Indigoid dyes by group E monooxygenases: mechanism and biocatalysis.
dye production
epoxidation
flavoprotein
indole monooxygenase
styrene monooxygenase
Journal
Biological chemistry
ISSN: 1437-4315
Titre abrégé: Biol Chem
Pays: Germany
ID NLM: 9700112
Informations de publication
Date de publication:
26 06 2019
26 06 2019
Historique:
received:
15
01
2019
accepted:
19
02
2019
pubmed:
8
3
2019
medline:
18
2
2020
entrez:
8
3
2019
Statut:
ppublish
Résumé
Since ancient times, people have been attracted by dyes and they were a symbol of power. Some of the oldest dyes are indigo and its derivative Tyrian purple, which were extracted from plants and snails, respectively. These 'indigoid dyes' were and still are used for coloration of textiles and as a food additive. Traditional Chinese medicine also knows indigoid dyes as pharmacologically active compounds and several studies support their effects. Further, they are interesting for future technologies like organic electronics. In these cases, especially the indigo derivatives are of interest but unfortunately hardly accessible by chemical synthesis. In recent decades, more and more enzymes have been discovered that are able to produce these indigoid dyes and therefore have gained attention from the scientific community. In this study, group E monooxygenases (styrene monooxygenase and indole monooxygenase) were used for the selective oxygenation of indole (derivatives). It was possible for the first time to show that the product of the enzymatic reaction is an epoxide. Further, we synthesized and extracted indigoid dyes and could show that there is only minor by-product formation (e.g. indirubin or isoindigo). Thus, group E monooxygenase can be an alternative biocatalyst for the biosynthesis of indigoid dyes.
Identifiants
pubmed: 30844759
doi: 10.1515/hsz-2019-0109
pii: hsz-2019-0109
doi:
Substances chimiques
Coloring Agents
0
Epoxy Compounds
0
Indoles
0
Indigo Carmine
D3741U8K7L
Mixed Function Oxygenases
EC 1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
939-950Références
Arora, P.K., Sharma, A., and Bae, H. (2015). Microbial degradation of indole and its derivatives. J. Chem. 2015, 1–13.
Boyd, C., Larkin, M.J., Reid, K.A., Sharma, N.D., and Wilson, K. (1997). Metabolism of naphthalene, 1-naphthol, indene, and indole by Rhodococcus sp. strain NCIMB 12038. Appl. Environ. Microbiol. 63, 151–155.
Cerniglia, C.E., Freeman, J.P., and Evans, F.E. (1984). Evidence for an arene oxide-NIH shift pathway in the transformation of naphthalene to 1-naphthol by Bacillus cereus. Arch. Microbiol. 138, 283–286.
Dua, A., Chauhan, K., and Pathak, H. (2014). Biotransformation of indigo pigment by indigenously isolated Pseudomonas sp. HAV-1 and assessment of its antioxidant property. Biotechnol. Res. Int. 2014, 109249.
Dupard-Julien, C.L., Kandlakunta, B., and Uppu, R.M. (2007). Determination of epoxides by high-performance liquid chromatography following derivatization with N,N-diethyldithiocarbamate. Anal. Bioanal. Chem. 387, 1027–1032.
Eisenbrand, G., Hippe, F., Jakobs, S., and Muehlbeyer, S. (2004). Molecular mechanisms of indirubin and its derivatives: novel anticancer molecules with their origin in traditional Chinese phytomedicine. J. Cancer Res. Clin. Oncol. 130, 627–635.
Ensley, B.D., Ratzkin, B.J., Osslund, T.D., Simon, M.J., Wackett, L.P., and Gibson, D.T. (1983). Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222, 167–169.
Farias-Silva, E., Cola, M., Calvo, T.R., Barbastefano, V., Ferreira, A.L., De Paula Michelatto, D., Alves de Almeida, A.C., Hiruma-Lima, C.A., Vilegas, W., and Brito, A.R. (2007). Antioxidant activity of indigo and its preventive effect against ethanol-induced DNA damage in rat gastric mucosa. Planta Med. 73, 1241–1246.
Fleischmann, C., Lievenbrück, M., and Ritter, H. (2015). Polymers and dyes. Developments and applications. Polymers 7, 717–746.
Fujioka, M. and Wada, H. (1968). The bacterial oxidation of indole. Biochim. Biophys. Acta Gen. Subj. 158, 70–78.
Fukuoka, K., Tanaka, K., Ozeki, Y., and Kanaly, R.A. (2015). Biotransformation of indole by Cupriavidus sp. strain KK10 proceeds through N-heterocyclic- and carbocyclic-aromatic ring cleavage and production of indigoids. Int. Biodeterior. Biodegradation 97, 13–24.
