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Applied Microbiology and Biotechnology

, Volume 103, Issue 7, pp 2959–2972 | Cite as

Biosynthesis of resveratrol and piceatannol in engineered microbial strains: achievements and perspectives

  • Anil Shrestha
  • Ramesh Prasad Pandey
  • Jae Kyung SohngEmail author
Mini-Review
  • 391 Downloads

Abstract

Resveratrol (3,5,4′-trihydroxystilbene) and piceatannol (3,5,3′,4′-tetrahydroxystilbene) are well-known natural products that are produced by plants. They are important ingredients in pharmaceutical industries and nutritional supplements. They display a wide spectrum of biological activity. Thus, the needs for these compounds are increasing. The natural products have been found in diverse plants, mostly such as grapes, passion fruit, white tea, berries, and many more. The extraction of these products from plants is quite impractical because of the low production in plants, downstream processing difficulties, chemical hazards, and environmental issues. Thus, alternative production in microbial hosts has been devised with combinatorial biosynthetic systems, including metabolic engineering, synthetic biology, and optimization in production process. Since the biosynthesis is not native in microbial hosts such as Escherichia coli, Saccharomyces cerevisiae, and Corynebacterium glutamicum, genetic engineering and manipulation have made it possible. In this review, the discussion will mainly focus on recent progress in production of resveratrol and piceatannol, including the various strategies used for their production.

Keywords

Resveratrol Piceatannol Metabolic engineering Pathway engineering Combinatorial synthesis 

Notes

Funding information

This work was supported by a grant from the Next-Generation BioGreen 21 Program (SSAC, grant no.: PJ013137), Rural Development Administration, Republic of Korea.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Competing interests

The authors declare that they have no competing interests.

References

  1. Afonso MS, Ferreira S, Domingues FC, Silva F (2014) Resveratrol production in bioreactor: assessment of cell physiological states and plasmid segregational stability. Biotechnol Rep (Amst) 5:7–13Google Scholar
  2. Almagro L, Belchí-Navarro S, Sabater-Jara AB, Vera-Urbina JC, Sellés-Marchart S, Bru R, Pedreño MA (2013) Bioproduction of trans-resveratrol from grapevine cell cultures. In: Ramawat K, Mérillon JM (eds) Natural products. Springer, Berlin, pp 1683–1713.  https://doi.org/10.1007/978-3-642-22144-6_54 Google Scholar
  3. Anekonda TS (2006) Resveratrol—a boon for treating Alzheimer’s disease? Brain Res Rev 52(2):316–326.  https://doi.org/10.1016/j.brainresrev.2006.04.004 Google Scholar
  4. Bai T, Dong DS, Pei L (2014) Synergistic antitumor activity of resveratrol and miR-200c in human lung cancer. Oncol Rep 31(5):2293–2297.  https://doi.org/10.3892/or.2014.3090 Google Scholar
  5. Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5:493–506.  https://doi.org/10.1038/nrd2060 Google Scholar
  6. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JA et al (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342Google Scholar
  7. Bavaresco L, Vezzulli S, Battilani P, Giorni P, Pietri A, Bertuzzi T (2003) Effect of ochratoxin A-producing Aspergilli on stilbenic phytoalexin synthesis in grapes. J Agric Food Chem 51(21):6151–6157.  https://doi.org/10.1021/jf0301908 Google Scholar
  8. Beekwilder J, Wolswinkel R, Jonker H, Hall R, de Vos CR, Bovy A (2006) Production of resveratrol in recombinant microorganisms. Appl Environ Microbiol 72(8):5670–5672.  https://doi.org/10.1128/AEM.00609-06 Google Scholar
  9. Beňová B, Adam M, Onderková K, Královský J, Krajíček M (2008) Analysis of selected stilbenes in Polygonum cuspidatum by HPLC coupled with CoulArray detection. J Sep Sci 31(13):2404–2409.  https://doi.org/10.1002/jssc.200800119 Google Scholar
  10. Berrougui H, Grenier G, Loued S, Drouin G, Khalil A (2009) A new insight into resveratrol as an atheroprotective compound: inhibition of lipid peroxidation and enhancement of cholesterol efflux. Atherosclerosis 207(2):420–427.  https://doi.org/10.1016/j.atherosclerosis.2009.05.017 Google Scholar
