Cloning and characterization of a norbelladine 4′-o-methyltransferase involved in the biosynthesis of the Alzheimer's drug galanthamine in Narcissus sp. aff. pseudonarcissus

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Kilgore, Matthew B ^a   Augustin, Megan M ^a   Starks, Courtney M ^b   O'Neil Johnson, Mark ^b   May, Gregory D ^c   Crow, John A ^c   Kutchan, Toni M ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b Sequoia Sciences Inc   (United States)

^c NATIONAL CENTER FOR GENOME RESOURCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GALANTAMINE; METHYLTRANSFERASE; NORBELLADINE 4' O METHYLTRANSFERASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; ALKALOID; COMPLEMENTARY DNA; PROTEIN METHYLTRANSFERASE;

AFFINITY CHROMATOGRAPHY; ARTICLE; CONTROLLED STUDY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME PURIFICATION; GENE EXPRESSION; GENE IDENTIFICATION; MOLECULAR CLONING; NARCISSUS; NARCISSUS PSEUDONARCISSUS; NONHUMAN; NORBELLADINE 4' O METHYLTRANSFERASE GENE; NUCLEOTIDE SEQUENCE; PLANT BULB; PLANT LEAF; PLANT TISSUE; SEQUENCE ANALYSIS; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PATHOLOGY;

ALKALOIDS; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ESCHERICHIA COLI; GALANTAMINE; HUMANS; NARCISSUS; PROTEIN O-METHYLTRANSFERASE;

EID: 84905002845     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103223     Document Type: Article

References (70)