Glawischnig, E., Grün, S., Frey, M., and Gierl, A. (1999). Cytochrome P450 monooxygenases of DIBOA biosynthesis. Specificity and conservation among grasses. Phytochemistry 50, 925–930.
Głowacki, E.D., Voss, G., Leonat, L., Irimia-Vladu, M., Bauer, S., and Sariciftci, N.S. (2012). Indigo and tyrian purple – from ancient natural dyes to modern organic semiconductors. Isr. J. Chem. 52, 540–551.
Gröning, J.A.D., Kaschabek, S.R., Schlömann, M., and Tischler, D. (2014). A mechanistic study on SMOB-ADP1: an NADH:flavin oxidoreductase of the two-component styrene monooxygenase of Acinetobacter baylyi ADP1. Arch. Microbiol. 196, 829–845.
Guengerich, F.P., Martin, M.V., McCormick, W.A., Nguyen, L.P., Glover, E., and Bradfield, C.A. (2004a). Aryl hydrocarbon receptor response to indigoids in vitro and in vivo. Arch. Biochem. Biophys. 423, 309–316.
Guengerich, F.P., Sorrells, J.L., Schmitt, S., Krauser, J.A., Aryal,P., and Meijer, L. (2004b). Generation of new protein kinase inhibitors utilizing cytochrome p450 mutant enzymes for indigoid synthesis. J. Med. Chem. 47, 3236–3241.
Gursky, L.J., Nikodinovic-Runic, J., Feenstra, K.A., and O’Connor, K.E. (2010). In vitro evolution of styrene monooxygenase from Pseudomonas putida CA-3 for improved epoxide synthesis. Appl. Microbiol. Biotechnol. 85, 995–1004.
Harrer, R. (2012). Indigo auf Speicherchips. Chem. Unser. Zeit 46, 136.
He, B., Pun, A.B., Zherebetskyy, D., Liu, Y., Liu, F., Klivansky, L.M., McGough, A.M., Zhang, B.A., Lo, K., Russell, T.P., et al. (2014). New form of an old natural dye: bay-annulated indigo (BAI) as an excellent electron accepting unit for high performance organic semiconductors. J. Am. Chem. Soc. 136, 15093–15101.
Heine, T., Großmann, C., Hofmann, S., and Tischler, D. (2018a). Enzymgesteuerte Indigoproduktion. Biospektrum 24, 446–448.
Heine, T., van Berkel, W.J.H., Gassner, G., van Pée, K.-H., and Tischler, D. (2018b). Two-component fad-dependent monooxygenases. Current knowledge and biotechnological opportunities. Biology (Basel) 7, 42.
Heine, T., Zimmerling, J., Ballmann, A., Kleeberg, S.B., Rückert, C., Busche, T., Winkler, A., Kalinowski, J., Poetsch, A., Scholtissek, A., et al. (2018c). On the enigma of glutathione-dependent styrene degradation in Gordonia rubripertincta CWB2. Appl. Environ. Microbiol. 84, e00154-18.
Hoessel, R., Leclerc, S., Endicott, J.A., Nobel, M.E., Lawrie, A., Tunnah, P., Leost, M., Damiens, E., Marie, D., Marko, D., et al. (1999). Indirubin, the active constituent of a Chinese antileukaemia medicine, inhibits cyclin-dependent kinases. Nat. Cell Biol. 1, 60–67.
Hössel, R. (1999). Synthese von Derivaten des Indirubins und Untersuchungen zur Mechanismusaufklärung ihrer antineoplastischen Wirkung.
Hsu, T.M., Welner, D.H., Russ, Z.N., Cervantes, B., Prathuri, R.L., Adams, P.D., and Dueber, J.E. (2018). Employing a biochemical protecting group for a sustainable indigo dyeing strategy. Nat. Chem. Biol. 14, 256–261.
Irimia-Vladu, M., Głowacki, E.D., Troshin, P.A., Schwabegger, G., Leonat, L., Susarova, D.K., Krystal, O., Ullah, M., Kanbur, Y., Bodea, M.A., et al. (2012). Indigo – a natural pigment for high performance ambipolar organic field effect transistors and circuits. Adv. Mater. Weinheim 24, 375–380.
Kapadia, G.J., Tokuda, H., Sridhar, R., Balasubramanian, V., Takayasu, J., Bu, P., Konoshima, T., and Nishino, H. (1998). Cancer chemopreventive activity of synthetic colorants used in foods, pharmaceuticals and cosmetic preparations. Cancer Lett. 129, 87–95.
Kim, J. and Park, W. (2015). Indole: a signaling molecule or a mere metabolic byproduct that alters bacterial physiology at a high concentration? J. Microbiol. 53, 421–428.
