Mutations of toluene-4-monooxygenase that alter regiospecificity of indole oxidation and lead to production of novel indigoid pigments

Applied and Environmental Microbiology

Volumn 71, Issue 9, 2005, Pages 5476-5483

  McClay, Kevin ^a   Boss, Corinne ^a   Keresztes, Ivan ^b   Steffan, Robert J ^a,c  

^a Shaw Environmental Inc   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; DYES; NUCLEAR MAGNETIC RESONANCE; OXIDATION; PIGMENTS; SUBSTRATES; THIN LAYER CHROMATOGRAPHY;

INDOLE OXIDATION; PHENOTYPIC DIFFERENCES;

ENZYMES;

7 HYDROXYINDOLE; AMINO ACID; INDIRUBIN; INDOLE; INDOXYL; ISATIN; OXINDOLE; PIGMENT; TOLUENE 4 MONOOXYGENASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

MUTATION;

ARTICLE; BURKHOLDERIA CEPACIA; CATALYSIS; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME MODIFICATION; INDIGO; LIQUID CHROMATOGRAPHY; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION; PHENOTYPE; POLYMERIZATION; SITE DIRECTED MUTAGENESIS; THIN LAYER CHROMATOGRAPHY;

BINDING SITES; CATALYTIC DOMAIN; ESCHERICHIA COLI; INDOLES; MUTATION; OXIDATION-REDUCTION; OXYGENASES; PIGMENTS, BIOLOGICAL; PROTEIN ENGINEERING; PROTEIN ISOFORMS;

BURKHOLDERIA CEPACIA;

EID: 25144476090     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.9.5476-5483.2005     Document Type: Article

References (44)