1. Gabrielsen B, Monath TP, Huggins JW, Kefauver DF, Pettit GR, et al. (1992) Antiviral (RNA) activity of selected Amaryllidaceae isoquinoline constituents and synthesis of related substances. J Nat Prod 55: 1569-1581.
2. Havelek R, Seifrtova M, Kralovec K, Bruckova L, Cahlikova L, et al. (2014) The effect of Amaryllidaceae alkaloids haemanthamine and haemanthidine on cell cycle progression and apoptosis in p53-negative human leukemic Jurkat cells. Phytomedicine 21: 479-490.
3. Liu J, Hu WX, He LF, Ye M, Li Y (2004) Effects of lycorine on HL-60 cells via arresting cell cycle and inducing apoptosis. FEBS Lett 578: 245-250. (Pubitemid 39601789)
4. Uyeo S, Kobayashi S (1953) Lycoris alkaloids. XXIV. Isolation and characterization of lycoremine. Pharm Bull 1: 139-142.
5. Barik J, Dajas-Bailador F, Wonnacott S (2005) Cellular responses to nicotinic receptor activation are decreased after prolonged exposure to galantamine in human neuroblastoma cells. Br J Pharmacol 145: 1084-1092. (Pubitemid 43079981)
6. Irwin RL, Smith HJ (1960) Cholinesterase inhibition by galanthamine and lycoramine. Biochem Pharmacol 3: 147-148.
7. Wilcock GK, Lilienfeld S, Gaens E (2000) Efficacy and safety of galantamine in patients with mild to moderate Alzheimer's disease: multicentre randomised controlled trial. Galantamine International-1 Study Group. BMJ 321: 1445-1449.
8. Wilcock G, Howe I, Coles H, Lilienfeld S, Truyen L, et al. (2003) A long-term comparison of galantamine and donepezil in the treatment of Alzheimer's disease. Drugs Aging 20: 777-789. (Pubitemid 36995254)
9. Mann JD (1963) Alkaloids and plant metabolism. VI. O-Methylation in vitro of norbelladine, a precursor of Amaryllidaceae alkaloids. J Biol Chem 238: 3820-3823.
10. Ejchhorn J, Takada T, Kita Y, Zenk MH (1998) Biosynthesis of the amaryllidaceae alkaloid galanthamine. Phytochemistry 49: 1037-1047. (Pubitemid 28457639)
11. Barton DHR, Kirby GW, Thomas GM (1963) Phenol oxidation and biosynthesis. Part VI. The biogenesis of Amaryllidaceae alkaloids. J Chem Soc: 4545-4558.
12. 1 unit of lycorine. J Am Chem Soc 84: 4348-4349.
13. Wildman WC, Battersby AR, Breuer SW (1962) Biosynthesis in the Amaryllidaceae. Incorporation of 3-C14-Tyrosine and phenylalanine in Nerine browdenii W. Wats. J Am Chem Soc 84: 4599-4600.
14. Suhadolnik RJ, Fischer AG, Zulalian J (1963) Biogenesis of the Amaryllidaceae alkaloids. II. Studies with whole plants, floral primordia and cell free extracts. Biochem Biophys Res Commun 11: 208-212.
15. Lehmann T, Pollmann S (2009) Gene expression and characterization of a stress-induced tyrosine decarboxylase from Arabidopsis thaliana. FEBS Lett 583: 1895-1900.
16. Battersby AR, Fales HM, Wildman WC (1961) Biosynthesis in the Amaryllidaceae. Tyrosine and norbelladine as precursors of haemanthamine. J Am Chem Soc 83: 4098-4099.
17. Battersby AR, Bink R, Breuer SW (1961) Biosynthesis in the Amaryllidaceae: incorporation of norbelladine into lycorine and norpluvine. Proc Chem Soc July: 243.
18. Barton DHR, Kirby GW, Taylor JB, Thomas GM (1961) The biosynthesis of Amaryllidaceae alkaloids. Proc Chem Soc July: 254-255.
19. Gerardy R, Zenk MH (1993) Purification and characterization of salutaridine: NADPH 7-oxidoreductase from Papaver somniferum. Phytochemistry 34: 125-132.
20. Roberts MF (1971) Polyphenolases in the 1000 g fraction of Papaver somniferum latex. Phytochemistry 10: 3021-3027.
21. Raman SB, Rathinasabapathi B (2003) beta-alanine N-methyltransferase of Limonium latifolium. cDNA cloning and functional expression of a novel N-methyltransferase implicated in the synthesis of the osmoprotectant beta-alanine betaine. Plant Physiol 132: 1642-1651. (Pubitemid 36872911)
22. Takeshita N, Fujiwara H, Mimura H, Fitchen JH, Yamada Y, et al. (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.
23. 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. (Pubitemid 38069768)
24. Nomura T, Kutchan TM (2010) Three new O-methyltransferases are sufficient for all O-methylation reactions of ipecac alkaloid biosynthesis in root culture of Psychotria ipecacuanha. J Biol Chem 285: 7722-7738.
25. 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. (Pubitemid 35365555)
26. Frick S, Kutchan TM (1999) Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis. Plant J 17: 329-339.
27. Widiez T, Hartman TG, Dudai N, Yan Q, Lawton M, et al. (2011) Functional characterization of two new members of the caffeoyl CoA O-methyltransferase-like gene family from Vanilla planifolia reveals a new class of plastid-localized O-methyltransferases. Plant Mol Biol 76: 475-488.
28. Johnson MT, Carpenter EJ, Tian Z, Bruskiewich R, Burris JN, et al. (2012) Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One 7: e50226.
29. FASTX-Toolkit website. Available: http://hannonlab.cshl.edu/fastx- toolkit. Accessed 2014 Jul 2.
30. Birol I, Jackman SD, Nielsen CB, Qian JQ, Varhol R, et al. (2009) De novo transcriptome assembly with ABySS. Bioinformatics 25: 2872-2877.
31. Luo R, Liu B, Xie Y, Li Z, Huang W, et al. (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1: 18.
32. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WE, et al. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 1147-1159. (Pubitemid 38811551)
33. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659. (Pubitemid 43985301)
34. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol: 138-148.
35. Lottaz C, Iseli C, Jongeneel CV, Bucher P (2003) Modeling sequencing errors by combining Hidden Markov models. Bioinformatics 19 Suppl 2: ii103-112. (Pubitemid 41296646)
36. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
37. Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, et al. (2007) The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol 72: 353-363.
38. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
40. Higashi Y, Smith TJ, Jez JM, Kutchan TM (2010) Crystallization and preliminary X-ray diffraction analysis of salutaridine reductase from the opium poppy Papaver somniferum. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 163-166.
41. Choi-Rhee E, Cronan JE (2005) A nucleosidase required for in vivo function of the S-adenosyl-L-methionine radical enzyme, biotin synthase. Chem Biol 12: 589-593. (Pubitemid 40727933)
42. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
43. Kalra S, Puniya BL, Kulshreshtha D, Kumar S, Kaur J, et al. (2013) De novo transcriptome sequencing reveals important molecular networks and metabolic pathways of the plant, Chlorophytum borivilianum. PLoS One 8: e83336.
44. Kwantes M, Liebsch D, Verelst W (2012) How MIKC*MADS-box genes originated and evidence for their conserved function throughout the evolution of vascular plant gametophytes. Mol Biol Evol 29: 293-302.
45. Zonneveld B (2010) The involvement of Narcissus hispanicus Gouan in the origin of Narcissus bujei and of cultivated trumpet daffodils (Amaryllidaceae). Anales del Jardín Botánico de Madrid 67: 29-39.
46. Schröder G, Wehinger E, Lukacin R, Wellmann F, Seefelder W, et al. (2004) Flavonoid methylation: a novel 49-O-methyltransferase from Catharanthus roseus, and evidence that partially methylated flavanones are substrates of four different flavonoid dioxygenases. Phytochemistry 65: 1085-1094. (Pubitemid 38542744)
47. Akashi T, Sawada Y, Shimada N, Sakurai N, Aoki T, et al. (2003) cDNA cloning and biochemical characterization of S-adenosyl-L-methionine: 2,7,49-trihydroxyisoflavanone 4 9-O-methyltransferase, a critical enzyme of the legume isoflavonoid phytoalexin pathway. Plant Cell Physiol 44: 103-112. (Pubitemid 36280704)
48. Kim DH, Kim BG, Lee Y, Ryu JY, Lim Y, et al. (2005) Regiospecific methylation of naringenin to ponciretin by soybean O-methyltransferase expressed in Escherichia coli. J Biotechnol 119: 155-162. (Pubitemid 41219544)
49. Gang DR, Lavid N, Zubieta C, Chen F, Beuerle T, et al. (2002) Characterization of phenylpropene O-methyltransferases from sweet basil: facile change of substrate specificity and convergent evolution within a plant O-methyltransferase family. Plant Cell 14: 505-519. (Pubitemid 34271302)
50. Joshi CP, Chiang VL (1998) Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol Biol 37: 663-674. (Pubitemid 28329241)
51. Wils CR, Brandt W, Manke K, Vogt T (2013) A single amino acid determines position specificity of an Arabidopsis thaliana CCoAOMT-like O-methyltransferase. FEBS Lett 587: 683-689.
52. Ibdah M, Zhang XH, Schmidt J, Vogt T (2003) A novel Mg(2+)-dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. J Biol Chem 278: 43961-43972. (Pubitemid 37377135)
53. Kopycki JG, Stubbs MT, Brandt W, Hagemann M, Porzel A, et al. (2008) Functional and structural characterization of a cation-dependent O-methyltransferase from the cyanobacterium Synechocystis sp. strain PCC 6803. J Biol Chem 283: 20888-20896.
54. Moreau Y, Tranchevent LC (2012) Computational tools for prioritizing candidate genes: boosting disease gene discovery. Nat Rev Genet 13: 523-536.
55. Saito K, Hirai MY, Yonekura-Sakakibara K (2008) Decoding genes with coexpression networks and metabolomics - 'majority report by precogs'. Trends Plant Sci 13: 36-43.
56. Wei H, Persson S, Mehta T, Srinivasasainagendra V, Chen L, et al. (2006) Transcriptional coordination of the metabolic network in Arabidopsis. Plant Physiol 142: 762-774. (Pubitemid 44583145)
57. Sun Y, Luo H, Li Y, Sun C, Song J, et al. (2011) Pyrosequencing of the Camptotheca acuminata transcriptome reveals putative genes involved in camptothecin biosynthesis and transport. BMC Genomics 12: 533.
58. Aharoni A, Keizer LC, Bouwmeester HJ, Sun Z, Alvarez-Huerta M, et al. (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12: 647-662.
59. Guterman I, Shalit M, Menda N, Piestun D, Dafny-Yelin M, et al. (2002) Rose scent: genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14: 2325-2338. (Pubitemid 35224835)
60. Mercke P, Kappers IF, Verstappen FW, Vorst O, Dicke M, et al. (2004) Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiol 135: 2012-2024. (Pubitemid 39182781)
61. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
62. Yamazaki M, Mochida K, Asano T, Nakabayashi R, Chiba M, et al. (2013) Coupling deep transcriptome analysis with untargeted metabolic profiling in Ophiorrhiza pumila to further the understanding of the biosynthesis of the anticancer alkaloid camptothecin and anthraquinones. Plant Cell Physiol 54: 686-696.
63. Day A, Neutelings G, Nolin F, Grec S, Habrant A, et al. (2009) Caffeoyl coenzyme A O-methyltransferase down-regulation is associated with modifications in lignin and cell-wall architecture in flax secondary xylem. Plant Physiol Biochem 47: 9-19.
64. Eswaran N, Parameswaran S, Sathram B, Anantharaman B, Kumar G RK, et al. (2010) Yeast functional screen to identify genetic determinants capable of conferring abiotic stress tolerance in Jatropha curcas. BMC Biotechnol 10: 23.
65. Ibrahim RK, Bruneau A, Bantignies B (1998) Plant O-methyltransferases: molecular analysis, common signature and classification. Plant Mol Biol 36: 1-10. (Pubitemid 28126467)
66. Hugueney P, Provenzano S, Verries̀ C, Ferrandino A, Meudec E, et al. (2009) A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine. Plant Physiol 150: 2057-2070.
67. Nestor A, Craig BS, Jack O, Ke Z (2008) Modulating lignin in plants. Google Patents.
68. 2+-dependent O-methyltransferases. J Mol Biol 378: 154-164.
69. 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. (Pubitemid 34952124)
70. Kato M, Mizuno K, Crozier A, Fujimura T, Ashihara H (2000) Caffeine synthase gene from tea leaves. Nature 406: 956-957.