Kunikata, T., Tatefuji, T., Aga, H., Iwaki, K., Ikeda, M., and Kurimoto, M. (2000). Indirubin inhibits inflammatory reactions in delayed-type hypersensitivity. Eur. J. Pharmacol. 410, 93–100.
Leclerc, S., Garnier, M., Hoessel, R., Marko, D., Bibb, J.A., Snyder, G.L., Greengard, P., Biernat, J., Wu, Y.Z., Mandelkow, E.M., et al. (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.
Lee, J.-H., Wood, T.K., and Lee, J. (2015). Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. 23, 707–718.
Li, G. and Young, K.D. (2013). Indole production by the tryptophanase TnaA in Escherichia coli is determined by the amount of exogenous tryptophan. Microbiology (Reading) 159, 402–410.
Lin, G.-H., Chen, H.-P., Huang, J.-H., Liu, T.-T., Lin, T.-K., Wang, S.-J., Tseng, C.-H., and Shu, H.-Y. (2012). Identification and characterization of an indigo-producing oxygenase involved in indole 3-acetic acid utilization by Acinetobacter baumannii. Antonie van Leeuwenhoek 101, 881–890.
Lin, G.-H., Chen, H.-P., Shu, H.-Y., and Lee, S.-W. (2015). Detoxification of indole by an indole-induced flavoprotein oxygenase from Acinetobacter baumannii. PLoS One 10, e0138798.
Ma, Q., Qu, Y., Zhang, X., Liu, Z., Li, H., Zhang, Z., Wang, J., Shen,W., and Zhou, J. (2015). Systematic investigation and microbial community profile of indole degradation processes in two aerobic activated sludge systems. Sci. Rep. 5, 17674.
Ma, Q., Liu, Z., Yang, B., Dai, C., and Qu, Y. (2018a). Characterization and functional gene analysis of a newly isolated indole-degrading bacterium Burkholderia sp. IDO3. J. Hazard. Mater. 367, 144–151.
Ma, Q., Zhang, X., and Qu, Y. (2018b). Biodegradation and biotransformation of indole. Advances and perspectives. Front. Microbiol. 9, 2625.
McClay, K., Boss, C., Keresztes, I., and Steffan, R.J. (2005). Mutations of toluene-4-monooxygenase that alter regiospecificity of indole oxidation and lead to production of novel indigoid pigments. Appl. Environ. Microbiol. 71, 5476–5483.
Mermod, N., Harayama, S., and Timmis, K.N. (1986). New route to bacterial production of indigo. Nat. Biotechnol. 4, 321–324.
Meyer, A. (2002). Hydroxylation of indole by laboratory-evolved 2-hydroxybiphenyl 3-monooxygenase. J. Biol. Chem. 277, 34161–34167.
Miyamoto, K., Okuro, K., and Ohta, H. (2007). Substrate specificity and reaction mechanism of recombinant styrene oxide isomerase from Pseudomonas putida S12. Tetrahedron Lett. 48, 3255–3257.
Montersino, S., Tischler, D., Gassner, G.T., and van Berkel, W.J.H. (2011). Catalytic and structural features of flavoprotein hydroxylases and epoxidases. Adv. Synth. Catal. 353, 2301–2319.
Murdock, D., Ensley, B.D., Serdar, C., and Thalen, M. (1993). Construction of metabolic operons catalyzing the de novo biosynthesis of indigo in Escherichia coli. Bio/Technology 11, 381–386.
Namgung, S., Park, H.A., Kim, J., Lee, P.-G., Kim, B.-G., Yang, Y.-H., and Choi, K.-Y. (2019). Ecofriendly one-pot biosynthesis of indigo derivative dyes using CYP102G4 and PrnA halogenase. Dyes Pigm. 162, 80–88.
O’Connor, K.E., Dobson, A.D., and Hartmans, S. (1997). Indigo formation by microorganisms expressing styrene monooxygenase activity. Appl. Environ. Microbiol. 63, 4287–4291.
Otto, K., Hofstetter, K., Röthlisberger, M., Witholt, B., and Schmid,A. (2004). Biochemical characterization of StyAB from Pseudomonas sp. strain VLB120 as a two-component flavin-diffusible monooxygenase. J. Bacteriol. 186, 5292–5302.
Pathak, H. and Madamwar, D. (2010). Biosynthesis of indigo dye by newly isolated naphthalene-degrading strain Pseudomonas sp. HOB1 and its application in dyeing cotton fabric. Appl. Biochem. Biotechnol. 160, 1616–1626.
Paul, C.E., Tischler, D., Riedel, A., Heine, T., Itoh, N., and Hollmann, F. (2015). Nonenzymatic regeneration of styrene monooxygenase for catalysis. ACS Catal. 5, 2961–2965.
Perpète, E.A., Preat, J., André, J.-M., and Jacquemin, D. (2006). An ab initio study of the absorption spectra of indirubin, isoindigo, and related derivatives. J. Phys. Chem. A 110, 5629–5635.
