Systems metabolic engineering of Escherichia coli for production of the antitumor drugs violacein and deoxyviolacein

Metabolic Engineering

Volumn 20, Issue , 2013, Pages 29-41

  Rodrigues, André L ^a   Trachtmann, Nathalie ^b   Becker, Judith ^a   Lohanatha, Ananta F ^a   Blotenberg, Jana ^a   Bolten, Christoph J ^a   Korneli, Claudia ^a   de Souza Lima, André O ^c   Porto, Luismar M ^d   Sprenger, Georg A ^b   Wittmann, Christoph ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b UNIVERSITY OF STUTTGART   (Germany)

^c UNIVERSIDADE DO VALE DO ITAJAÍ   (Brazil)

^d FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Chorismate; Chromobacterium violaceum; Fed batch; Janthinobacterium lividum; Pathway deregulation; Tryptophan

Indexed keywords

AMINO ACIDS; BATCH DATA PROCESSING; BIOCHEMISTRY; METABOLIC ENGINEERING; VIRUSES;

CHORISMATE; CHROMOBACTERIUM VIOLACEUM; FED BATCHES; JANTHINOBACTERIUM LIVIDUM; TRYPTOPHAN;

ESCHERICHIA COLI;

ANTINEOPLASTIC AGENT; CHAPERONE; CHORISMIC ACID; DEOXYVIOLACEIN; SERINE; TRYPTOPHAN; UNCLASSIFIED DRUG; VIOLACEIN;

AMINO ACID ANALYSIS; ARTICLE; BACTERIAL STRAIN; BATCH PROCESS; BIOSYNTHESIS; BIOTECHNOLOGY; CHROMOBACTERIUM VIOLACEUM; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTALLIZATION; DEGRADATION; DRUG MANUFACTURE; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLIC ENGINEERING; METABOLITE; NEGATIVE FEEDBACK; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

CHROMOBACTERIUM VIOLACEUM; ESCHERICHIA COLI; JANTHINOBACTERIUM LIVIDUM;

CHORISMATE; CHROMOBACTERIUM VIOLACEUM; FED-BATCH; JANTHINOBACTERIUM LIVIDUM; PATHWAY DEREGULATION; TRYPTOPHAN;

ANTINEOPLASTIC AGENTS; CHROMOBACTERIUM; ESCHERICHIA COLI; GENES, BACTERIAL; INDOLES; METABOLIC ENGINEERING; MULTIGENE FAMILY;

EID: 84884166429     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2013.08.004     Document Type: Article

References (65)