  11. Bhan N, Xu P, Khalidi O, Koffas MAG (2013) Redirecting carbon flux into malonyl-CoA to improve resveratrol titers: proof of concept for genetic interventions predicted by OptForce computational framework. Chem Eng Sci 103:109–114.  https://doi.org/10.1016/j.ces.2012.10.009 Google Scholar
  12. Bhullar KS, Hubbard BP (2015) Lifespan and healthspan extension by resveratrol. Biochim Biophys Acta 1852(6):1209–1218.  https://doi.org/10.1016/j.bbadis.2015.01.012 Google Scholar
  13. Borriello A, Bencivenga D, Caldarelli I, Tramontano A, Borgia A, Zappia V, Della Ragione F (2014) Resveratrol: from basic studies to bedside. In: Zappia V, Panico S, Russo G, Budillon A, Della Ragione F (eds) Advances in nutrition and cancer. Cancer treatment and research, vol 159. Springer, BerlinGoogle Scholar
  14. Boue SM, Shih BY, Burow ME, Eggleston G, Lingle S, Pan YB, Daigle K, Bhatnagar D (2013) Postharvest accumulation of resveratrol and piceatannol in sugarcane with enhanced antioxidant activity. J Agric Food Chem 61(35):8412–8419.  https://doi.org/10.1021/jf4020087 Google Scholar
  15. Bradamante S, Barenghi L, Villa A (2004) Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev 22(3):169–188.  https://doi.org/10.1111/j.1527-3466.2004.tb00139.x Google Scholar
  16. Braga A, Ferreira P, Oliveira J, Rocha I, Faria N (2018a) Heterologous production of resveratrol in bacterial hosts: current status and perspectives. World J Microbiol Biotechnol 34(8):122.  https://doi.org/10.1007/s11274-018-2506-8 Google Scholar
  17. Braga A, Oliveira J, Silva R, Ferreira P, Rocha I, Kallscheuer N, Marienhagen J, Faria N (2018b) Impact of the cultivation strategy on resveratrol production from glucose in engineered Corynebacterium glutamicum. J Biotechnol 265:70–75.  https://doi.org/10.1016/j.jbiotec.2017.11.006 Google Scholar
  18. Bru R, Sellés S, Casado-Vela J, Belchí-Navarro S, Pedreño MA (2006) Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. J Agric Food Chem 54(1):65–71.  https://doi.org/10.1021/jf051485j Google Scholar
  19. Bulter T, Bernstein JR, Liao JC (2003) A perspective of metabolic engineering strategies: moving up the systems hierarchy. Biotechnol Bioeng 84(7):815–821.  https://doi.org/10.1002/bit.10845 Google Scholar
  20. Camacho-Zaragoza JM, Hernández-Chávez G, Moreno-Avitia F, Ramírez-Iñiguez R, Martínez A, Bolívar F, Gosset G (2016) Engineering of a microbial coculture of Escherichia coli strains for the biosynthesis of resveratrol. Microb Cell Factories 15(1):163.  https://doi.org/10.1186/s12934-016-0562-z Google Scholar
  21. Cantos E, Espín JC, Fernández MJ, Oliva J, Tomás-Barberán FA (2003) Postharvest UV-C-irradiated grapes as a potential source for producing stilbene-enriched red wines. J Agric Food Chem 51(5):1208–1214.  https://doi.org/10.1021/jf020939z Google Scholar
  22. Carpéné C, Pejenaute H, del Moral R, Boulet N, Hijona E, Andrade F, Villanueva-Millán M, Aguirre L, Arbones-Mainar JM (2018) The dietary antioxidant piceatannol inhibits adipogenesis of human adipose mesenchymal stem cells and limits glucose transport and lipogenic activities in adipocytes. Int J Mol Sci 19(7):2081.  https://doi.org/10.3390/ijms19072081 Google Scholar
  23. Choi O, Wu CZ, Kang SY, Ahn JS, Uhm TB, Hong YS (2011) Biosynthesis of plant-specific phenylpropanoids by construction of an artificial biosynthetic pathway in Escherichia coli. J Ind Microbiol Biotechnol 38(10):1657–1665.  https://doi.org/10.1007/s10295-011-0954-3 Google Scholar
  24. Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177(3):143–155.  https://doi.org/10.1016/j.plantsci.2009.05.012 Google Scholar
  25. Chu LL, Pandey RP, Jung N, Jung HJ, Kim EH, Sohng JK (2016) Hydroxylation of diverse flavonoids by CYP450 BM3 variants: biosynthesis of eriodictyol from naringenin in whole cells and its biological activities. Microb Cell Factories 15(1):135Google Scholar
  26. de Fouchécour F, Sánchez-Castañeda A-K, Saulou-Bérion C, Spinnler H (2018) Process engineering for microbial production of 3-hydroxypropionic acid. Biotechnol Adv 36(4):1207–1222.  https://doi.org/10.1016/j.biotechadv.2018.03.020 Google Scholar
  27. De La Lastra CA, Villegas I (2005) Resveratrol as an anti inflammatory and anti-aging agent: mechanisms and clinical implications. Mol Nutr Food Res 49(5):405–430.  https://doi.org/10.1002/mnfr.200500022 Google Scholar
