Metabolic engineering of Escherichia coli for the production of indirubin from glucose

Journal of Biotechnology

Volumn 267, Issue , 2018, Pages 19-28

  Du, Jikun ^a   Yang, Dongsoo ^a   Luo, Zi Wei ^a   Lee, Sang Yup ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Escherichia coli; Indigo; Indirubin; Metabolic engineering; Synthetic biology

Indexed keywords

AMINO ACIDS; AROMATIZATION; DIAGNOSIS; ENZYMES; ESCHERICHIA COLI; GENE ENCODING; GLUCOSE; METABOLISM; NEURODEGENERATIVE DISEASES; POLYCYCLIC AROMATIC HYDROCARBONS; SUBSTRATES;

COMBINATORIAL APPROACH; ENGINEERED ESCHERICHIA COLI; FED-BATCH FERMENTATION; FERMENTATIVE PRODUCTION; FLAVIN CONTAINING MONOOXYGENASE; INDIGO; INDIRUBIN; SYNTHETIC BIOLOGY;

METABOLIC ENGINEERING;

AROMATIC AMINO ACID; DIMETHYLANILINE MONOOXYGENASE; GLUCOSE; INDIRUBIN; PHOSPHATE; PHOSPHOENOLPYRUVATE; TRYPTOPHAN; TRYPTOPHANASE; BACTERIAL PROTEIN; DIMETHYLANILINE MONOOXYGENASE (N-OXIDE FORMING); INDOLE DERIVATIVE; OXYGENASE; PYRUVATE KINASE; REPRESSOR PROTEIN; TRANSKETOLASE; TRPR PROTEIN, E COLI;

ARTICLE; BIOSYNTHESIS; ESCHERICHIA COLI; FED BATCH FERMENTATION; METABOLIC ENGINEERING; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; REPRESSOR GENE; SYNTHETIC BIOLOGY; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; PISCIRICKETTSIACEAE; PROCEDURES;

BACTERIAL PROTEINS; ESCHERICHIA COLI; GLUCOSE; INDOLES; METABOLIC ENGINEERING; OXYGENASES; PHOSPHOENOLPYRUVATE; PISCIRICKETTSIACEAE; PYRUVATE KINASE; REPRESSOR PROTEINS; SUBSTRATE SPECIFICITY; TRANSKETOLASE; TRYPTOPHANASE;

EID: 85040024093     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2017.12.026     Document Type: Article

References (46)