1. Ahmetagic A., Pemberton J.M. Stable high level expression of the violacein indolocarbazole anti-tumour gene cluster and the Streptomyces lividans amyA gene in E. coli K12. Plasmid 2010, 63:79-85.
2. 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 2010, 330:70-74.
3. AlZaid Siddiquee K., Arauzo-Bravo M.J., Shimizu K. Metabolic flux analysis of pykF gene knockout Escherichia coli based on 13 C-labeling experiments together with measurements of enzyme activities and intracellular metabolite concentrations. Appl. Microbiol. Biotechnol 2004, 63:407-417.
4. Albermann C., Trachtmann N., Sprenger G.A. A simple and reliable method to conduct and monitor expression cassette integration into the Escherichia coli chromosome. Biotechnol. J 2010, 5:32-38.
5. Asamizu S., Kato Y., Igarashi Y., Onaka H. VioE, a prodeoxyviolacein synthase involved in violacein biosynthesis, is responsible for intramolecular indole rearrangement. Tetrahedron Lett. 2007, 48:2923-2926.
6. August P.R., Grossman T.H., Minor C., Draper M.P., MacNeil I.A., Pemberton J.M., Call K.M., Holt D., Osburne M.S. Sequence analysis and functional characterization of the violacein biosynthetic pathway from Chromobacterium violaceum. J. Mol. Microbiol. Biotechnol. 2000, 2:513-519.
7. Balderas-Hernández V.E., Sabido-Ramos A., Silva P., Cabrera-Valladares N., Hernández-Chávez G., Báez-Viveros J.L., Martínez A., Bolívar F., Gosset G. Metabolic engineering for improving anthranilate synthesis from glucose in Escherichia coli. Microb. Cell Fact. 2009, 8:19.
8. Balibar C.J., Walsh C.T. In vitro biosynthesis of violacein from l-tryptophan by the enzymes VioA-E from Chromobacterium violaceum. Biochemistry 2006, 45:15444-15457.
9. Becker J., Klopprogge C., Schröder H., Wittmann C. Metabolic engineering of the tricarboxylic acid cycle for improved lysine production by Corynebacterium glutamicum. Appl. Environ. Microbiol. 2009, 75:7866-7869.
10. Becker J., Wittmann C. Systems and synthetic metabolic engineering for amino acid production-the heartbeat of industrial strain development. Curr. Opin. Biotechnol 2012, 23:718-726.
11. Bolten C.J., Kiefer P., Letisse F., Portais J.C., Wittmann C. Sampling for metabolome analysis of microorganisms. Anal. Chem. 2007, 79:3843-3849.
12. Buschke N., Schröder H., Wittmann C. Metabolic engineering of Corynebacterium glutamicum for production of 1,5-diaminopentane from hemicellulose. Biotechnol. J 2011, 6:306-317.
13. Caligiuri M.G., Bauerle R. Identification of amino acid residues involved in feedback regulation of the anthranilate synthase complex from Salmonella typhimurium. Evidence for an amino-terminal regulatory site. J. Biol. Chem 1991, 266:8328-8335.
14. Cherepanov P.P., Wackernagel W. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 1995, 158:9-14.
15. Datsenko K.A., Wanner B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Nat. Acad. Sci. U.S.A. 2000, 97:6640-6645.
16. de Vasconcelos A.T.R., de Almeida D.F., Hungria M., Guimaraes C.T., Antônio R.V., Almeida F.C., de Almeida L.G.P., de Almeida R., Alves-Gomes J.A., Andrade E.M. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc. Nat. Acad. Sci. U.S.A. 2003, 100:11660-11665.
17. Durán M., Ponezi A.N., Faljoni-Alario A., Teixeira M.F.S., Justo G.Z., Durán N. Potential applications of violacein: a microbial pigment. Med. Chem. Res. 2012, 21:1524-1532.
18. Durán N., Justo G.Z., Ferreira C.V., Melo P.S., Cordi L., Martins D. Violacein: properties and biological activities. Biotechnol. Appl. Biochem. 2007, 48:127-134.
19. Ferreira C.V., Bos C.L., Versteeg H.H., Justo G.Z., Durán N., Peppelenbosch M.P. Molecular mechanism of violacein-mediated human leukemia cell death. Blood 2004, 104:1459-1464.
20. Gu P., Yang F., Kang J., Wang Q., Qi Q. One-step of tryptophan attenuator inactivation and promoter swapping to improve the production of l-tryptophan in Escherichia coli. Microb. Cell Fact. 2012, 11:30.
21. Henkin T.M., Yanofsky C. Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. BioEssays 2002, 24:700-707.
