Microbial production of indolylglucosinolate through engineering of a multi-gene pathway in a versatile yeast expression platform

Metabolic Engineering

Volumn 14, Issue 2, 2012, Pages 104-111

  Mikkelsen, Michael Dalgaard ^a   Buron, Line Due ^b   Salomonsen, Bo ^a   Olsen, Carl Erik ^a   Hansen, Bjarne Gram ^b   Mortensen, Uffe Hasbro ^b   Halkier, Barbara Ann ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Biosynthetic pathway; Glucosinolates; Natural products; Pathway engineering; Yeast expression platform

Indexed keywords

ARABIDOPSIS THALIANA; BIOSYNTHETIC PATHWAY; CRUCIFEROUS PLANTS; EPIDEMIOLOGICAL STUDIES; GLUCOSINOLATES; HUMAN HEALTH; MICROBIAL CELLS; MICROBIAL PRODUCTION; NATURAL PRODUCTS; PROOF OF CONCEPT; STABLE EXPRESSION; YEAST EXPRESSION; YEAST EXPRESSION PLATFORM;

GENE EXPRESSION; HEALTH RISKS; PLANTS (BOTANY);

YEAST;

GLUCOSINOLATE; INDOLYLGLUCOSINOLATE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; FUNGAL CELL; FUNGAL STRAIN; GENE EXPRESSION; GENE TARGETING; HOST; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICA; GLUCOSINOLATES; HUMANS; METABOLIC ENGINEERING; NEOPLASMS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS THALIANA; BRASSICA OLERACEA VAR. ITALICA; SACCHAROMYCES CEREVISIAE;

EID: 84857995434     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2012.01.006     Document Type: Article

References (44)