  28. Deng N, Liu C, Chang E, Ji J, Yao X, Yue J, Bartish IV, Chen L, Jiang Z, Shi S (2017) High temperature and UV-C treatments affect stilbenoid accumulation and related gene expression levels in Gnetum parvifolium. Electron J Biotechnol 25:43–49.  https://doi.org/10.1016/j.ejbt.2016.11.001 Google Scholar
  29. Du J, Shao Z, Zhao H (2011) Engineering microbial factories for synthesis of value-added products. J Ind Microbiol Biotechnol 38(8):873–890.  https://doi.org/10.1007/s10295-011-0970-3 Google Scholar
  30. Dubrovina AS, Kiselev KV (2017) Regulation of stilbene biosynthesis in plants. Planta 246(4):597–623.  https://doi.org/10.1007/s00425-017-2730-8 Google Scholar
  31. Fernández-Mar MI, Mateos R, García-Parrilla MC, Puertas B, Cantos-Villar E (2012) Bioactive compounds in wine: resveratrol, hydroxytyrosol and melatonin: a review. Food Chem 130(4):797–813.  https://doi.org/10.1016/j.foodchem.2011.08.023 Google Scholar
  32. Finzel K, Lee DJ, Burkart MD (2015) Using modern tools to probe the structure–function relationship of fatty acid synthases. Chembiochem 16(4):528–547.  https://doi.org/10.1002/cbic.201402578 Google Scholar
  33. Frombaum M, Le Clanche S, Bonnefont-Rousselot D, Borderie D (2012) Antioxidant effects of resveratrol and other stilbene derivatives on oxidative stress and NO bioavailability: potential benefits to cardiovascular diseases. Biochimie 94(2):269–276.  https://doi.org/10.1016/j.biochi.2011.11.001 Google Scholar
  34. Frommeyer G, Wolfes J, Ellermann C, Kochhäuser S, Dechering DG, Eckardt L (2018) Acute electrophysiologic effects of the polyphenols resveratrol and piceatannol in rabbit atria. Clin Exp Pharmacol Physiol (Accepted) 46:94–98.  https://doi.org/10.1111/1440-1681.13005 Google Scholar
  35. Furuya T, Kino K (2014) Regioselective synthesis of piceatannol from resveratrol: catalysis by two-component flavin-dependent monooxygenase HpaBC in whole cells. Tetrahedron Lett 55(17):2853–2855.  https://doi.org/10.1016/j.tetlet.2014.03.076 Google Scholar
  36. Furuya T, Sai M, Kino K (2018) Efficient monooxygenase-catalyzed piceatannol production: application of cyclodextrins for reducing product inhibition. J Biosci Bioeng 126(4):478–481.  https://doi.org/10.1016/j.jbiosc.2018.04.016 Google Scholar
  37. Halls C, Yu O (2008) Potential for metabolic engineering of resveratrol biosynthesis. Trends Biotechnol 26(2):77–81.  https://doi.org/10.1016/j.tibtech.2007.11.002 Google Scholar
  38. Hamberger B, Hahlbrock K (2004) The 4-coumarate: CoA ligase gene family in Arabidopsis thaliana comprises one rare, sinapate-activating and three commonly occurring isoenzymes. Proc Natl Acad Sci 101:2209–2214.  https://doi.org/10.1073/pnas.0307307101 Google Scholar
  39. Heo KT, Kang SY, Jang JH, Hong YS (2017) Sam5, a Coumarate 3-hydroxylase from Saccharothrix espanaensis: new insight into the piceatannol production as a resveratrol 3’-hydroxylase. ChemistrySelect 2(28):8785–8789.  https://doi.org/10.1002/slct.201701969 Google Scholar
  40. Holthoff JH, Woodling KA, Doerge DR, Burns ST, Hinson JA, Mayeux PR (2010) Resveratrol, a dietary polyphenolic phytoalexin, is a functional scavenger of peroxynitrite. Biochem Pharmacol 80(8):1260–1265.  https://doi.org/10.1016/j.bcp.2010.06.027 Google Scholar
  41. Huang LL, Xue Z, Zhu QQ (2010) inventors; EI du Pont de Nemours and Co, assignee. Method for the production of resveratrol in a recombinant oleaginous microorganism. United States patent US 7,772,444. Aug 10Google Scholar
  42. Huang Q, Lin Y, Yan Y (2013) Caffeic acid production enhancement by engineering a phenylalanine over-producing Escherichia coli strain. Biotechnol Bioeng 110(12):3188–3196.  https://doi.org/10.1002/bit.24988 Google Scholar
  43. Hubbard BP, Sinclair DA (2014) Small molecule SIRT1 activators for the treatment of aging and age-related diseases. Trends Pharmacol Sci 35:146–154Google Scholar
  44. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275(5297):218–220.  https://doi.org/10.1126/science.275.5297.218 Google Scholar
  45. Jiang H, Wood KV, Morgan J (2005) Metabolic engineering of the phenylpropanoid pathway in Saccharomyces cerevisiae. Appl Environ Microbiol 71(6):2962–2969.  https://doi.org/10.1128/AEM.71.6.2962 Google Scholar