22. Howard-Jones A.R., Walsh C.T. Staurosporine and rebeccamycin aglycones are assembled by the oxidative action of StaP, StaC, and RebC on chromopyrrolic acid. J. Am. Chem. Soc. 2006, 128:12289-12298.
23. Ikeda M. Towards bacterial strains overproducing l-tryptophan and other aromatics by metabolic engineering. Appl. Microbiol. Biotechnol 2006, 69:615-626.
24. Jensen K.F. The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J. Bacteriol 1993, 175:3401-3407.
25. Jiang P., Wang H., Xiao S., Fang M., Zhang R., He S., Lou K., Xing X.H. Pathway redesign for deoxyviolacein biosynthesis in Citrobacter freundii and characterization of this pigment. Appl. Microbiol. Biotechnol. 2012, 94:1521-1532.
26. Jiang P., Wang H., Zhang C., Lou K., Xing X.H. Reconstruction of the violacein biosynthetic pathway from Duganella sp. B2 in different heterologous hosts. Appl. Microbiol. Biotechnol. 2010, 86:1077-1088.
27. Kimmel K.E., Maier S. Effect of cultural conditions on the synthesis of violacein in mesophilic and psychrophilic strains of Chromobacterium. Can. J. Microbiol. 1969, 15:111-116.
28. Kodach L.L., Bos C.L., Durán N., Peppelenbosch M.P., Ferreira C.V., Hardwick J.C.H. Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis 2006, 27:508-516.
29. Korneli C., David F., Biedendieck R., Jahn D., Wittmann C. Getting the big beast to work-systems biotechnology of Bacillus megaterium for novel high-value proteins. J. Biotechnol. 2013, 163:87-96.
30. Krömer J.O., Fritz M., Heinzle E., Wittmann C. In vivo quantification of intracellular amino acids and intermediates of the methionine pathway in Corynebacterium glutamicum. Anal. Biochem. 2005, 340:171-173.
31. Krömer J.O., Heinzle E., Schröder H., Wittmann C. Accumulation of homolanthionine and activation of a novel pathway for isoleucine biosynthesis in Corynebacterium glutamicum McbR deletion strains. J. Bacteriol 2006, 188:609-618.
32. Landick R., Carey J., Yanofsky C. Translation activates the paused transcription complex and restores transcription of the trp operon leader region. Proc. Nat. Acad. Sci. U.S.A. 1985, 82:4663-4667.
33. Lee N., Francklyn C., Hamilton E.P. Arabinose-induced binding of AraC protein to araI2 activates the araBAD operon promoter. Proc. Nat. Acad. Sci. U.S.A. 1987, 84:8814-8818.
34. Li Y., Chen G.K., Tong X.W., Zhang H.T., Liu X.G., Liu Y.H., Lu F.P. Construction of Escherichia coli strains producing l-serine from glucose. Biotechnol. Lett. 2012, 34:1525-1530.
35. Maier, T., Flinspach, R., 2005. European Patent Application 1496111A2.
36. May, G., Brummer, B., Ott, H., 1991. Treatment of Prophylaxis of Polio and Herpes Virus Infections-Comprises Admin. of 3-(1,2-dihydro-5-(5-hydroxy-1H-indol-3-yl)-2-oxo-3Hpyrrole-3-ylidene)-1,3-dihydro-2H-indol-2-one. German patent, DE 3935066.
37. McClean K.H., Winson M.K., Fish L., Taylor A., Chhabra S.R., Camara M., Daykin M., Lamb J.H., Swift S., Bycroft B.W., Stewart G.S.A.B., Williams P. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997, 143:3703-3711.
38. Mendes A.S., de Carvalho J.E., Duarte M.C.T., Durán N., Bruns R.E. Factorial design and response surface optimization of crude violacein for Chromobacterium violaceum production. Biotechnol. Lett. 2001, 23:1963-1969.
39. Nakamura Y., Asada C., Sawada T. Production of antibacterial violet pigment by psychrotropic bacterium RT102 strain. Biotechnol. Bioprocess Eng. 2003, 8:37-40.
40. Olano C., Lombó F., Méndez C., Salas J.A. Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab. Eng. 2008, 10:281-292.
41. Park J.H., Lee K.H., Kim T.Y., Lee S.Y. Metabolic engineering of Escherichia coli for the production of l-valine based on transcriptome analysis and in silico gene knockout simulation. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:7797-7802.
42. Patjanasoontorn B., Boonma P., Wilailackana C., Sittikesorn J. Hospital acquired Janthinobacterium lividum septicemia in Srinagarind hospital. J. Med. Assoc. Thail 1992, 75:6-10.