1. Ajikumar, P.K., Xiao, W.H., Tyo, K.E.J., Wang, Y., Simeon, F., Leonard, E., Mucha, O., Phon, T.H., Pfeifer, B., Stephanopoulos, G., Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330 (2010), 70–74.
2. Ameria, S.P.L., Jung, H.S., Kim, H.S., Han, S.S., Kim, H.S., Lee, J.H., Characterization of a flavin-containing monooxygenase from Corynebacterium glutamicum and its application to production of indigo and indirubin. Biotechnol. Lett. 37 (2015), 1637–1644.
3. Berry, A., Dodge, T.C., Pepsin, M., Weyler, W., Application of metabolic engineering to improve both the production and use of biotech indigo. J. Ind. Microbiol. Biotechnol. 28 (2002), 127–133.
4. Bongaerts, J., Kramer, M., Muller, U., Raeven, L., Wubbolts, M., Metabolic engineering for microbial production of aromatic amino acids and derived compounds. Metab. Eng. 3 (2001), 289–300.
5. Brown, S., Clastre, M., Courdavault, V., O'Connor, S.E., De novo production of the plant-derived alkaloid strictosidine in yeast. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3205–3210.
6. Chemler, J.A., Koffas, M.A.G., Metabolic engineering for plant natural product biosynthesis in microbes. Curr. Opin. Biotechnol. 19 (2008), 597–605.
7. Datsenko, K.A., Wanner, B.L., One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97 (2000), 6640–6645.
8. De Luca, V., Salim, V., Levac, D., Atsumi, S.M., Yu, F., Discovery and functional analysis of monoterpenoid indole alkaloid pathways in plants. Methods Enzymol. 515 (2012), 207–229.
9. De Luca, V., Salim, V., Thamm, A., Masada, S.A., Yu, F., Making iridoids/secoiridoids and monoterpenoid indole alkaloids: progress on pathway elucidation. Curr. Opin. Plant. Biol. 19 (2014), 35–42.
10. Fang, M.Y., Wang, T.M., Zhang, C., Bai, J.L., Zheng, X., Zhao, X.J., Lou, C.B., Xing, X.H., Intermediate-sensor assisted push-pull strategy and its application in heterologous deoxyviolacein production in Escherichia coli. Metab. Eng. 33 (2016), 41–51.
11. Fossati, E., Ekins, A., Narcross, L., Zhu, Y., Falgueyret, J.P., Beaudoin, G.A.W., Facchini, P.J., Martin, V.J.J., Reconstitution of a 10-gene pathway for synthesis of the plant alkaloid dihydrosanguinarine in Saccharomyces cerevisiae. Nat. Commun., 5, 2014, 3283.
12. Galanie, S., Thodey, K., Trenchard, I.J., Interrante, M.F., Smolke, C.D., Complete biosynthesis of opioids in yeast. Science 349 (2015), 1095–1100.
13. Gosset, G., Production of aromatic compounds in bacteria. Curr. Opin. Biotechnol. 20 (2009), 651–658.
14. Gu, P.F., Yang, F., Kang, J.H., Wang, Q., Qi, Q.S., One-step of tryptophan attenuator inactivation and promoter swapping to improve the production of L-tryptophan in Escherichia coli. Microb. Cell Fact., 11, 2012, 30.
15. Han, G.H., Gim, G.H., Kim, W., Seo, S.I., Kim, S.W., Enhanced indirubin production in recombinant Escherichia coli harboring a flavin-containing monooxygenase gene by cysteine supplementation. J. Biotechnol. 164 (2013), 179–187.
16. Hoessel, R., Leclerc, S., Endicott, J.A., Nobel, M.E.M., Lawrie, A., Tunnah, P., Leost, M., Damiens, E., Marie, D., Marko, D., Niederberger, E., Tang, W.C., Eisenbrand, G., Meijer, L., Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1 (1999), 60–67.
17. Ikeda, M., Towards bacterial strains overproducing L-tryptophan and other aromatics by metabolic engineering. Appl. Microbiol. Biotechnol. 69 (2006), 615–626.
18. Keasling, J.D., Manufacturing molecules through metabolic engineering. Science 330 (2010), 1355–1358.
19. Kim, B., Park, H., Na, D., Lee, S.Y., Metabolic engineering of Escherichia coli for the production of phenol from glucose. Biotechnol. J. 9 (2014), 621–629.
20. Lee, K.H., Park, J.H., Kim, T.Y., Kim, H.U., Lee, S.Y., Systems metabolic engineering of Escherichia coli for L-threonine production. Mol. Syst. Biol., 3, 2007, 149.
21. Lee, J.Y., Shin, Y.S., Shin, H.J., Kim, G.J., Production of natural indirubin from indican using non-recombinant Escherichia coli. Bioresour. Technol. 102 (2011), 9193–9198.
22. Lee, S.Y., High cell-density culture of Escherichia coli. Trends Biotechnol. 14 (1996), 98–105.
23. Lu, J.L., Liao, J.C., Metabolic engineering and control analysis for production of aromatics: role of transaldolase. Biotechnol. Bioeng. 53 (1997), 132–138.
24. Luetke-Eversloh, T., Stephanopoulos, G., Combinatorial pathway analysis for improved L-tyrosine production in Escherichia coli: identification of enzymatic bottlenecks by systematic gene overexpression. Metab. Eng. 10 (2008), 69–77.
25. Luo, Z.W., Lee, S.Y., Biotransformation of p-xylene into terephthalic acid by engineered Escherichia coli. Nat. Commun., 8, 2017, 15689.