  46. Juminaga D, Baidoo EE, Redding-Johanson AM, Batth TS, Burd H, Mukhopadhyay A, Petzold CJ, Keasling JD (2012) Modular engineering of L-tyrosine production in Escherichia coli. Appl Environ Microbiol 78(1):89–98.  https://doi.org/10.1128/AEM.06017-11 Google Scholar
  47. Kallscheuer N, Vogt M, Stenzel A, Gätgens J, Bott M, Marienhagen J (2016) Construction of a Corynebacterium glutamicum platform strain for the production of stilbenes and (2S)-flavanones. Metab Eng 38:47–55.  https://doi.org/10.1016/j.ymben.2016.06.003 Google Scholar
  48. Kalra N, Roy P, Prasad S, Shukla Y (2008) Resveratrol induces apoptosis involving mitochondrial pathways in mouse skin tumorigenesis. Life Sci 82(7–8):348–358.  https://doi.org/10.1016/j.lfs.2007.11.006 Google Scholar
  49. Kang SY, Lee JK, Choi O, Kim CY, Jang JH, Hwang BY, Hong YS (2014) Biosynthesis of methylated resveratrol analogs through the construction of an artificial biosynthetic pathway in E. coli. BMC Biotechnol 14(1):67.  https://doi.org/10.1186/1472-6750-14-67 Google Scholar
  50. Katsuyama Y, Funa N, Horinouchi S (2007a) Precursor-directed biosynthesis of stilbene methyl ethers in Escherichia coli. Biotechnol J 2(10):1286–1293.  https://doi.org/10.1002/biot.200700098 Google Scholar
  51. Katsuyama Y, Funa N, Miyahisa I, Horinouchi S (2007b) Synthesis of unnatural flavonoids and stilbenes by exploiting the plant biosynthetic pathway in Escherichia coli. Chem Biol 14(6):613–621.  https://doi.org/10.1016/j.chembiol.2007.05.004 Google Scholar
  52. Katz M, Smits HP, Förster J, Nielsen JB, Evola SA (2015) Metabolically engineered cells for the production of resveratrol or an oligomeric or glycosidically-bound derivative thereof. United States patent US 9,040,269. 2015 May 26Google Scholar
  53. Kim DH, Ahn T, Jung HC, Pan JG, Yun CH (2009) Generation of the human metabolite piceatannol from the anticancer-preventive agent resveratrol by bacterial cytochrome P450 BM3. Drug Metab Dispos 37(5):932–926Google Scholar
  54. King FE, King TJ, Godson DH, Manning LC (1956) The chemistry of extractives from hardwoods Part XXVIII The occurrence of 3:4:3′:5′-tetrahydroxy-and 3:4:5:3′:5′-pentahydroxy-stilbene in Vouacapoua species. J Chem Soc (Resumed) 0:4477–4480.  https://doi.org/10.1039/JR9560004477 Google Scholar
  55. Kiselev KV, Grigorchuk VP, Ogneva ZV, Suprun AR, Dubrovina AS (2016) Stilbene biosynthesis in the needles of spruce Picea jezoensis. Phytochemistry 131:57–67.  https://doi.org/10.1016/j.phytochem.2016.08.011 Google Scholar
  56. Krivoruchko A, Nielsen J (2015) Production of natural products through metabolic engineering of Saccharomyces cerevisiae. Curr Opin Biotechnol 35:7–15.  https://doi.org/10.1016/j.copbio.2014.12.004 Google Scholar
  57. Ku KL, Chang PS, Cheng YC, Lien CY (2005) Production of stilbenoids from the callus of Arachis hypogaea: a novel source of the anticancer compound piceatannol. J Agric Food Chem 53(10):3877–3881.  https://doi.org/10.1021/jf050242o Google Scholar
  58. Lambert C, Richard T, Renouf E, Bisson J, Waffo-Téguo P, Bordenave L, Ollat N, Mérillon JM, Cluzet S (2013) Comparative analyses of stilbenoids in canes of major Vitis vinifera L. cultivars. J Agric Food Chem 61(47):11392–11399.  https://doi.org/10.1021/jf403716y Google Scholar
  59. Lancon A, Kaminski J, Tili E, Michaille JJ, Latruffe N (2012) Control of microRNA expression as a new way for resveratrol to deliver its beneficial effects. J Agric Food Chem 60(36):8783–8789.  https://doi.org/10.1021/jf301479v Google Scholar
  60. Lee N, Kim EJ, Kim BG (2012) Regioselective hydroxylation of trans-resveratrol via inhibition of tyrosinase from Streptomyces avermitilis MA4680. ACS Chem Biol 7(10):1687–1692.  https://doi.org/10.1021/cb300222b Google Scholar
  61. Lee N, Lee SH, Baek K, Kim BG (2015) Heterologous expression of tyrosinase (MelC2) from Streptomyces avermitilis MA4680 in E. coli and its application for ortho-hydroxylation of resveratrol to produce piceatannol. Appl Microbiol Biotechnol 99(19):7915–7924.  https://doi.org/10.1007/s00253-015-6691-1 Google Scholar
  62. Li M, Kildegaard KR, Chen Y, Rodriguez A, Borodina I, Nielsen J (2015) De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae. Metab Eng 32:1–11.  https://doi.org/10.1016/j.ymben.2015.08.007 Google Scholar
