013
37. Sariyar, G. (2002) Biodiversity in the alkaloids of Turkish Papaver species. Pure Appl. Chem. 74, 557-574
38. Williams, E. J., and Bowles, D. J. (2004) Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res. 14, 1060-1067
39. Michalak, P. (2008) Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics 91, 243-248