Microbial Factories for the Production of Benzylisoquinoline Alkaloids

Trends in Biotechnology - Tập 34 - Trang 228-241 - 2016
Lauren Narcross1,2, Elena Fossati1,2, Leanne Bourgeois1,2, John E. Dueber3, Vincent J.J. Martin1,2
1Department of Biology, Concordia University, Montréal, Québec H4B 1R6, Canada
2Centre for Structural and Functional Genomics, Concordia University, Montréal, Québec H4B 1R6, Canada
3Department of Bioengineering, University of California, Berkeley, Berkeley, CA 94704, USA

Tài liệu tham khảo

Li, 2009, Drug discovery and natural products: end of an era or an endless frontier?, Science, 325, 161, 10.1126/science.1168243 Harvey, 2007, Natural products as a screening resource, Curr. Opin. Chem. Biol., 11, 480, 10.1016/j.cbpa.2007.08.012 David, 2014, The pharmaceutical industry and natural products: historical status and new trends, Phytochem. Rev., 14, 299, 10.1007/s11101-014-9367-z Harvey, 2008, Natural products in drug discovery, Drug Discov. Today, 13, 894, 10.1016/j.drudis.2008.07.004 Lahlou, 2013, The success of natural products in drug discovery, Pharmacol. Pharm., 4, 17, 10.4236/pp.2013.43A003 Cordell, 2011, Sustainable medicines and global health care, Planta Med., 77, 1129, 10.1055/s-0030-1270731 Rathbone, 2002, Microbial transformation of alkaloids, Curr. Opin. Microbiol., 5, 274, 10.1016/S1369-5274(02)00317-X Paddon, 2014, Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development, Nat. Rev. Microbiol., 12, 355, 10.1038/nrmicro3240 Pickens, 2014, Metabolic engineering for the production of natural products, Annu. Rev. Chem. Biomol. Eng., 2, 211, 10.1146/annurev-chembioeng-061010-114209 Hagel, 2013, Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world, Plant Cell Physiol., 54, 647, 10.1093/pcp/pct020 Cordell, 2001, The potential of alkaloids in drug discovery, Phyther. Res., 15, 183, 10.1002/ptr.890 Stadler, 1989, (S)-norcoclaurine is the central intermediate in benzylisoquinoline alkaloid biosynthesis, Phytochemistry, 28, 1083, 10.1016/0031-9422(89)80187-6 Winzer, 2012, A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine, Science, 336, 1704, 10.1126/science.1220757 Farrow, 2013, Dioxygenases catalyze O-demethylation and O O-demethylenation with widespread roles in benzylisoquinoline alkaloid metabolism in opium poppy, J. Biol. Chem., 288, 28997, 10.1074/jbc.M113.488585 Takemura, 2013, Molecular cloning and characterization of a cytochrome P450 in sanguinarine biosynthesis from Eschscholzia californica cells, Phytochemistry, 91, 100, 10.1016/j.phytochem.2012.02.013 Ruff, 2012, Biocatalytic production of tetrahydroisoquinolines, Tetrahedron Lett., 53, 1071, 10.1016/j.tetlet.2011.12.089 Liscombe, 2007, Molecular cloning and characterization of tetrahydroprotoberberine cis-N-methyltransferase, an enzyme involved in alkaloid biosynthesis in opium poppy, J. Biol. Chem., 282, 14741, 10.1074/jbc.M611908200 Farrow, 2015, Stereochemical inversion of (S)-reticuline by a cytochrome P450 fusion in opium poppy, Nat. Chem. Biol., 9, 728, 10.1038/nchembio.1879 Pittard, 2008, Biosynthesis of the aromatic amino acids, EcoSal Plus, 3, 10.1128/ecosalplus.3.6.1.8 Juminaga, 2012, Modular engineering of L-tyrosine production in Escherichia coli, Appl. Environ. Microbiol., 78, 89, 10.1128/AEM.06017-11 Gold, 2015, Metabolic engineering of a tyrosine-overproducing yeast platform using