Transcriptome-enabled discovery and functional characterization of enzymes related to (2S)-pinocembrin biosynthesis from Ornithogalum caudatum and their application for metabolic engineering

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• 作者：Lei Guo ; Xi Chen ; Li-Na Li ; Wei Tang ; Yi-Ting Pan…
• 关键词：(2S) ; Pinocembrin ; Ornithogalum caudatum ; Metabolic engineering ; 4 ; Coumarate ; coenzyme A ligase ; Chalcone synthase ; Chalcone isomerase
• 刊名：Microbial Cell Factories
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：15
• 期：1
• 全文大小：1,425 KB
• 参考文献：1.Lotti C, CampoFernandez M, Piccinelli AL, Cuesta-Rubio O, MarquezHernandez I, Rastrelli L. Chemical constituents of red Mexican propolis. J Agric Food Chem. 2010;58:2209–13.CrossRef
  2.Shrestha SP, Amano Y, Narukawa Y, Takeda T. Nitric oxide production inhibitory activity of flavonoids contained in trunk exudates of Dalbergia sissoo. J Nat Prod. 2008;71:98–101.CrossRef
  3.Villanueva VR, Barbier M, Gonnet M, Lavie P. [The flavonoids of propolis. Isolation of a new bacteriostatic substance: pinocembrin (dihydroxy-5, 7 flavanone)]. Ann Inst Pasteur (Paris). 1970;118:84–7.
  4.Athikomkulchai S, Awale S, Ruangrungsi N, Ruchirawat S, Kadota S. Chemical constituents of Thai propolis. Fitoterapia. 2013;88:96–100.CrossRef
  5.Melliou E, Chinou I. Chemical analysis and antimicrobial activity of Greek propolis. Planta Med. 2004;70:515–9.CrossRef
  6.Feng R, Guo ZK, Yan CM, Li EG, Tan RX, Ge HM. Anti-inflammatory flavonoids from Cryptocarya chingii. Phytochemistry. 2012;76:98–105.CrossRef
  7.Gua JQ, Wang Y, Franzblau SG, Montenegro G, Timmermann BN. Constituents of Quinchamalium majus with potential antitubercular activity. Z Naturforsch C. 2004;59:797–802.
  8.Biondi DM, Rocco C, Ruberto G. New dihydrostilbene derivatives from the leaves of Glycyrrhiza glabra and evaluation of their antioxidant activity. J Nat Prod. 2003;66:477–80.CrossRef
  9.Lan X, Wang W, Li Q, Wang J. The natural flavonoid pinocembrin: molecular targets and potential therapeutic applications. Mol Neurobiol. 2016. doi:10.​1007/​s12035-015-9125-2
  10.Rasul A, Millimouno FM, AliEltayb W, Ali M, Li J, Li X. Pinocembrin: a novel natural compound with versatile pharmacological and biological activities. Biomed Res Int. 2013;2013:379850.CrossRef
  11.Li F, Awale S, Tezuka Y, Esumi H, Kadota S. Study on the constituents of mexican propolis and their cytotoxic activity against PANC-1 human pancreatic cancer cells. J Nat Prod. 2010;73:623–7.CrossRef
  12.Liu R, Li JZ, Song JK, Zhou D, Huang C, Bai XY, Xie T, Zhang X, Li YJ, Wu CX, et al. Pinocembrin improves cognition and protects the neurovascular unit in Alzheimer related deficits. Neurobiol Aging. 2014;35:1275–85.CrossRef
  13.Sayre CL, Takemoto JK, Martinez SE, Davies NM. Chiral analytical method development and application to pre-clinical pharmacokinetics of pinocembrin. Biomed Chromatogr. 2013;27:681–4.CrossRef
  14.Yuan Y, Yang QY, Tong YF, Chen F, Qi Y, Duan YB, Wu S. Synthesis and enantiomeric resolution of (+/−)-pinocembrin. J Asian Nat Prod Res. 2008;10:999–1002.CrossRef
  15.Caccamese S, Caruso C, Parrinello N, Savarino A. High-performance liquid chromatographic separation and chiroptical properties of the enantiomers of naringenin and other flavanones. J Chromatogr A. 2005;1076:155–62.CrossRef
  16.Krause M, Galensa R. Direct enantiomeric separation of racemic flavanones by high-performance liquid chromatography using cellulose triacetate as a chiral stationary phase. J Chromatogr A. 1988;441:417–22.CrossRef
  17.Trantas EA, Koffas MA, Xu P, Ververidis F. When plants produce not enough or at all: metabolic engineering of flavonoids in microbial hosts. Front Plant Sci. 2015;6:7.CrossRef