  63. Li M, Schneider K, Kristensen M, Borodina I, Nielsen J (2016) Engineering yeast for high-level production of stilbenoid antioxidants. Sci Rep 6:1–8.  https://doi.org/10.1038/srep36827 Google Scholar
  64. Lim CG, Fowler ZL, Hueller T, Schaffer S, Koffas MA (2011) High-yield resveratrol production in engineered Escherichia coli. Appl Environ Microbiol 77(10):3451–3460.  https://doi.org/10.1128/AEM.02186-10 Google Scholar
  65. Lin Y, Yan Y (2014) Biotechnological production of plant-specific hydroxylated phenylpropanoids. Biotechnol Bioeng 111(9):1895–1899.  https://doi.org/10.1002/bit.25237 Google Scholar
  66. Lin LL, Lien CY, Cheng YC, Ku KL (2007) An effective sample preparation approach for screening the anticancer compound piceatannol using HPLC coupled with UV and fluorescence detection. J Chromatogr B 853(1–2):175–182.  https://doi.org/10.1016/j.jchromb.2007.03.007 Google Scholar
  67. Liu CC, Zhang LL, An J, Chen B, Yang H (2016) Recent strategies for efficient production of polyhydroxyalkanoates by micro-organisms. Lett Appl Microbiol 62:9–15Google Scholar
  68. Lorenz P, Roychowdhury S, Engelmann M, Wolf G, Horn TF (2003) Oxyresveratrol and resveratrol are potent antioxidants and free radical scavengers: effect on nitrosative and oxidative stress derived from microglial cells. Nitric Oxide 9(2):64–76.  https://doi.org/10.1016/j.niox.2003.09.005 Google Scholar
  69. Lu Y, Shao D, Shi J, Huang Q, Yang H, Jin M (2016) Strategies for enhancing resveratrol production and the expression of pathway enzymes. Appl Microbiol Biotechnol 100(17):7407–7421.  https://doi.org/10.1007/s00253-016-7723-1 Google Scholar
  70. Lucas J, Hsieh TC, Halicka HD, Darzynkiewicz Z, Wu JM (2018) Upregulation of PD-L1 expression by resveratrol and piceatannol in breast and colorectal cancer cells occurs via HDAC3/p300-mediated NF-κB signaling. Int J Oncol 53(4):1469–1480.  https://doi.org/10.3892/ijo.2018.4512 Google Scholar
  71. Lütke-Eversloh T, Stephanopoulos G (2007) L-tyrosine production by deregulated strains of Escherichia coli. Appl Microbiol Biotechnol 5(1):103–110.  https://doi.org/10.1007/s00253-006-0792-9 Google Scholar
  72. MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85(3):273–282.  https://doi.org/10.1139/O07-018 Google Scholar
  73. Maeurer M, Rao M, Zumla A (2016) Host-directed therapies for antimicrobial resistant respiratory tract infections. Curr Opin Pulm Med 22:203–211Google Scholar
  74. Marienhagen J, Bott M (2013) Metabolic engineering of microorganisms for the synthesis of plant natural products. J Biotechnol 163(2):166–178.  https://doi.org/10.1016/j.jbiotec.2012.06.001 Google Scholar
  75. Maruki-Uchida H, Morita M, Yonei Y, Sai M (2018) Effect of passion fruit seed extract rich in piceatannol on the skin of women: a randomized, placebo-controlled, double-blind trial. J Nutr Sci Vitaminol 64(1):75–80.  https://doi.org/10.3177/jnsv.64.75 Google Scholar
  76. Matsui Y, Sugiyama K, Kamei M, Takahashi T, Suzuki T, Katagata Y, Ito T (2010) Extract of passion fruit (Passiflora edulis) seed containing high amounts of piceatannol inhibits melanogenesis and promotes collagen synthesis. J Agric Food Chem 58(20):11112–11118.  https://doi.org/10.1021/jf102650d Google Scholar
  77. McFadyen MC, Murray GI (2005) Cytochrome P450 1B1: a novel anticancer therapeutic target. Future Oncol 1(2):259–263.  https://doi.org/10.1517/14796694.1.2.259 Google Scholar
  78. Mei YZ, Liu RX, Wang DP, Wang X, Dai CC (2015) Biocatalysis and biotransformation of resveratrol in microorganisms. Biotechnol Lett 37(1):9–18.  https://doi.org/10.1007/s10529-014-1651-x Google Scholar
  79. Mikulski D, Go’rniak R, Molski M (2010) A theoretical study of the structure-radical scavenging activity of trans-resveratrol analogues and cis-resveratrol in gas phase and water environment. Eur J Med Chem 45(3):1015–1027.  https://doi.org/10.1016/j.ejmech.2009.11.044 Google Scholar
  80. Na D, Yoo SM, Chung H, Park H, Park JH, Lee SY (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat Biotechnol 31(2):170–174.  https://doi.org/10.1038/nbt.2461 Google Scholar
  81. Nijampatnam B, Zhang H, Cai X, Michalek SM, Wu H, Velu SE (2018) Inhibition of Streptococcus mutans biofilms by the natural stilbene piceatannol through the inhibition of glucosyltransferases. ACS Omega 3(7):8378–8385.  https://doi.org/10.1021/acsomega.8b00367 Google Scholar