targeted metabolomics, Microb. Cell Fact., 14, 1, 10.1186/s12934-015-0252-2 McKenna, 2014, Rational and combinatorial approaches to engineering styrene production by Saccharomyces cerevisiae, Microb. Cell Fact., 13, 1, 10.1186/s12934-014-0123-2 Patnaik, 2008, Tyrosine production by recombinant Escherichia coli: fermentation optimization and recovery, Biotechnol. Bioeng., 99, 741, 10.1002/bit.21765 Rodriguez, 2015, Establishment of a yeast platform strain for production of p-coumaric acid through metabolic engineering of aromatic amino acid biosynthesis, Metab. Eng., 31, 181, 10.1016/j.ymben.2015.08.003 Westfall, 2012, Production of amorphadiene in yeast, and its conversion to dihydroartemisinic acid, precursor to the antimalarial agent artemisinin, Proc. Natl. Acad. Sci. U.S.A., 109, E111, 10.1073/pnas.1110740109 Kunjapur, 2014, Synthesis and accumulation of aromatic aldehydes in an engineered strain of Escherichia coli, J. Am. Chem. Soc., 136, 11644, 10.1021/ja506664a Hazelwood, 2008, The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism, Appl. Environ. Microbiol., 74, 2259, 10.1128/AEM.02625-07 Kunjapur, 2015, Microbial engineering for aldehyde synthesis, Appl. Environ. Microbiol., 81, 1892, 10.1128/AEM.03319-14 Rodriguez, 2014, Toward aldehyde and alkane production by removing aldehyde reductase activity in Escherichia coli, Metab. Eng., 25, 227, 10.1016/j.ymben.2014.07.012 Hawkins, 2009 Nakagawa, 2011, A bacterial platform for fermentative production of plant alkaloids, Nat. Commun., 2, 1, 10.1038/ncomms1327 Cushing, 1948, The oxidation of catechol-type substrates by tyrosinase, J. Am. Chem. Soc., 70, 1184, 10.1021/ja01183a090 Prieto, 1993, Characterization of an Escherichia coli aromatic hydroxylase with a broad substrate range, J. Bacteriol., 175, 2162, 10.1128/jb.175.7.2162-2167.1993 Claus, 2006, Bacterial tyrosinases, Syst. Appl. Microbiol., 29, 3, 10.1016/j.syapm.2005.07.012 Hatlestad, 2012, The beet R locus encodes a new cytochrome P450 required for red betalain production, Nat. Genet., 44, 816, 10.1038/ng.2297 Daubner, 2011, Tyrosine hydroxylase and regulation of dopamine synthesis, Arch. Biochem. Biophys., 508, 1, 10.1016/j.abb.2010.12.017 Nakagawa, 2014, (R,S)-tetrahydropapaveroline production by stepwise fermentation using engineered Escherichia coli, Sci. Rep., 4, 6695, 10.1038/srep06695 DeLoache, 2015, An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose, Nat. Chem. Biol., 11, 465, 10.1038/nchembio.1816 Ehrenworth, 2015, Pterin-dependent mono-oxidation for the microbial synthesis of a modified monoterpene indole alkaloid, ACS Synth. Biol., 10.1021/acssynbio.5b00025 Trenchard, 2015, De novo production of the key branch point benzylisoquinoline alkaloid reticuline in yeast, Metab. Eng., 31, 74, 10.1016/j.ymben.2015.06.010 Koopman, 2012, De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae, Microb. Cell Fact., 11, 1, 10.1186/1475-2859-11-155 Horwitz, 2015, Efficient multiplexed integration of synergistic alleles and metabolic pathways in yeasts via CRISPR-Cas, Cell Syst., 1, 88, 10.1016/j.cels.2015.02.001 Stöckigt, 2011, The Pictet–Spengler reaction in nature and in organic chemistry, Angew. Chem. Int. Ed., 50, 8538, 10.1002/anie.201008071 Minami, 2007, Functional analysis of norcoclaurine synthase in Coptis japonica, J. Biol. Chem., 282, 6274, 10.1074/jbc.M608933200 Minami, 