Isolation and characterization of O-methyltransferases involved in the biosynthesis of glaucine in Glaucium flavum

Plant Physiology

Volumn 169, Issue 2, 2015, Pages 1127-1140

  Chang, Limei ^a   Hagel, Jillian M ^a   Facchini, Peter J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APORPHINE DERIVATIVE; BENZYLISOQUINOLINE DERIVATIVE; BERBERINE DERIVATIVE; DISCRETAMINE; GLAUCINE; ISOQUINOLINE DERIVATIVE; LAUDANOSINE; METHYLTRANSFERASE; PLANT PROTEIN; RECOMBINANT PROTEIN; RETICULINE; TETRAHYDROPAPAVEROLINE;

ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; MEDICINAL PLANT; METABOLISM; PAPAVERACEAE; PHYLOGENY; PLANT ROOT;

APORPHINES; BENZYLISOQUINOLINES; BERBERINE ALKALOIDS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, PLANT; ISOQUINOLINES; METHYLTRANSFERASES; PAPAVERACEAE; PHYLOGENY; PLANT PROTEINS; PLANT ROOTS; PLANTS, MEDICINAL; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TETRAHYDROPAPAVEROLINE;

EID: 84942894278     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01240     Document Type: Article

References (45)

1. Battersby AR, McHugh JL, Staunton J, Todd M (1971) Biosynthesis of the apparently “directly coupled” aporphine alkaloids. J Chem Soc Chem Commun 1971: 985–986
2. Bhakuni DS, Jain S (1988) The biosynthesis of glaucine in Litsea glutinosa. J Chem Soc Perkin Trans 1: 1447–1449
3. Bournine L, Bensalem S, Wauters JN, Iguer-Ouada M, Maiza-Benabdesselam F, Bedjou F, Castronovo V, Bellahcène A, Tits M, Frédérich M (2013) Identification and quantification of the main active anticancer alkaloids from the root of Glaucium flavum. Int J Mol Sci 14: 23533–23544
4. Choi KB, Morishige T, Shitan N, Yazaki K, Sato F (2002) Molecular cloning and characterization of coclaurine N-methyltransferase from cultured cells of Coptis japonica. J Biol Chem 277: 830–835
5. Cortijo J, Villagrasa V, Pons R, Berto L, Martí-Cabrera M, Martinez-Losa M, Domenech T, Beleta J, Morcillo EJ (1999) Bronchodilator and antiinflammatory activities of glaucine: In vitro studies in human airway smooth muscle and polymorphonuclear leukocytes. Br J Pharmacol 127: 1641–1651
6. Dang TTT, Chen X, Facchini PJ (2015) Acetylation serves as a protective group in noscapine biosynthesis in opium poppy. Nat Chem Biol 11: 104–106
7. Dang TTT, Facchini PJ (2012) Characterization of three O-methyltransferases involved in noscapine biosynthesis in opium poppy. Plant Physiol 159: 618–631
8. Dargan PI, Button J, Hawkins L, Archer JR, Ovaska H, Lidder S, Ramsey J, Holt DW, Wood DM (2008) Detection of the pharmaceutical agent glaucine as a recreational drug. Eur J Clin Pharmacol 64: 553–554
9. Daskalova E, Iskrenova E, Kiryakov HG, Evstatieva L (1988) Minor alkaloids of Glaucium flavum. Phytochemistry 27: 953–955
10. Desgagné-Penix I, Farrow SC, Cram D, Nowak J, Facchini PJ (2012) Integration of deep transcript and targeted metabolite profiles for eight cultivars of opium poppy. Plant Mol Biol 79: 295–313
11. Farrow SC, Hagel JM, Facchini PJ (2012) Transcript and metabolite profiling in cell cultures of 18 plant species that produce benzylisoquinoline alkaloids. Phytochemistry 77: 79–88
12. Fossati E, Ekins A, Narcross L, Zhu Y, Falgueyret JP, Beaudoin GA, Facchini PJ, Martin VJJ (2014) Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat Commun 5: 3283
13. Frenzel T, Zenk MH (1990) S-adenosyl-L-methionine:39hydroxyl-Nmethyl-(S)-coclaurine-49-O-methyltransferase, a regio- and stereoselective enzyme of the (S)-reticuline pathway. Phytochemistry 29: 3505–3511
14. Gambino G, Perrone I, Gribaudo I (2008) A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19: 520–525
15. Hagel JM, Facchini PJ (2010) Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat Chem Biol 6: 273–275
16. Hagel JM, Facchini PJ (2013) Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol 54: 647–672
17. Hawkins KM, Smolke CD (2008) Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae. Nat Chem Biol 4: 564–573
18. Ikezawa N, Iwasa K, 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
19. Inui T, Tamura K, Fujii N, Morishige T, Sato F (2007) Overexpression of Coptis japonica norcoclaurine 6-O-methyltransferase overcomes the ratelimiting step in benzylisoquinoline alkaloid biosynthesis in cultured Eschscholzia californica. Plant Cell Physiol 48: 252–262
20. Kintsurashvili LG, Vachnadze VY (2000) Alkaloids of Glaucium corniculatum and G. flavum growing in Georgia. Chem Nat Compd 36: 225–226