  18.Wu J, Du G, Zhou J, Chen J. Metabolic engineering of Escherichia coli for (2S)-pinocembrin production from glucose by a modular metabolic strategy. Metab Eng. 2013;16:48–55.CrossRef
  19.Miyahisa I, Kaneko M, Funa N, Kawasaki H, Kojima H, Ohnishi Y, Horinouchi S. Efficient production of (2S)-flavanones by Escherichia coli containing an artificial biosynthetic gene cluster. Appl Microbiol Biotechnol. 2005;68:498–504.CrossRef
  20.Hwang EI, Kaneko M, Ohnishi Y, Horinouchi S. Production of plant-specific flavanones by Escherichia coli containing an artificial gene cluster. Appl Environ Microbiol. 2003;69:2699–706.CrossRef
  21.Umehara K, Nemoto K, Matsushita A, Terada E, Monthakantirat O, De-Eknamkul W, Miyase T, Warashina T, Degawa M, Noguchi H. Flavonoids from the heartwood of the Thai medicinal plant Dalbergia parviflora and their effects on estrogenic-responsive human breast cancer cells. J Nat Prod. 2009;72:2163–8.CrossRef
  22.Su B-N, Jung Park E, Vigo JS, Graham JG, Cabieses F, Fong HHS, Pezzuto JM, Kinghorn AD. Activity-guided isolation of the chemical constituents of Muntingia calabura using a quinone reductase induction assay. Phytochemistry. 2003;63:335–41.CrossRef
  23.Hegazi AG, Abd El Hady FK, Abd Allah FA. Chemical composition and antimicrobial activity of European propolis. Z Naturforsch C. 2000;55:70–5.CrossRef
  24.Yaw-Lung H, Jim-Min F, Yu-Shia C. Terpenoids and flavonoids from Pseudotsuga wilsoniana. Phytochemistry. 1998;47:845–50.CrossRef
  25.Yang Q-y, Yuan Y, QI Y, Tong Y-f, Wu S. RP-HPLC chiral separation of pinocembrin. Chin J Pharm Anal. 2010;1:029.
  26.Kim BG, Lee H, Ahn JH. Biosynthesis of pinocembrin from glucose using engineered Escherichia coli. J Microbiol Biotechnol. 2014;24:1536–41.
  27.Park SR, Yoon JA, Paik JH, Park JW, Jung WS, Ban YH, Kim EJ, Yoo YJ, Han AR, Yoon YJ. Engineering of plant-specific phenylpropanoids biosynthesis in Streptomyces venezuelae. J Biotechnol. 2009;141:181–8.CrossRef
  28.Yan Y, Kohli A, Koffas MA. Biosynthesis of natural flavanones in Saccharomyces cerevisiae. Appl Environ Microbiol. 2005;71:5610–3.CrossRef
  29.Leonard E, Yan Y, Lim KH, Koffas MA. Investigation of two distinct flavone synthases for plant-specific flavone biosynthesis in Saccharomyces cerevisiae. Appl Environ Microbiol. 2005;71:8241–8.CrossRef
  30.Jiang H, Wood KV, Morgan JA. Metabolic engineering of the phenylpropanoid pathway in Saccharomyces cerevisiae. Appl Environ Microbiol. 2005;71:2962–9.CrossRef
  31.Leonard E, Lim KH, Saw PN, Koffas MA. Engineering central metabolic pathways for high-level flavonoid production in Escherichia coli. Appl Environ Microbiol. 2007;73:3877–86.CrossRef
  32.Yeku O, Frohman MA. Rapid amplification of cDNA ends (RACE). Methods Mol Biol. 2011;703:107–22.CrossRef
  33.Gross GG. From lignins to tannins: forty years of enzyme studies on the biosynthesis of phenolic compounds. Phytochemistry. 2008;69:3018–31.CrossRef
  34.Gosch C, Halbwirth H, Kuhn J, Miosic S, Stich K. Biosynthesis of phloridzin in apple (Malus domestica Borkh.). Plant Sci. 2009;176:223–31.CrossRef
  35.Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M. Purification, cloning, and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem. 2003;278:95–103.CrossRef
  36.Holser R. Kinetics of cinnamoyl glycerol formation. J Am Oil Chem Soc. 2008;85:221–5.CrossRef
  37.Kaneko M, Hwang EI, Ohnishi Y, Horinouchi S. Heterologous production of flavanones in Escherichia coli: potential for combinatorial biosynthesis of flavonoids in bacteria. J Ind Microbiol Biotechnol. 2003;30:456–61.CrossRef
  38.Abdullah N, Sahibul-Anwar H, Ideris S, Hasuda T, Hitotsuyanagi Y, Takeya K, Diederich M, Choo C. Goniolandrene A and B from Goniothalamus macrophyllus. Fitoterapia. 2013;88:1–6.CrossRef
  39.Grote A, Hiller K, Scheer M, Munch R, Nortemann B, Hempel DC, Jahn D. JCat: a novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Res. 2005;33:W526–31.CrossRef