2008, Microbial production of plant benzylisoquinoline alkaloids, Proc. Natl. Acad. Sci. U.S.A., 105, 7393, 10.1073/pnas.0802981105 Kim, 2013, Improvement of reticuline productivity from dopamine by using engineered Escherichia coli, Biosci. Biotechnol. Biochem., 77, 2166, 10.1271/bbb.130552 Lichman, 2015, ‘Dopamine-first’ mechanism enables the rational engineering of the norcoclaurine synthase aldehyde activity profile, FEBS J., 282, 1137, 10.1111/febs.13208 Trenchard, 2015, Engineering strategies for the fermentative production of plant alkaloids in yeast, Metab. Eng., 30, 96, 10.1016/j.ymben.2015.05.001 Ziegler, 2006, Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis, Plant J., 48, 177, 10.1111/j.1365-313X.2006.02860.x Rinner, 2012, Synthesis of morphine alkaloids and derivatives, Top. Curr. Chem., 309, 33, 10.1007/128_2011_133 Winzer, 2015, Morphinan biosynthesis in opium poppy requires a P450-oxidoreductase fusion protein, Science, 349, 309, 10.1126/science.aab1852 Galanie, 2015, Complete biosynthesis of opioids in yeast, Science, 349, 1095, 10.1126/science.aac9373 Thodey, 2014, A microbial biomanufacturing platform for natural and semisynthetic opioids, Nat. Chem. Biol., 10, 1, 10.1038/nchembio.1613 Unterlinner, 1999, Molecular cloning and functional expression of codeinone reductase: the penultimate enzyme in morphine biosynthesis in the opium poppy Papaver somniferum, Plant J., 18, 465, 10.1046/j.1365-313X.1999.00470.x Hagel, 2010, Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy, J. Biol. Chem., 6, 273 Fossati, 2015, Synthesis of morphinan alkaloids in Saccharomyces cerevisiae, PLoS ONE, 10, e0124459, 10.1371/journal.pone.0124459 Theuns, 1984, Neodihydrothebaine and bractazonine, two dibenz[d,f]azonine alkaloids of Papaver bracteatum, Phytochemistry, 23, 1157, 10.1016/S0031-9422(00)82630-8 Hawkins, 2008, Production of benzylisoquinoline alkaloids in Saccharomyces cerevisiae, Nat. Chem. Biol., 4, 564, 10.1038/nchembio.105 Beaudoin, 2014, Benzylisoquinoline alkaloid biosynthesis in opium poppy, Planta, 240, 19, 10.1007/s00425-014-2056-8 Beaudoin, 2015 Fossati, 2014, Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae, Nat. Commun., 5, 1, 10.1038/ncomms4283 Dang, 2015, Acetylation serves as a protective group in noscapine biosynthesis in opium poppy, Nat. Chem. Biol., 11, 104, 10.1038/nchembio.1717 Jakočiūnas, 2015, Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae, Metab. Eng., 28, 213, 10.1016/j.ymben.2015.01.008 Dang, 2012, Biochemical genomics for gene discovery in benzylisoquinoline alkaloid biosynthesis in opium poppy and related species, Methods Enzymol., 515, 231, 10.1016/B978-0-12-394290-6.00011-2 Desgagné-Penix, 2012, Systematic silencing of benzylisoquinoline alkaloid biosynthetic genes reveals the major route to papaverine in opium poppy, Plant J., 72, 331, 10.1111/j.1365-313X.2012.05084.x Matasci, 2014, Data access for the 1,000 Plants (1KP) project, Gigascience, 3, 1, 10.1186/2047-217X-3-17 Facchini, 2012, Synthetic biosystems for the production of high-value plant metabolites, Trends Biotechnol., 30, 127, 10.1016/j.tibtech.2011.10.001 Singla, 2010, BIAdb: a curated database of benzylisoquinoline alkaloids, BMC Pharmacol., 10, 1, 10.1186/1471-2210-10-4 Peking Union Medical College Hospital (2011) Pharmacokinetics and Pharmacodynamics of Higenamine in Chinese Healthy