26. Lutke-Eversloh, T., Stephanopoulos, G., L-tyrosine production by deregulated strains of Escherichia coli. Appl. Microbiol. Biotechnol. 75 (2007), 103–110.
27. Meyer, A., Wursten, M., Schmid, A., Kohler, H.P.E., Witholt, B., Hydroxylation of indole by laboratory-evolved 2-hydroxybiphenyl 3-monooxygenase. J. Biol. Chem. 277 (2002), 34161–34167.
28. Murdock, D., Ensley, B.D., Serdar, C., Thalen, M., Construction of metabolic operons catalyzing the de novo biosynthesis of indigo in Escherichia coli. Nat. Biotechnol. 11 (1993), 381–386.
29. Nam, S., Buettner, R., Turkson, J., Kim, D., Cheng, J.Q., Muehlbeyer, S., Hippe, F., Vatter, S., Merz, K.H., Eisenbrand, G., Jove, R., Indirubin derivatives inhibit Stat3 signaling and induce apoptosis in human cancer cells. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 5998–6003.
30. Noda, S., Shirai, T., Oyama, S., Kondo, A., Metabolic design of a platform Escherichia coli strain producing various chorismate derivatives. Metab. Eng. 33 (2016), 119–129.
31. O'Connor, S.E., Maresh, J.J., Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat. Prod. Rep. 23 (2006), 532–547.
32. Palmeros, B., Wild, J., Szybalski, W., Le Borgne, S., Hernandez-Chavez, G., Gosset, G., Valle, F., Bolivar, F., Family of removable cassettes designed to obtain antibiotic-resistance-free genomic modifications of Escherichia coli and other bacteria. Gene 247 (2000), 255–264.
33. Patnaik, R., Liao, J.C., Engineering of Escherichia coli central metabolism for aromatic metabolite production with near theoretical yield. Appl. Environ. Microbiol. 60 (1994), 3903–3908.
34. Pickens, L.B., Tang, Y., Chooi, Y.H., Metabolic engineering for the production of natural products. Annu. Rev. Chem. Biomol. 2 (2011), 211–236.
35. 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.T., Shiba, Y., Sarpong, R., Keasling, J.D., Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440 (2006), 940–943.
36. Rodrigues, A.L., Trachtmann, N., Becker, J., Lohanatha, A.F., Blotenberg, J., Bolten, C.J., Korneli, C., Lima, A.O.D., Porto, L.M., Sprenger, G.A., Wittmann, C., Systems metabolic engineering of Escherichia coli for production of the antitumor drugs violacein and deoxyviolacein. Metab. Eng. 20 (2013), 29–41.
37. Rodriguez, A., Kildegaard, K.R., Li, M.J., Borodina, I., Nielsen, J., Establishment of a yeast platform strain for production of p-coumaric acid through metabolic engineering of aromatic amino acid biosynthesis. Metab. Eng. 31 (2015), 181–188.
38. Rui, L.Y., Reardon, K.F., Wood, T.K., Protein engineering of toluene ortho-monooxygenase of Burkholderia cepacia G4 for regiospecific hydroxylation of indole to form various indigoid compounds. Appl. Microbiol. Biotechnol. 66 (2005), 422–429.
39. Seldes, A.M., Burucua, J.E., Maier, M.S., Abad, G., Jauregui, A., Siracusano, G., Blue pigments in South American painting (1610–1780). J. Am. Inst. Conserv. 38 (1999), 100–123.
40. Song, C.W., Lee, S.Y., Rapid one-step inactivation of single or multiple genes in Escherichia coli. Biotechnol. J. 8 (2013), 776–784.
41. Trenchard, I.J., Smolke, C.D., Engineering strategies for the fermentative production of plant alkaloids in yeast. Metab. Eng. 30 (2015), 96–104.
42. Wang, L., Zhou, G.B., Liu, P., Song, J.H., Liang, Y., Yan, X.J., Xu, F., Wang, B.S., Mao, J.H., Shen, Z.X., Chen, S.J., Chen, Z., Dissection of mechanisms of Chinese medicinal formula Realgar-Indigo naturalis as an effective treatment for promyelocytic leukemia. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 4826–4831.
43. Wang, J., Cheng, L.K., Wang, J., Liu, Q., Shen, T., Chen, N., Genetic engineering of Escherichia coli to enhance production of L-tryptophan. Appl. Microbiol. Biotechnol. 97 (2013), 7587–7596.
44. Wongsaroj, L., Sallabhan, R., Dubbs, J.M., Mongkolsuk, S., Loprasert, S., Cloning of toluene 4-monooxygenase genes and application of two-phase system to the production of the anticancer agent, indirubin. Mol. Biotechnol. 57 (2015), 720–726.
45. Zhang, X.W., Qu, Y.Y., Ma, Q., Kong, C.L., Zhou, H., Cao, X.Y., Shen, W.L., Shen, E., Zhou, J.T., Production of indirubin from tryptophan by recombinant Escherichia coli containing naphthalene dioxygenase genes from Comamonas sp. MQ. Appl. Biochem. Biotechnol. 172 (2014), 3194–3206.
46. Zhao, Z.J., Zou, C., Zhu, Y.X., Dai, J., Chen, S., Wu, D., Wu, J., Chen, J., Development of L-tryptophan production strains by defined genetic modification in Escherichia coli. J. Ind. Microbiol. Biotechnol. 38 (2011), 1921–1929.