  40.Flores S, de Anda-Herrera R, Gosset G, Bolívar FG. Growth-rate recovery of Escherichia coli cultures carrying a multicopy plasmid, by engineering of the pentose-phosphate pathway. Biotechnol Bioeng. 2004;87:485–94.CrossRef
  41.Glick BR. Metabolic load and heterologous gene expression. Biotechnol Adv. 1995;13:247–61.CrossRef
  42.Takamura Y, Nomura G. Changes in the intracellular concentration of acetyl-CoA and malonyl-CoA in relation to the carbon and energy metabolism of Escherichia coli K12. J Gen Microbiol. 1988;134:2249–53.
  43.Leonard E, Yan Y, Fowler ZL, Li Z, Lim CG, Lim KH, Koffas MA. Strain improvement of recombinant Escherichia coli for efficient production of plant flavonoids. Mol Pharm. 2008;5:257–65.CrossRef
  44.Gao X, Wang P, Tang Y. Engineered polyketide biosynthesis and biocatalysis in Escherichia coli. Appl Microbiol Biotechnol. 2010;88:1233–42.CrossRef
  45.Hutt AJ. Chirality and pharmacokinetics: an area of neglected dimensionality? Drug Metabol Drug Interact. 2007;22:79–112.
  46.Smith SW. Chiral toxicology: it’s the same thing…only different. Toxicol Sci. 2009;110:4–30.CrossRef
  47.Eriksson T, Bjorkman S, Hoglund P. Clinical pharmacology of thalidomide. Eur J Clin Pharmacol. 2001;57:365–76.CrossRef
  48.Gui J, Shen J, Li L. Functional characterization of evolutionarily divergent 4-coumarate:coenzyme a ligases in rice. Plant Physiol. 2011;157:574–86.CrossRef
  49.Gaid MM, Scharnhop H, Ramadan H, Beuerle T, Beerhues L. 4-Coumarate:CoA ligase family members from elicitor-treated Sorbus aucuparia cell cultures. J Plant Physiol. 2011;168:944–51.CrossRef
  50.Silber MV, Meimberg H, Ebel J. Identification of a 4-coumarate:CoA ligase gene family in the moss, Physcomitrella patens. Phytochemistry. 2008;69:2449–56.CrossRef
  51.Ehlting J, Buttner D, Wang Q, Douglas CJ, Somssich IE, Kombrink E. Three 4-coumarate:coenzyme A ligases in Arabidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 1999;19:9–20.CrossRef
  52.Schneider K, Hovel K, Witzel K, Hamberger B, Schomburg D, Kombrink E, Stuible HP. The substrate specificity-determining amino acid code of 4-coumarate:CoA ligase. Proc Natl Acad Sci USA. 2003;100:8601–6.CrossRef
  53.Ehlting J, Shin JJ, Douglas CJ. Identification of 4-coumarate:coenzyme a ligase (4CL) substrate recognition domains. Plant J. 2001;27:455–65.CrossRef
  54.Abe I, Morita H. Structure and function of the chalcone synthase superfamily of plant type III polyketide synthases. Nat Prod Rep. 2010;27:809–38.CrossRef
  55.Austin MB, Noel JP. The chalcone synthase superfamily of type III polyketide synthases. Nat Prod Rep. 2003;20:79–110.CrossRef
  56.Ferrer JL, Jez JM, Bowman ME, Dixon RA, Noel JP. Structure of chalcone synthase and the molecular basis of plant polyketide biosynthesis. Nat Struct Biol. 1999;6:775–84.CrossRef
  57.Koopman F, Beekwilder J, Crimi B, van Houwelingen A, Hall RD, Bosch D, van Maris AJ, Pronk JT, Daran JM. De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae. Microb Cell Fact. 2012;11:155.CrossRef
  58.Watts KT, Lee PC, Schmidt-Dannert C. Exploring recombinant flavonoid biosynthesis in metabolically engineered Escherichia coli. Chembiochem. 2004;5:500–7.CrossRef
  59.Miyahisa I, Funa N, Ohnishi Y, Martens S, Moriguchi T, Horinouchi S. Combinatorial biosynthesis of flavones and flavonols in Escherichia coli. Appl Microbiol Biotechnol. 2006;71:53–8.CrossRef
  60.Wu J, Liu P, Fan Y, Bao H, Du G, Zhou J, Chen J. Multivariate modular metabolic engineering of Escherichia coli to produce resveratrol from l -tyrosine. J Biotechnol. 2013;167:404–11.CrossRef
  61.Gao S, Yu HN, Xu RX, Cheng AX, Lou HX. Cloning and functional characterization of a 4-coumarate CoA ligase from liverwort Plagiochasma appendiculatum. Phytochemistry. 2015;111:48–58.CrossRef