Subjects (ClinicalTrials.gov Identifier NCT01451229), ClinicalTrials.gov Bloomer, 2015, Clinical safety assessment of oral higenamine supplementation in healthy, young men, Hum. Exp. Toxicol., 34, 1, 10.1177/0960327114565490 Law, 2013, DrugBank 4.0: Shedding new light on drug metabolism, Nucleic Acids Res., 42, D1091, 10.1093/nar/gkt1068 Amirkia, 2014, Alkaloids as drug leads – a predictive structural and biodiversity-based analysis, Phytochem. Lett., 10, xlviii, 10.1016/j.phytol.2014.06.015 Bowman, 2006, Neuromuscular block, Br. J. Pharmacol., 147, S277, 10.1038/sj.bjp.0706404 Frampton, 1993, Mivacurium. A review of its pharmacology and therapeutic potential in general anaesthesia, Drugs, 45, 1066, 10.2165/00003495-199345060-00009 2011, A Study of Noscapine HCl (CB3304) in Patients with Relapsed or Refractory Multiple Myeloma Kang, 2015, Glaucine inhibits breast cancer cell migration and invasion by inhibiting MMP-9 gene expression through the suppression of NF-κB activation, Mol. Cell. Biochem., 403, 85, 10.1007/s11010-015-2339-9 Shanghai Jiao Tong University School of Medicine (2007) Efficacy and Safety of Berberine in the Treatment of Diabetes with Dyslipidemia (ClinicalTrials.gov Identifier NCT00462046), ClinicalTrials.gov Peng, 2015, Antibacterial activity and mechanism of berberine against Streptococcus agalactiae, Int. J. Clin. Exp. Pathol., 8, 5217 Zha, 2010, Berberine inhibits HIV protease inhibitor-induced inflammatory response by modulating ER stress signaling pathways in murine macrophages, PLoS ONE, 5, 2, 10.1371/journal.pone.0009069 Meade, 2015, (−)-Stepholidine is a potent pan-dopamine receptor antagonist of both G protein- and β-arrestin-mediated signaling, Psychopharmacology (Berl.), 232, 917, 10.1007/s00213-014-3726-8 Food, 2003, Oral health care drug products for over-the-counter human use; antigingivitis/antiplaque drug products; establishment of a monograph, Fed. Regist., 68, 1 Nam, 2012, Network context and selection in the evolution to enzyme specificity, Science, 337, 1101, 10.1126/science.1216861 Fischbach, 2007, One pathway, many products, Nat. Chem. Biol., 3, 353, 10.1038/nchembio0707-353 Shin, 2013, Production of bulk chemicals via novel metabolic pathways in microorganisms, Biotechnol. Adv., 31, 925, 10.1016/j.biotechadv.2012.12.008 Aharoni, 2005, The ‘evolvability’ of promiscuous protein functions, Nat. Genet., 37, 73, 10.1038/ng1482 Yoshikuni, 2006, Designed divergent evolution of enzyme function, Nature, 440, 1078, 10.1038/nature04607 Jones, 2015, Metabolic pathway balancing and its role in the production of biofuels and chemicals, Curr. Opin. Biotechnol., 33, 52, 10.1016/j.copbio.2014.11.013 Furubayashi, 2015, A highly selective biosynthetic pathway to non-natural C50 carotenoids assembled from moderately selective enzymes, Nat. Commun., 6, 1, 10.1038/ncomms8534 Martin, V. et al. Valorbec, Société en Commandite. Method of making a benzylisoquinoline alkaloid (BIA) metabolite, enzymes therefore, WO/2015/103711 Smolke, C.D. et al. The Board of Trustees of the Leland Stanford Junior University. Benzylisoquinoline alkaloids (bia) producing microbes, and methods of making and using the same, US20140273109 A1 Tang, 2009, Microbial conversion of glycerol to 1,3-propanediol by an engineered strain of Escherichia coli, Appl. Environ. Microbiol., 75, 1628, 10.1128/AEM.02376-08