1. Berry, A., T. C. Dodge, M. Pepsin, and W. Weyler. 2002. Application of metabolic engineering to improve both the production and use of biotech indigo. J. Ind. Microbiol. Biotechnol. 28:127-133.
2. Canada, K. A., S. Iwashita, H. Shim, and T. K. Wood. 2002. Directed evolution of toluene ortho-monooxygenase for enhanced 1-naphthol synthesis and chlorinated ethene degradation. J. Bacteriol. 184:344-349.
3. Choi, H. S., J. K. Kim, E. H. Cho, Y. C. Kim, J. I. Kim, and S. W. Kim. 2003. A novel flavin-containing monooxygenase from Methylophaga sp. strain SK1 and its indigo synthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 306:93093-93096.
4. Chunmei, Y., R. T. Watson, J. S. Elmendorf, D. B. Sacks, and J. E. Pessin. 2000. Calmodulin antagonists inhibit insulin-stimulated GLUT4 (glucose transporter 4) translocation by preventing the formation of phosphatidylinositol 3,4,5-trisphosphate in 3T3L1 adipocytes. Mol. Endocrinol. 14:317-326.
5. Colgan, S. T., G. R. Haggan, and R. H. Reed. 1996. Assay and purity evaluation of 5-chlorooxindole by liquid chromatography. J. Pharm. Biomed. Anal. 14:825-833.
6. Cotteret, J., J. Alex, R. Herve, and V. J. Jacques. July 2000. Method for dyeing keratin fibers with compositions which contain 6- or 7-hydroxyindole derivatives as couplers and oxidation dye precursors. U.S. patent 6,090,160.
7. Doukyu, N., K. Toyoda, and R. Aono. 2003. Indigo production by Escherichia coli carrying the phenol hydroxylase gene from Acinetobacter sp. strain ST-550 in a water-organic solvent two-phase system. Appl. Microbiol. Biotechnol. 60:720-725.
8. Drewlo, S., C. O. Bramer, M. Madkour, F. Mayer, and A. Steinbuchel. 2001. Cloning and expression of a Ralstonia eutropha HF39 gene mediating indigo formation in Escherichia coli. Appl. Environ. Microbiol. 67:1964-1969.
9. Eaton, R. W., and P. J. Chapman. 1995. Formation of indigo and related compounds from indolecarboxylic acids by aromatic acid-degrading bacteria: chromogenic reactions for cloning genes encoding dioxygenases that act on aromatic acids. J. Bacteriol. 177:6983-6988.
10. Ensley, B. D., B. J. Ratzki, T. D. Osslund, M. J. Simon, L. P. Wackett, and D. T. Gibson. 1983. Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222:167-169.
11. Furuya, T., S. Takahashi, Y. Ishii, K. Kino, and K. Kirimura. 2004. Cloning of a gene encoding flavin reductase coupling with dibenzothiophene monooxygenase through coexpression screening using indigo production as selective indication. Biochem. Biophys. Res. Commun. 313:570-575.
12. Gallagher, S. C., A. George, and H. Dalton. 1998. Sequence-alignment modeling and molecular docking studies of the epoxygenase component of alkene monooxygenase from Nocardia corallina B-276. Eur. J. Biochem. 254:480-489.
13. Gillam, E. M., L. M. Notley, H. Cai, J. J. De Voss, and F. P. Guengerich. 2000. Oxidation of indole by cytochrome P450 enzymes. Biochemistry 39:13817-13824.
14. Guengerich, F. P., F. Martin, M. V. McCormick, W. A. Nguyen, L. P. Glover, and E. Bradfield. 2004. Aryl hydrocarbon receptor response to indigoids in vitro and in vivo. Arch. Biochem. Biophys. 423:309-316.
15. Hareland, W. A., R. L. Crawford, P. J. Chapman, and S. Dagley. 1975. Metabolic function and properties of 4-hydroxyphenylacetic acid 1-hydroxylase from Pseudomonas acidovorans. J. Bacteriol. 121:272-285.
16. Hoessel, R., S. Leclerc, J. A. Endicott, M. E. Nobel, A. Lawrie, P. Tunnah, M. Leost, E. Damiens, D. Marie, D. Marko, E. Niederberger, W. Tang, G. Eisenbrand, and L. Meijer. 1999. Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1:60-67.
17. Hosoe, T., K. Nozawa, N. Kawahara, K. Fukushima, K. Nishimura, M. Miyaji, and K. Kawai. 1999. Isolation of a new potent cytotoxic pigment along with indigotin from the pathogenic basidiomycetous fungus Schizophyllum commune. Mycopathology 146:9-12.
18. Jensen, J. B., H. Egsgaard, H. Van Onckelen, and B. U. Jochimsen. 1995. Catabolism of indole-3-acetic acid and 4- and 5-chloroindole-3-acetic acid in Bradyrhizobium japonicum. J. Bacteriol. 177:5762-5766.
19. Kapadia, G. J., H. Tokuda, R. Sridhar, V. Balasubramanian, J. Takayasu, P. Bu, F. Enjo, M. Takasaki, T. Konoshima, and H. Nishino. 1998. Cancer chemopreventive activity of synthetic colorants used in foods, pharmaceuticals and cosmetic preparations. Cancer Lett. 129:87-95.
20. Keil, H., C. M. Saint, and P. A. Williams. 1987. Gene organization of the first catabolic operon of TOL plasmid pWW53: production of indigo by the xylA gene product. J. Bacteriol. 169:764-770.
21. Knockaert, M. M. Blondel, S. Bach, M. Leost, M. Elbi, C. Hager, G. L. Nagy, S. R. Han, D. Denison, M. Ffrench, M. Ryan, X. P. Magiatis, P. Polychronopoulos, P. Greengard, A. L. Skaltsounis, and L. Meijer. 2004. Independent actions on cyclin-dependent kinases and aryl hydrocarbon receptor mediate the antiproliferative effects of indirubins. Oncogene 23:4400-4412.