  82. Okawara M, Katsuki H, Kurimoto E, Shibata H, Kume T, Akaike A (2007) Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol 73(4):550–560.  https://doi.org/10.1016/j.bcp.2006.11.003 Google Scholar
  83. Ovesná Z, Kozics K, Bader Y, Saiko P, Handler N, Erker T, Szekeres T (2006) Antioxidant activity of resveratrol, piceatannol and 3,3′,4,4′,5,5′-hexahydroxy-trans-stilbene in three leukemia cell lines. Oncol Rep 16(3):617–624.  https://doi.org/10.3892/or.16.3.617 Google Scholar
  84. Pandey RP, Parajuli P, Koffas MAG, Sohng JK (2016) Microbial production of natural and non-natural flavonoids: pathway engineering, directed evolution and systems/synthetic biology. Biotechnol Adv 34(5):634–662Google Scholar
  85. Park SR, Yoon JA, Paik JH, Park JW, Jung WS, Ban YH, Kim EJ, Yoo YJ, Han AR, Yoon YJ (2009) Engineering of plant-specific phenylpropanoids biosynthesis in Streptomyces venezuelae. J Biotechnol 141(3–4):181–188.  https://doi.org/10.1016/j.jbiotec.2009.03.013 Google Scholar
  86. Paul B, Chereyathmanjiyil A, Masih I, Chapuis L, Benoı̂t A (1998) Biological control of Botrytis cinerea causing grey mould disease of grapevine and elicitation of stilbene phytoalexin (resveratrol) by a soil bacterium. FEMS Microbiol Lett 165(1):65–70.  https://doi.org/10.1111/j.1574-6968.1998.tb13128.x Google Scholar
  87. Pickens LB, Tang Y, Chooi YH (2011) Metabolic engineering for the production of natural products. Annu Rev Chem Biomol Eng 2:211–236.  https://doi.org/10.1146/annurev-chembioeng-061010-114209 Google Scholar
  88. Potter GA, Patterson LH, Wanogho E, Perry PJ, Butler PC, Ijaz T, Ruparelia KC, Lamb JH, Farmer PB, Stanley LA, Burke MD (2002) The cancer preventative agent resveratrol is converted to the anticancer agent piceatannol by the cytochrome P450 enzyme CYP1B1. Br J Cancer 86(5):774–778.  https://doi.org/10.1038/sj.bjc.6600197 Google Scholar
  89. Poulsen MM, Fjeldborg K, Ornstrup MJ, Kjær TN, Nøhr MK, Pedersen SB (2015) Resveratrol and inflammation: challenges in translating pre-clinical findings to improved patient outcomes. Biochim Biophys Acta (BBA)-Mol Basis Dis 1852(6):1124–1136.  https://doi.org/10.1016/j.bbadis.2014.12.024 Google Scholar
  90. Raiber S, Schröder G, Schröder J (1995) Molecular and enzymatic characterization of two stilbene synthases from Eastern white pine (Pinus strobus) A single Arg/His difference determines the activity and the pH dependence of the enzymes. FEBS Lett 361(2–3):299–302.  https://doi.org/10.1016/0014-5793(95)00199-J Google Scholar
  91. Rege SD, Geetha T, Griffin GD, Broderick TL, Babu JR (2014) Neuroprotective effects of resveratrol in Alzheimer disease pathology. Front Aging Neurosci 6(218).  https://doi.org/10.3389/fnagi.2014.00218
  92. Rimal H, Yu SC, Lee JH, Tokutaro Y, Oh TJ (2018) Hydroxylation of resveratrol with DoxA in vitro: an enzyme with the potential for the bioconversion of a bioactive stilbene. J Microbiol Biotechnol 28(4):561–565Google Scholar
  93. Rivière C, Pawlus AD, Mérillon JM (2012) Natural stilbenoids: distribution in the plant kingdom and chemotaxonomic interest in Vitaceae. Nat Prod Rep 29(11):1317–1333.  https://doi.org/10.1039/C2NP20049J Google Scholar
  94. Rodrigues JL, Prather KLJ, Kluskens LD, Rodrigues LR (2015) Heterologous production of curcuminoids. Microbiol Mol Biol Rev 79(1):39–60.  https://doi.org/10.1128/MMBR.00031-14 Google Scholar
  95. Rodriguez A, Kildegaard KR, Li M, Borodina I, Nielsen J (2015) Establishment of a yeast platform strain for production of p-coumaric acid through metabolic engineering of aromatic amino acid biosynthesis. Metab Eng 31:181–188.  https://doi.org/10.1016/j.ymben.2015.08.003 Google Scholar
  96. Rosano GL, Ceccarelli EA (2014) Recombinant protein expression in Escherichia coli: advances and challenges. Front Microbiol 5(172).  https://doi.org/10.3389/fmicb.2014.00172
  97. Rosler J, Krekel F, Amrhein N, Schmid J (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol 113(1):175–179.  https://doi.org/10.1104/pp.113.1.175 Google Scholar
  98. Sahdev S, Khattar SK, Saini KS (2008) Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 307(1–2):249–264.  https://doi.org/10.1007/s11010-007-9603-6 Google Scholar