  62.Li ZB, Li CF, Li J, Zhang YS. Molecular cloning and functional characterization of two divergent 4-coumarate : coenzyme A ligases from Kudzu (Pueraria lobata). Biol Pharm Bull. 2014;37:113–22.CrossRef
  63.Yu HN, Wang L, Sun B, Gao S, Cheng AX, Lou HX. Functional characterization of a chalcone synthase from the liverwort Plagiochasma appendiculatum. Plant Cell Rep. 2015;34:233–45.CrossRef
  64.Sun W, Meng X, Liang L, Jiang W, Huang Y, He J, Hu H, Almqvist J, Gao X, Wang L. Molecular and biochemical analysis of chalcone synthase from Freesia hybrid in flavonoid biosynthetic pathway. PLoS One. 2015;10:e0119054.CrossRef
  65.Cheng H, Li L, Cheng S, Cao F, Wang Y, Yuan H. Molecular cloning and function assay of a chalcone isomerase gene (GbCHI) from Ginkgo biloba. Plant Cell Rep. 2011;30:49–62.CrossRef
  66.Kong J-Q. Phenylalanine ammonia-lyase, a key component used for phenylpropanoids production by metabolic engineering. RSC Adv. 2015;5:62587–603.CrossRef
  67.Zhu S, Wu J, Du G, Zhou J, Chen J. Efficient synthesis of eriodictyol from L-Tyrosine in Escherichia coli. Appl Environ Microbiol. 2014;80:3072–80.CrossRef
  68.Veliky IA, Martin SM. A fermenter for plant cell suspension cultures. Can J Microbiol. 1970;16:223–6.CrossRef
  69.Wang Z-B, Chen X, Wang W, Cheng K-D, Kong J-Q. Transcriptome-wide identification and characterization of Ornithogalum saundersiae phenylalanine ammonia lyase gene family. RSC Adv. 2014;4:27159–75.CrossRef
  70.Guo L, Kong JQ. cDNA cloning and expression analysis of farnesyl pyrophosphate synthase from Ornithogalum saundersiae. Z Naturforsch C. 2014;69:259–70.CrossRef
  71.Kong JQ, Lu D, Wang ZB. Molecular cloning and yeast expression of cinnamate 4-hydroxylase from Ornithogalum saundersiae baker. Molecules. 2014;19:1608–21.CrossRef
  72.Malla S, Koffas MA, Kazlauskas RJ, Kim BG. Production of 7-O-methyl aromadendrin, a medicinally valuable flavonoid, in Escherichia coli. Appl Environ Microbiol. 2012;78:684–94.CrossRef
  73.McKhann HI, Hirsch AM. Isolation of chalcone synthase and chalcone isomerase cDNAs from alfalfa (Medicago sativa L.): highest transcript levels occur in young roots and root tips. Plant Mol Biol. 1994;24:767–77.CrossRef
  74.van Summeren-Wesenhagen PV, Marienhagen J. Metabolic engineering of Escherichia coli for the synthesis of the plant polyphenol pinosylvin. Appl Environ Microbiol. 2015;81:840–9.CrossRef
  75.Santos CN, Koffas M, Stephanopoulos G. Optimization of a heterologous pathway for the production of flavonoids from glucose. Metab Eng. 2011;13:392–400.CrossRef
  76.Moche M, Schneider G, Edwards P, Dehesh K, Lindqvist Y. Structure of the complex between the antibiotic cerulenin and its target, beta-ketoacyl-acyl carrier protein synthase. J Biol Chem. 1999;274:6031–4.CrossRef
  
• 作者单位：Lei Guo (1)
  Xi Chen (1) (2)
  Li-Na Li (1)
  Wei Tang (2)
  Yi-Ting Pan (3)
  Jian-Qiang Kong (1)
  
  1. Institute of Materia Medica, Chinese Academy of Medical Sciences and Peking Union Medical College (State Key Laboratory of Bioactive Substance and Function of Natural Medicines & Ministry of Health Key Laboratory of Biosynthesis of Natural Products), Beijing, 100050, China
  2. School of Medicine of Wuhan University, Wuhan, China
  3. School of Chemical Engineering, Beijing Institute of Petrochemical Technology, Beijing, China
  
• 刊物类别：Chemistry and Materials Science
• 刊物主题：Biotechnology
  Applied Microbiology
  Environmental Engineering/Biotechnology
  
• 出版者：BioMed Central
• ISSN：1475-2859

文摘

Background (2S)-Pinocembrin is a chiral flavanone with versatile pharmacological and biological activities. Its health-promoting effects have spurred on research effects on the microbial production of (2S)-pinocembrin. However, an often-overlooked salient feature in the analysis of microbial (2S)-pinocembrin is its chirality.