22. Kukor, J. J., R. H. Olsen, and J. S. Siak. 1989. Recruitment of a chromosomally encoded maleylacetate reductase for degradation of 2,4-dichlorophenoxyacetic acid by plasmid pJP4. J. Bacteriol. 17:3385-3390.
23. Kunikata, T., T. Tatefuji, H. Aga, K. Iwaki, M. Ikeda, and M. Kurimoto. 2000. Indirubin inhibits inflammatory reactions in delayed-type hypersensitivity. Eur. J. Pharmacol. 410:93-100.
24. Leclerc, S., M. Garnier, R. Hoessel, D. Marko, J. A. Bibb, G. L. Snyder, P. Greengard, J. Biernat, Y. Z. Wu, E. M. Mandelkow, G. Eisenbrand, and L. Meijer. 2001. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276:251-260.
25. Li, Q.-S., U. Schwaneberg, P. Fischer, and R. D. Schmid. 2000. Directed evolution of the fatty-acid hydroxylase P450 BM-3 into and indole-hydroxylating catalyst. Chem. Eur. J. 6:1531-1535.
26. McClay, K., B. G. Fox, and R. J. Steffan. 2000. Toluene monooxygenase-catalyzed epoxidation of alkenes. Appl. Environ. Microbiol. 66:1877-1882.
27. McGovern, S. L., and B. K. Shoichet. 2003. Kinase inhibitors: not just for kinases anymore. J. Med. Chem. 46:1478-1483.
28. Mitchell, K. H., J. M. Studts, and B. G. Fox. 2002. Combined participation of hydroxylase active site residues and effector protein binding in a para to ortho modulation of toluene 4-monooxygenase regiospecificity. Biochemistry 41:3176-3188.
29. Mitchell, K. H., C. E. Rogge, T. Gierahn, and B. G. Fox. 2003. Insight into the mechanism of aromatic hydroxylation by toluene 4-monooxygenase by use of specifically deuterated toluene and p-xylene. Proc. Natl. Acad. Sci. USA 100:3784-3789.
30. Murdock, D., B. D. Ensley, C. Serdar, and M. Thalen. 1993. Construction of metabolic operons catalyzing the de novo biosynthesis of indigo in Escherichia coli. Bio/Technology 11:381-386.
31. Nakamura, K., M. V. Martin, and F. P. Guengerich. 2001. Random mutagenesis of human cytochrome P450 2A6 and screening with indole oxidation products. Arch. Biochem. Biophys. 395:25-31.
32. Niederer, C., R. Behra, A. Harder, R. P. Schwarzenbach, and B. I. Escher. 2004. Mechanistic approaches for evaluating the toxicity of reactive organochlorines and epoxides in green algae. Environ. Toxicol. Chem. 23:697-704.
33. Nudoreku, R., B. Fuooboo, J. Amon, and K. Oberurande. September 1986. 7-Hydroxyindole derivatives, salts therof, use as drug, composition and intermediates. International patent JP61207383.
34. O'Connor, K. E., A. D. Dobson, and S. Hartmans. 1997. Indigo formation by microorganisms expressing styrene monooxygenase activity. Appl. Environ. Microbiol. 63:4287-4291.
35. Pikus, J. D., J. M. Studts, C. Achim, K. E. Kaufmann, E. Munck, R. J. Steffan, K. McClay, B. G. Fox. 1996. Recombinant toluene-4-monooxygenase: catalytic and Mossbauer studies of the purified diiron and rieske components of a four-protein complex. Biochemistry 35:9106-9119.
36. Pikus, J. D., J. M. Studts, K. McClay, and R. J. Steffan, and B. G. Fox. 1997. Changes in the regiospecificity of aromatic hydroxylation produced by active site engineering in the diiron enzyme toluene-4-monooxygenase. Biochemistry 36:9283-9289.
37. Polychronopoulos, P. P. Magiatis, A. L. Skaltsounis, V. Myrianthopoulos, E. Mikros, A. Tarricone, A. Musacchio, S. M. Roe, L. Pearl, M. Leost, P. Greengard, and L. Meijer. 2004. Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J. Med. Chem. 47:935-946.
38. Rui, L., K. F. Reardon, and T. K. Wood. 2005. Protein engineering of toluene ortho-monooxygenase of Burkholderia cepacia G4 for regiospecific hydroxylation of indole to form various indigoid compounds. Appl. Microbiol. Biotechnol. 66:422-429.
39. Shields, M. S., M. J. Reagin, R. R. Gerger, R. Campbell, and C. Somerville. 1995. TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4. Appl. Environ. Microbiol. 61:1352-1356.
40. Woo, H., J. Sanseverino, C. D. Cox, K. G. Robinson, and G. S. Sayler. 2000. The measurement of toluene dioxygenase activity in biofilm culture of Pseudomonas pulida F1. J. Microbiol. Methods 40:181-191.
41. Xiao, Z., Y. Hao, B. Liu, and L. Qian. 2002. Indirubin and meisoindigo in the treatment of chronic myelogenous leukemia in China. Leuk. Lymphoma 43:1763-1768.
42. Yasokui, M. December 1989. Production of 7-hydroxyindole-2-carboxylic acid compound. International patent JP1308249.
43. Yen, K. M., M. R. Karl, L. M. Blatt, M. J. Simon, R. B. Winter, P. R. Fausset, H. S. Lu, A. A. Harcourt, and K. K. Chen. 1991. Cloning and characterization of a Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase. J. Bacteriol. 173:5315-5327.
44. Zollinger, H. 1991. Color chemistry: syntheses, properties, and applications of organic dyes and pigments, 2nd rev. ed., p. 191-195. Wiley-VCH, Weinheim, Germany.