Petermayer, C. and Dube, H. (2018). Indigoid photoswitches. Visible light responsive molecular tools. Acc. Chem. Res. 51, 1153–1163.
Qu, Y., Ma, Q., Liu, Z., Wang, W., Tang, H., Zhou, J., and Xu, P. (2017). Unveiling the biotransformation mechanism of indole in a Cupriavidus sp. strain. Mol. Microbiol. 106, 905–918.
Riedel, A., Heine, T., Westphal, A.H., Conrad, C., Rathsack, P., van Berkel, W.J.H., and Tischler, D. (2015). Catalytic and hydrodynamic properties of styrene monooxygenases from Rhodococcus opacus 1CP are modulated by cofactor binding. AMB Express 5, 112.
Sadauskas, M., Vaitekūnas, J., Gasparavičiūtė, R., and Meškys,R. (2017). Indole biodegradation in Acinetobacter sp. strain O153. Genetic and biochemical characterization. Appl. Environ. Microbiol. 83.
Sambrook, J. and Russell, D.W., eds. (2001). Molecular Cloning. A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
Sharma, V., Kumar, P., and Pathak, D. (2010). Biological importance of the indole nucleus in recent years: a comprehensive review. J. Heterocyclic Chem. 39, 491–502.
Studier, F.W. (2005). Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207–234.
Tan, C., Zhang, X., Zhu, Z., Xu, M., Yang, T., Osire, T., Yang, S., and Rao, Z. (2019). Asp305Gly mutation improved the activity and stability of the styrene monooxygenase for efficient epoxide production in Pseudomonas putida KT2440. Microb. Cell. Fact. 18, 12. doi: 10.1186/s12934-019-1065-5.
Tischler, D., Eulberg, D., Lakner, S., Kaschabek, S.R., van Berkel, W.J.H., and Schlömann, M. (2009). Identification of a novel self-sufficient styrene monooxygenase from Rhodococcus opacus 1CP. J. Bacteriol. 191, 4996–5009.
Tischler, D., Kermer, R., Gröning, J.A.D., Kaschabek, S.R., van Berkel, W.J.H., and Schlömann, M. (2010). StyA1 and StyA2B from Rhodococcus opacus 1CP: a Multifunctional styrene monooxygenase system. J. Bacteriol. 192, 5220–5227.
Tischler, D., Gröning, J.A.D., Kaschabek, S.R., and Schlömann, M. (2012). One-component styrene monooxygenases: an evolutionary view on a rare class of flavoproteins. Appl. Biochem. Biotechnol. 167, 931–944.
Tischler, D., Schwabe, R., Siegel, L., Joffroy, K., Kaschabek, S., Scholtissek, A., and Heine, T. (2018). VpStyA1/VpStyA2B of Variovorax paradoxus EPS. An aryl alkyl sulfoxidase rather than a styrene epoxidizing monooxygenase. Molecules (Basel, Switzerland) 23, 809. doi: 10.3390/molecules23040809.
Toda, H., Imae, R., Komio, T., and Itoh, N. (2012). Expression and characterization of styrene monooxygenases of Rhodococcus sp. ST-5 and ST-10 for synthesizing enantiopure (S)-epoxides. Appl. Microbiol. Biotechnol. 96, 407–418.
Uehara, K., Takagishi, K., and Tanaka, M. (1987). The Al/Indigo/Au photovoltaic cell. Solar Cells 22, 295–301.
van Hellemond, E.W., Janssen, D.B., Fraaije, M.W., Janssen, D.B., and Fraaije, M.W. (2007). Discovery of a novel styrene monooxygenase originating from the metagenome. Appl. Environ. Microbiol. 73, 5832–5839.
Wu, Z.-L., Aryal, P., Lozach, O., Meijer, L., and Guengerich, F.P. (2005). Biosynthesis of new indigoid inhibitors of protein kinases using recombinant cytochrome P450 2A6. Chem. Biodivers. 2, 51–65.
Xiao, Z., Hao, Y., Liu, B., and Qian, L. (2002). Indirubin and meisoindigo in the treatment of chronic myelogenous leukemia in China. Leuk. Lymphoma 43, 1763–1768.
Yuan, L.-J. (2011). Biooxidation of indole and characteristics of the responsible enzymes. Afr. J. Biotechnol. 10, 83B807F36739.
Zhang, X., Jing, J., Zhang, L., Song, Z., Zhou, H., Wu, M., Qu, Y., and Liu, L. (2018). Biodegradation characteristics and genomic functional analysis of indole-degrading bacterial strain Acinetobacter sp. JW. J. Chem. Technol. Biotechnol. Doi: 10.1002/jctb.5858.