21. Lapa GB, Sheichenko OP, Serezhechkin AG, Tolkachev ON (2004) HPLC determination of glaucine in yellow horn poppy grass (Glaucium flavum Crantz). Pharm Chem J 38: 441–442
22. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948
23. Liscombe DK, Facchini PJ (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
24. Liscombe DK, MacLeod BP, Loukanina N, Nandi OI, Facchini PJ (2005) Evidence for the monophyletic evolution of benzylisoquinoline alkaloid biosynthesis in angiosperms. Phytochemistry 66: 2501–2520
25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25: 402–408
26. Milanowski DJ, Winter RE, Elvin-Lewis MP, Lewis WH (2002) Geographic distribution of three alkaloid chemotypes of Croton lechleri. J Nat Prod 65: 814–819
27. Morishige T, Dubouzet E, Choi KB, Yazaki K, Sato F (2002) Molecular cloning of columbamine O-methyltransferase from cultured Coptis japonica cells. Eur J Biochem 269: 5659–5667
28. Morishige T, Tsujita T, Yamada Y, Sato F (2000) Molecular characterization of the S-adenosyl-L-methionine:39-hydroxy-N-methylcoclaurine 49-O-methyltransferase involved in isoquinoline alkaloid biosynthesis in Coptis japonica. J Biol Chem 275: 23398–23405
29. Morteza-Semnani K, Amin G, Shidfar MR, Hadizadeh H, Shafiee A (2003) Antifungal activity of the methanolic extract and alkaloids of Glaucium oxylobum. Fitoterapia 74: 493–496
30. Muemmler S, Rueffer M, Nagakura N, Zenk MH (1985) S-adenosyl-Lmethionine: (S)-scoulerine 9-O-methyltransferase, a highly stereo- and regio-specific enzyme in tetrahydroprotoberberine biosynthesis. Plant Cell Rep 4: 36–39
31. Nakagawa A, Minami H, Kim JS, Koyanagi T, Katayama T, Sato F, Kumagai H (2011) A bacterial platform for fermentative production of plant alkaloids. Nat Commun 2: 326
32. Orallo F, Fernández Alzueta A, Campos-Toimil M, Calleja JM (1995) Study of the in vivo and in vitro cardiovascular effects of (+)-glaucine and N-carbethoxysecoglaucine in rats. Br J Pharmacol 114: 1419–1427
33. Ounaroon A, Decker G, Schmidt J, Lottspeich F, Kutchan TM (2003) (R,S)-Reticuline 7-O-methyltransferase and (R,S)-norcoclaurine 6-O-methyltransferase of Papaver somniferum - cDNA cloning and characterization of methyl transfer enzymes of alkaloid biosynthesis in opium poppy. Plant J 36: 808–819
34. Peled B, Waisel Y, Carmeli S (1988) Alkaloid content in various chemoecotypes of Glaucium flavum from Israel. Phytochemistry 27: 1021–1024
35. Petitto V, Serafini M, Gallo FR, Multari G, Nicoletti M (2010) Alkaloids from Glaucium flavum from Sardinia. Nat Prod Res 24: 1033–1035
36. Pienkny S, Brandt W, Schmidt J, Kramell R, Ziegler J (2009) Functional characterization of a novel benzylisoquinoline O-methyltransferase suggests its involvement in papaverine biosynthesis in opium poppy (Papaver somniferum L). Plant J 60: 56–67
37. Rueffer M, Nagakura N, Zenk MH (1983) A highly specific O-methyltransferase for nororientaline synthesis isolated from Argemone platyceras cell cultures. Planta Med 49: 196–198
38. Sato F, Takeshita N, Fitchen JH, Fujiwara H, Yamada Y (1993) S-adenosyl-L-methionine:scoulerine-9-O-methyltransferase from cultured Coptis japonica cells. Phytochemistry 32: 659–664
39. Takeshita N, Fujiwara H, Mimura H, Fitchen JH, Yamada Y, Sato F (1995) Molecular cloning and characterization of S-adenosyl-L-methionine: scoulerine-9-O-methyltransferase from cultured cells of Coptis japonica. Plant Cell Physiol 36: 29–36
40. Tautenhahn R, Böttcher C, Neumann S (2008) Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics 9: 504
41. Winzer T, Gazda V, He Z, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE, et al (2012) A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336: 1704–1708
42. Xiao M, Zhang Y, Chen X, Lee EJ, Barber CJ, Chakrabarty R, Desgagné-Penix I, Haslam TM, Kim YB, Liu E, et al (2013) Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. J Biotechnol 166: 122–134
43. Xu XH, Yu GD, Wang ZT (2004) Resource investigation and quality evaluation on wild Corydalis yanhusuo. Zhongguo Zhong Yao Za Zhi 29: 399–401
44. Zetler G (1988) Neuroleptic-like, anticonvulsant and antinociceptive effects of aporphine alkaloids: bulbocapnine, corytuberine, boldine and glaucine. Arch Int Pharmacodyn Ther 296: 255–281
45. Ziegler J, Diaz-Chávez ML, Kramell R, Ammer C, Kutchan TM (2005) Comparative macroarray analysis of morphine containing Papaver somniferum and eight morphine free Papaver species identifies an Omethyltransferase involved in benzylisoquinoline biosynthesis. Planta 222: 458–471