43. Pemberton J.M., Vincent K.M., Penfold R.J. Cloning and heterologous expression of the violacein biosynthesis gene cluster from Chromobacterium violaceum. Curr. Microbiol. 1991, 22:355-358.
44. Rodrigues A.L., Göcke Y., Bolten C.J., Brock N.L., Dickschat J.S., Wittmann C. Microbial production of the drugs violacein and deoxyviolacein-analytical development and strain comparison. Biotechnol. Lett. 2012, 34:717-720.
45. Rüffer N., Heidersdorf U., Kretzers I., Sprenger G.A., Raeven L., Takors R. Fully integrated l-phenylalanine separation and concentration using reactive-extraction with liquid-liquid centrifuges in a fed-batch process with E. coli. Bioprocess Biosyst. Eng. 2004, 26:239-248.
46. Saïda F., Uzan M., Odaert B., Bontems F. Expression of highly toxic genes in E. coli: special strategies and genetic tools. Curr. Protein Pept. Sci. 2006, 7:47-56.
47. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York.
48. Sánchez C., Braña A.F., Méndez C., Salas J.A. Reevaluation of the violacein biosynthetic pathway and its relationship to indolocarbazole biosynthesis. ChemBioChem 2006, 7:1231-1240.
49. Sawada K., Zen-In S., Wada M., Yokota A. Metabolic changes in a pyruvate kinase gene deletion mutant of Corynebacterium glutamicum ATCC 13032. Metab. Eng. 2010, 12:401-407.
50. Shinoda K., Hasegawa T., Sato H., Shinozaki M., Kuramoto H., Takamiya Y., Sato T., Nikaidou N., Watanabe T., Hoshino T. Biosynthesis of violacein: a genuine intermediate, protoviolaceinic acid, produced by VioABDE, and insight into VioC function. Chem. Commun. 2007, 2007:4140-4142.
51. Shirata A., Tsukamoto T., Yasui H., Hata T., Hayasaka S., Kojima A., Kato H. Isolation of bacteria producing bluish-purple pigment and use for dyeing. Jpn. Agric. Res. Q. 2000, 34:131-140.
52. Sprenger G.A. Genetics of pentose-phosphate pathway enzymes of Escherichia coli K-12. Arch. Microbiol 1995, 164:324-330.
53. Sprenger G.A. Aromatic amino acids. Amino Acid Biosynthesis-Pathways, Regulation and Metabolic Engineering 2007, vol. 5:93-127. Springer, Berlin Heidelberg.
54. Sprenger G.A., Schörken U., Sprenger G., Sahm H. Transketolase A of Escherichia coli K12. Eur. J. Biochem. 1995, 230:525-532.
55. Thomason L.C., Costantino N., Court D.L. E. coli genome manipulation by P1 transduction. Curr. Protoc. Mol. Biol. 2007, 79. (1.17.1-1.17.8).
56. Ti T.Y., Tan W.C., Chong A.P.Y., Lee E.H. Nonfatal and fatal infections caused by Chromobacterium violaceum. Clin. Infect. Dis. 1993, 17:505-507.
57. Tyo K.E.J., Kocharin K., Nielsen J. Toward design-based engineering of industrial microbes. Curr. Opin. Microbiol. 2010, 13:255-262.
58. Wang H., Jiang P., Lu Y., Ruan Z., Jiang R., Xing X.H., Lou K., Wei D. Optimization of culture conditions for violacein production by a new strain of Duganella sp. B2. Biochem. Eng. J. 2009, 44:119-124.
59. 2 in shake-flasks. Biotechnol. Lett. 2003, 25:377-380.
60. Wrede F., Rothhaas A. Über das Violacein, den violetten Farbstoff des Bacillus violaceus. I. Hoppe-Seyler's Z. Physiol. Chem. 1933, 233:113-118.
61. Yang C., Jiang P., Xiao S., Zhang C., Lou K., Xing X.H. Fed-batch fermentation of recombinant Citrobacter freundii with expression of a violacein-synthesizing gene cluster for efficient violacein production from glycerol. Biochem. Eng. J. 2011, 57:55-62.
62. Yang L.H., Xiong H., Lee O.O., Qi S.H., Qian P.Y. Effect of agitation on violacein production in Pseudoalteromonas luteoviolacea isolated from a marine sponge. Lett. Appl. Microbiol. 2007, 44:625-630.
63. Yee L., Blanch H.W. Recombinant protein expression in high cell density fed-batch cultures of Escherichia coli. Nat. Biotechnol. 1992, 10:1550-1556.
64. Zhang W., Li F., Nie L. Integrating multiple 'omics' analysis for microbial biology: application and methodologies. Microbiology 2010, 156:287-301.
65. Zhang Y., Shang X., Lai S., Zhang G., Liang Y., Wen T. Development and application of an arabinose-inducible expression system by facilitating inducer uptake in Corynebacterium glutamicum. Appl. Environ. Microbiol. 2012, 78:5831-5838.