  99. Sano S, Sugiyama K, Ito T, Katano Y, Ishihata A (2011) Identification of the strong vasorelaxing substance scirpusin B, a dimer of piceatannol, from passion fruit (Passiflora edulis) seeds. J Agric Food Chem 59(11):6209–6213.  https://doi.org/10.1021/jf104959t Google Scholar
  100. Santos CNS, Koffas M, Stephanopoulos G (2011) Optimization of a heterologous pathway for the production of flavonoids from glucose. Metab Eng 13:392–400.  https://doi.org/10.1016/j.ymben.2011.02.002 Google Scholar
  101. Savoia D (2012) Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol 7:979–990.  https://doi.org/10.2217/fmb.12.68 Google Scholar
  102. Sergent T, Kohnen S, Jourez B, Beauve C, Schneider YJ, Vincke C (2014) Characterization of black locust (Robinia pseudoacacia L.) heartwood extractives: identification of resveratrol and piceatannol. Wood Sci Technol 48(5):1005–1017.  https://doi.org/10.1007/s00226-014-0656-x Google Scholar
  103. Shin SY, Han NS, Park YC, Kim MD, Seo JH (2011) Production of resveratrol from p-coumaric acid in recombinant Saccharomyces cerevisiae expressing 4-coumarate:coenzyme A ligase and stilbene synthase genes. Enzyme Microb Technol 48:48–53Google Scholar
  104. Shrestha A, Pandey RP, Pokhrel AR, Dhakal D, Chu LL, Sohng JK (2018) Modular pathway engineering for resveratrol and piceatannol production in engineered Escherichia coli. Appl Microbiol Biotechnol 102(22):9691–9706.  https://doi.org/10.1007/s00253-018-9323-8 Google Scholar
  105. Sobolev VS (2008) Localized production of phytoalexins by peanut (Arachis hypogaea) kernels in response to invasion by Aspergillus species. J Agric Food Chem 56(6):1949–1954.  https://doi.org/10.1021/jf703595w Google Scholar
  106. Stervbo U, Vang O, Bonnesen C (2007) A review of the content of the putative chemopreventive phytoalexin resveratrol in red wine. Food Chem 101:449–457Google Scholar
  107. Subrahmanyam S, Cronan JE Jr (1998) Overproduction of a functional fatty acid biosynthetic enzyme blocks fatty acid synthesis in Escherichia coli. J Bacteriol 180:4596–602Google Scholar
  108. Sun X, Shen X, Jain R, Lin Y, Wang J, Sun J, Wang J, Yan Y, Yuan Q (2015) Synthesis of chemicals by metabolic engineering of microbes. Chem Soc Rev 44(11):3760–3785.  https://doi.org/10.1039/C5CS00159E Google Scholar
  109. Sydor T, Schaffer S, Boles E (2010) Considerable increase in resveratrol production by recombinant industrial yeast strains with use of rich medium. Appl Environ Microbiol 76(10):3361–3363.  https://doi.org/10.1128/AEM.02796-09 Google Scholar
  110. Takamura Y, Nomura G (1988) Changes in the intracellular concentration of acetyl-CoA and malonyl-CoA in relation to the carbon and energy metabolism of Escherichia coli K12. Microbiology 134(8):2249–2253.  https://doi.org/10.1099/00221287-134-8-2249 Google Scholar
  111. Takaoka M (1939) The phenolic substances of white Hellebore (Veratrum grandiflorum Loes fil.) II Oxyresveratrol. Nippon Kagaku Kaishi 60:1261–1264Google Scholar
  112. Tellone E, Galtieri A, Russo A, Giardina B, Ficarra S (2015) Resveratrol: a focus on several neurodegenerative diseases. Oxid Med Cell Longev 2015, Article ID 392169:1–14.  https://doi.org/10.1155/2015/392169 Google Scholar
  113. van Summeren-Wesenhagen PV, Marienhagen J (2015) Metabolic engineering of Escherichia coli for the synthesis of the plant polyphenol pinosylvin. Appl Environ Microbiol 81(3):840–849.  https://doi.org/10.1128/AEM.02966-14 Google Scholar
  114. Vezzulli S, Battilani P, Bavaresco L (2007) Stilbene-synthase gene expression after Aspergillus carbonarius infection in grapes. Am J Enol Vitic 58(1):132–134Google Scholar
  115. Vingtdeux V, Dreses-Werringloer U, Zhao H, Davies P, Marambaud P (2008) Therapeutic potential of resveratrol in Alzheimer’s disease. BMC Neurosci 9:1–5.  https://doi.org/10.1186/1471-2202-9-S2-S6 Google Scholar
  116. Wang Y, Yu O (2012) Synthetic scaffolds increased resveratrol biosynthesis in engineered yeast cells. J Biotechnol 157(1):258–260.  https://doi.org/10.1016/j.jbiotec.2011.11.003 Google Scholar
  117. Wang J, Ho L, Zhao Z, Seror I, Humala N, Dickstein DL, Thiyagarajan M, Percival SS, Talcott ST, Pasinetti GM (2006) Moderate consumption of cabernet sauvignon attenuates abeta neuropathology in a mouse model of Alzheimer’s disease. FASEB J 20:2313–2320.  https://doi.org/10.1096/fj.06-6281com Google Scholar