1. Asadollahi M.A., Maury J., Møller K., Nielsen K.F., Schalk M., Clark A., Nielsen J. Production of plant sesquiterpenes in Saccharomyces cerevisiae: effect of ERG9 repression on sesquiterpene biosynthesis. Biotechnol. Bioeng. 2008, 99:666-677.
2. Becker J.V.W., Armstrong G., Merwe M., Lambrechts M., Vivier M., Pretorius I. Metabolic engineering of Saccharomyces cerevisiae for the synthesis of the wine-related antioxidant resveratrol. FEMS Yeast Res. 2003, 4:79-85.
3. Brew C., Aronchik I., Hsu J., Sheen J., Dickson R., Bjeldanes L., Firestone G. Indole-3-carbinol activates the ATM signaling pathway independent of DNA damage to stabilize p53 and induce G1 arrest of human mammary epithelial cells. Int. J. Cancer 2006, 118:857-868.
4. De Jong J., Liu Y., Bollon A., Long R., Jennewein S., Williams D., Croteau R. Genetic engineering of taxol biosynthetic genes in Saccharomyces cerevisiae. Biotechnol. Bioeng. 2006, 93.
5. Engels B., Dahm P., Jennewein S. Metabolic engineering of taxadiene biosynthesis in yeast as a first step towards Taxol (Paclitaxel) production. Metab. Eng. 2008, 10:201-206.
6. Fahey J., Zalcmann A., Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001, 56:5-51.
7. Farhi M., Marhevka E., Masci T., Marcos E., Eyal Y., Ovadis M., Abeliovich H., Vainstein A. Harnessing yeast subcellular compartments for the production of plant terpenoids. Metab. Eng. 2011, 13:474-481.
8. Flagfeldt D., Siewers V., Huang L., Nielsen J. Characterization of chromosomal integration sites for heterologous gene expression in Saccharomyces cerevisiae. Yeast 2009, 26:545-551.
9. Geu-Flores F., Møldrup M., Böttcher C., Olsen C., Scheel D., Halkier B. Cytosolic gamma-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell 2011, 23:2456-2469.
10. Geu-Flores F., Nielsen M., Nafisi M., Møldrup M., Olsen C., Motawia M., Halkier B. Glucosinolate engineering identifies a gamma-glutamyl peptidase. Nat. Chem. Biol. 2009, 5:575-577.
11. Geu-Flores F., Nour-Eldin H., Nielsen M., Halkier B. USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res. 2007, 35:e55. 10.1093/nar/gkm106.
12. Gietz R., Schiestl R. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2007, 2:31-34.
13. Halkier B., Gershenzon J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 2006, 57:303-333.
14. Hansen B., Kliebenstein D., Halkier B. Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 2007, 50:902-910.
15. Hansen B., Salomonsen B., Nielsen M., Nielsen J., Hansen N., Nielsen K., Regueira T., Nielsen J., Patil K., Mortensen U. Versatile enzyme expression and characterization system for Aspergillus nidulans, with the Penicillium brevicompactum polyketide synthase gene from the mycophenolic acid gene cluster as a test case. Appl. Environ. Microbiol. 2011, 77:3044-3051.
16. Hansen E.H., Moller B.L., Kock G.R., Bunner C.M., Kristensen C., Jensen O.R., Okkels F.T., Olsen C.E., Motawia M.S., Hansen J. De novo biosynthesis of vanillin in fission yeast (Schizosaccharomyces pombe) and baker's yeast (Saccharomyces cerevisiae). Appl. Environ. Microbiol. 2009, 75:2765-2774.
17. Hayes J., Kelleher M., Eggleston I. The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur. J. Nutr. 2008, 47:73-88.
18. Howson R., Huh W., Ghaemmaghami S., Falvo J., Bower K., Belle A., Dephoure N., Wykoff D., Weissman J., O'Shea E. Construction, verification and experimental use of two epitope-tagged collections of budding yeast strains. Comp. Funct. Genom. 2005, 6:2-16.
19. Johnston M., Flick J., Pexton T. Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 1994, 14:3834-3841.
20. Kim D., Han B., Ahn B., Hasegawa R., Shirai T., Ito N., Tsuda H. Enhancement by indole-3-carbinol of liver and thyroid gland neoplastic development in a rat medium-term multiorgan carcinogenesis model. Carcinogenesis 1997, 18:377-381.
21. Lim C.G., Fowler Z., Hueller T., Schaffer S., Koffas M. High-yield resveratrol production in engineered Escherichia coli. Appl. Environ. Microbiol. 2011, 77:3451-3460.
22. McGrath D., Spigelman A. Putative mechanisms of action for indole-3-carbinol in the prevention of colorectal cancer. Expert Opin. Ther. Targets 2008, 12:729-738.
23. Mikkelsen M., Olsen C., Halkier B. Production of the cancer-preventive glucoraphanin in tobacco. Mol. Plant 2010, 3:751-759.
24. Miller J.H., Platt T., Müller-Hill B. Experiments in molecular genetics. In: Assay of Betagalactosidase 1977, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, (Chapter VII).
25. Møldrup M., Geu-Flores F., Olsen C., Halkier B. Modulation of sulfur metabolism enables efficient glucosinolate engineering. BMC Biotechnol. 2011, 11:12.
26. Nour-Eldin H., Geu-Flores F., Halkier B. USER cloning and USER fusion: the ideal cloning techniques for small and big laboratories. Methods Mol. Biol. 2010, 643:185-200.
27. Nour-Eldin H., Hansen B., Nørholm M., Jensen J., Halkier B. Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 2006, 34:E122.
28. Nørholm M.H.H. A mutant Pfu DNA polymerase designed for advanced uracil-excision DNA engineering. BMC Biotechnol. 2010, 10:21.
29. Pfalz M., Mikkelsen M., Bednarek P., Olsen C., Halkier B., Kroymann J. Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 2011, 23:716-729.
30. Rahman K., Aranha O., Sarkar F. Indole-3-carbinol (I3C) induces apoptosis in tumorigenic but not in nontumorigenic breast epithelial cells. Nutr. Cancer 2003, 45:101-112.
31. Ro D.K., Paradise E.M., Ouellet M., Fisher K.J., Newman K.L., Ndungu J.M., Ho K.A., Eachus R.A., Ham T.S., Kirby J., Chang M.C.Y., Withers S., Shiba Y., Sarpong R., Keasling J.D. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 2006, 440:940-943.
32. Shao Z., Zhao H., Zhao H. DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res. 2009, 37. e16 (10 pp.).
33. Sherman F., Fink G.R., Hicks J.B. Laboratory Course Manual for Methods in Yeast Genetics 1986, Cold Spring Harbor Laboratory, New York.
34. Shimamoto K., Dewa Y., Ishii Y., Kemmochi S., Taniai E., Hayashi H., Imaoka M., Morita R., Kuwata K., Suzuki K., Shibutania M., Mitsumori K. Indole-3-carbinol enhances oxidative stress responses resulting in the induction of preneoplastic liver cell lesions in partially hepatectomized rats initiated with diethylnitrosamine. Toxicology 2011, 283:109-117.
35. Shimamoto K., Dewa Y., Kemmochi S., Taniai E., Hayashi H., Imaoka M., Shibutani M., Mitsumori K. Relationship between CYP1A induction by indole-3-carbinol or flutamide and liver tumor-promoting potential in rats. Arch. Toxicol. 2011, 85:1159-1166.
36. Siewers V., Mortensen U., Nielsen J. Genetic engineering tools for Saccharomyces cerevisiae. Manual of Industrial Microbiology and Biotechnology 2010, 287-301. ASM Press, Washington, DC, USA. R. Baltz, J.E. Davies, A.L. Demain (Eds.).
37. Sønderby I., Geu-Flores F., Halkier B. Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci. 2010, 15:283-290.
38. Traka M., Mithen R. Glucosinolates, isothiocyanates and human health. Phytochem. Rev. 2009, 8:269-282.
39. Urban P., Mignotte C., Kazmaier M., Delorme F., Pompon D. Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J. Biol. Chem. 1997, 272:19176-19186.
40. Verkerk R., Schreiner M., Krumbein A., Ciska E., Holst B., Rowland I., De Schrijver R., Hansen M., Gerhauser C., Mithen R., Dekker M. Glucosinolates in Brassica vegetables: the influence of the food supply chain on intake, bioavailability and human health. Mol. Nutr. Food Res. 2009, 53:S219-S265.
41. Walter W., Schaumann E. The chemistry of thiohydroxamic acids. Int. J. Methods Synth. Org. Chem. 1971, 111-130.
42. Wang T., Schoene N., Milner J., Kim Y. Broccoli-derived phytochemicals indole-3-carbinol and 3,3'-diindolylmethane exerts concentration-dependent pleiotropic effects on prostate cancer cells: comparison with other cancer preventive phytochemicals. Mol. Carcinog. 2012, 51:244-256.
43. Wang Y., Halls C., Zhang J., Matsuno M., Zhang Y., Yu O. Stepwise increase of resveratrol biosynthesis in yeast Saccharomyces cerevisiae by metabolic engineering. Metab. Eng. 2011, 11:310-318.
44. Yan Y., Kohli A., Koffas M. Biosynthesis of natural flavanones in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2005, 71:5610-5613.