  118. Wang Y, Halls C, Zhang J, Matsuno M, Zhang Y, Yu O (2011) Stepwise increase of resveratrol biosynthesis in yeast Saccharomyces cerevisiae by metabolic engineering. Metab Eng 13(5):455–463.  https://doi.org/10.1016/j.ymben.2011.04.005 Google Scholar
  119. Wang S, Zhang S, Xiao A, Rasmussen M, Skidmore C, Zhan J (2015) Metabolic engineering of Escherichia coli for the biosynthesis of various phenylpropanoid derivatives. Metab Eng 29:153–159.  https://doi.org/10.1016/j.ymben.2015.03.011 Google Scholar
  120. Wang J, Guleria S, Koffas MA, Yan Y (2016) Microbial production of value-added nutraceuticals. Curr Opin Biotechnol 37:97–104.  https://doi.org/10.1016/j.copbio.2015.11.003 Google Scholar
  121. Wang J, Yang Y, Yan Y (2018) Bioproduction of resveratrol. In: Schwab W, Lange B, Wüst M (eds) Biotechnology of natural products. Springer, Cham, pp 61–79.  https://doi.org/10.1007/978-3-319-67903-7_3 Google Scholar
  122. Watts KT, Lee PC, Schmidt-Dannert C (2006) Biosynthesis of plant-specific stilbene polyketides in metabolically engineered Escherichia coli. BMC Biotechnol 6:1–12.  https://doi.org/10.1186/1472-6750-6-22 Google Scholar
  123. Whitlock NC, Baek SJ (2012) The anticancer effects of resveratrol: modulation of transcription factors. Nutr Cancer 64(4):493–502.  https://doi.org/10.1080/01635581.2012.667862 Google Scholar
  124. Wittgen HG, van Kempen LC (2007) Reactive oxygen species in melanoma and its therapeutic implications. Melanoma Res 17(6):400–409.  https://doi.org/10.1097/CMR.0b013e3282f1d312 Google Scholar
  125. Wu J, Liu P, Fan Y, Bao H, Du G, Zhou J, Chen J (2013) Multivariate modular metabolic engineering of Escherichia coli to produce resveratrol from L-tyrosine. J Biotechnol 167(4):404–411.  https://doi.org/10.1016/j.jbiotec.2013.07.030 Google Scholar
  126. Wu J, Zhou P, Zhang X, Dong M (2017) Efficient de novo synthesis of resveratrol by metabolically engineered Escherichia coli. J Ind Microbiol Biotechnol 44(7):1083–1095.  https://doi.org/10.1007/s10295-017-1937-9 Google Scholar
  127. Xia N, Daiber A, Forstermann U, Li H (2017) Antioxidant effects of resveratrol in the cardiovascular system. Br J Pharmacol 174(12):1633–1646.  https://doi.org/10.1111/bph.13492 Google Scholar
  128. Yang X, Li X, Ren J (2014) From French paradox to cancer treatment: anti-cancer activities and mechanisms of resveratrol. Anti Cancer Agents Med Chem 14:806–825.  https://doi.org/10.2174/1871520614666140521121722 Google Scholar
  129. Yang Y, Lin Y, Li L, Linhardt RJ, Yan Y (2015) Regulating malonyl-CoA metabolism via synthetic antisense RNAs for enhanced biosynthesis of natural products. Metab Eng 29:217–226.  https://doi.org/10.1016/j.ymben.2015.03.018 Google Scholar
  130. Yesilirmak F, Sayers Z (2009) Heterelogous expression of plant genes. Int J Plant Genom 2009, Article ID 296482, 16 pages.  https://doi.org/10.1155/2009/296482
  131. Yokozawa T, Kim YJ (2007) Piceatannol inhibits melanogenesis by its antioxidative actions. Biol Pharm Bull 30(11):2007–2011.  https://doi.org/10.1248/bpb.30.2007 Google Scholar
  132. Zha W, Rubin-Pitel SB, Shao Z, Zhao H (2009) Improving cellular malonyl-CoA level in Escherichia coli via metabolic engineering. Metab Eng 11(3):192–198.  https://doi.org/10.1016/j.ymben.2009.01.005 Google Scholar
  133. Zhang H, Stephanopoulos G (2013) Engineering Escherichia coli for caffeic acid biosynthesis from renewable sugars. Appl Microbiol Biotechnol 97(8):3333–3341.  https://doi.org/10.1007/s00253-012-4544-8 Google Scholar
  134. Zhang E, Guo X, Meng Z, Wang J, Sun J, Yao X, Xun H (2015) Construction, expression, and characterization of Arabidopsis thaliana 4-CL and Arachis hypogaea RS fusion gene 4-CL:: RS in Escherichia coli. World J Microbiol Biotechnol 31(9):1379–1385.  https://doi.org/10.1007/s11274-015-1889-z Google Scholar
  135. Zhang Y, Li SZ, Li J, Pan X, Cahoon RE, Jaworski JG, Wang X, Jez JM, Chen F, Yu O (2006) Using unnatural protein fusions to engineer resveratrol biosynthesis in yeast and mammalian cells. J Am Chem Soc 128:13030–13031Google Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Life Science and Biochemical EngineeringSun Moon UniversityAsan-siRepublic of Korea
  2. 2.Department of Pharmaceutical Engineering and BiotechnologySun Moon UniversityAsan-siRepublic of Korea

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