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Microbiology & Fermentation Technology

Subcellular localization of aphidicolin biosynthetic enzymes heterologously expressed in Aspergillus oryzae

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Pages 139-147 | Received 05 Aug 2017, Accepted 17 Oct 2017, Published online: 01 Dec 2017

References

  • Machida M, Yamada O, Gomi K. Genomics of Aspergillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res. 2008;15:173–183.10.1093/dnares/dsn020
  • Heneghan MN, Yakasai AA, Halo LM, et al. First heterologous reconstruction of a complete functional fungal biosynthetic multigene cluster. ChemBioChem. 2010;11:1508–1512.10.1002/cbic.v11:11
  • Fujii R, Minami A, Tsukagoshi T, et al. Total biosynthesis of diterpene aphidicolin, a specific inhibitor of DNA polymerase α: heterologous expression of four biosynthetic genes in Aspergillus oryzae. Biosci Biotechnol Biochem. 2011;75:1813–1817.10.1271/bbb.110366
  • Tagami K, Liu C, Minami A, et al. Reconstitution of biosynthetic machinery for indole-diterpene paxilline in Aspergillus oryzae. J Am Chem Soc. 2013;135:1260–1263.10.1021/ja3116636
  • Tagami K, Minami A, Fujii R, et al. Rapid reconstitution of biosynthetic machinery for fungal metabolites in Aspergillus oryzae: total biosynthesis of aflatrem. ChemBioChem. 2014;15:2076–2080.10.1002/cbic.201402195
  • Matsuda Y, Wakimoto T, Mori T, et al. Complete biosynthetic pathway of anditomin: nature’s sophisticated synthetic route to a complex fungal meroterpenoid. J Am Chem Soc. 2014;136:15326–15336.10.1021/ja508127q
  • Ugai T, Minami A, Fujii R, et al. Heterologous expression of highly reducing polyketide synthase involved in betaenone biosynthesis. Chem Commun. 2015;51:1878–1881.10.1039/C4CC09512J
  • Matsuda Y, Iwabuchi T, Wakimoto T, et al. Uncovering the unusual D-ring construction in terretonin biosynthesis by collaboration of a multifunctional cytochrome P450 and a unique isomerase. J Am Chem Soc. 2015;137:3393–3401.10.1021/jacs.5b00570
  • Liu C, Tagami K, Minami A, et al. Reconstitution of biosynthetic machinery for highly elaborated indole diterpene penitrem. Angew Chem Int. 2015;54:5748–5752.10.1002/anie.201501072
  • Ye Y, Minami A, Mándi A, et al. Genome mining for sesterterpenes using bifunctional terpene syntheses reveals a unified intermediate of di/sesterterpenes. J Am Chem Soc. 2015;137:11846–11853.10.1021/jacs.5b08319
  • Bailey AM, Alberti F, Kilaru S, et al. Identification and manipulation of the pleuromutilin gene cluster from Clitopilus passeckerianus for increased rapid antibiotic production. Sci Rep. 2016;6:25202.10.1038/srep25202
  • Ikegami S, Taguchi T, Ohashi M, et al. Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-alpha. Nature. 1978;275:458–460.10.1038/275458a0
  • Toyomasu T, Nakaminami K, Toshima H, et al. Cloning of a gene cluster responsible for the biosynthesis of diterpene aphidicolin, a specific inhibitor of DNA polymerase alpha. Biosci Biotechnol Biochem. 2004;68:146–152.10.1271/bbb.68.146
  • Lim FY, Keller NP. Spatial and temporal control of fungal natural products synthesis. Nat Prod Rep. 2014;31:1277–1286.10.1039/C4NP00083H
  • Kistler HC, Broz K. Cellular compartmentalization of secondary metabolism. Front Microbiol. 2015;6:68.
  • Hong SY, Linz JE. Functional expression and sub-cellular localization of the early aflatoxin pathway enzyme Nor-1 in Aspergillus parasiticus. Mycol Res. 2009;113:591–601.10.1016/j.mycres.2009.01.013
  • Chanda A, Roze LV, Kang S, et al. A key role for vesicles in fungal secondary metabolism. Proc Nat Acad Sci USA. 2009;106:19533–19538.10.1073/pnas.0907416106
  • Bartoszewska M, Opaliński L, Veenhuis M, et al. The significance of peroxisomes in secondary metabolite biosynthesis in filamentous fungi. Biotechnol Lett. 2011;33:1921–1931.10.1007/s10529-011-0664-y
  • Kiel JA, van der Klei IJ, van den Berg MA, et al. Overproduction of a single protein, Pc-Pex11p, results in 2-fold enhanced penicillin production by Penicillium chrysogenum. Fungal Genet Biol. 2005;42:154–164.10.1016/j.fgb.2004.10.010
  • Opalinski L, Kiel JA, Homan TG, et al. Penicillium chrysogenum Pex14/17p—a novel component of the peroxisomal membrane that is important for penicillin production. FEBS J. 2014;277:3203–3218.
  • Minetoki T, Nunokawa Y, Gomi K, et al. Deletion analysis of promoter elements of the Aspergillus oryzae agdA gene encoding α-glucosidase. Curr Genet. 1996;30(5):432–438.10.1007/s002940050153
  • Hasegawa S, Takizawa M, Suyama H, et al. Characterization and expression analysis of a maltose-utilizing (MAL) cluster in Aspergillus oryzae. Fungal Genet Biol. 2010;47:1–9.10.1016/j.fgb.2009.10.005
  • Minetoki T, Tsuboi H, Koda A, et al. Development of high expression system with the improved promoter using the cis-acting element in Aspergillus species. J Biol Macromol. 2003;3:89–96.
  • Makita T, Katsuyama Y, Tani S, et al. Inducer-dependent nuclear localization of a Zn(II)2Cys6 transcriptional activator, AmyR, in Aspergillus nidulans. Biosci Biotechnol Biochem. 2009;73:391–399.10.1271/bbb.80654
  • Krogh A, Larsson B, von Heijne G, et al. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–580.10.1006/jmbi.2000.4315
  • Shintani T, Reggiori F. Fluorescence microscopy-based assays for monitoring yeast Atg protein trafficking. Methods Enzymol. 2008;451:43–56.10.1016/S0076-6879(08)03204-7
  • Hiramoto T, Tanaka M, Ichikawa T, et al. Endocytosis of a maltose permease is induced when amylolytic enzyme production is repressed in Aspergillus oryzae. Fungal Genet Biol. 2015;82:136–144.10.1016/j.fgb.2015.05.015
  • Maruyama J, Kikuchi S, Kitamoto K. Differential distribution of the endoplasmic reticulum network as visualized by the BipA-EGFP fusion protein in hyphal compartments across the septum of the filamentous fungus, Aspergillus oryzae. Fungal Genet Biol. 2006;43:642–654.10.1016/j.fgb.2005.11.007
  • Zhang S, Ban A, Ebara N, et al. Self-excising Cre/mutant lox marker recycling system for multiple gene integrations and consecutive gene deletions in Aspergillus oryzae. J Biosci Bioeng. 2017;123(4):403–411.10.1016/j.jbiosc.2016.11.001
  • O Hatamoto, G Umitsuki, M Machida, et al., inventor; Noda Institute for Scientific Research, Kikkoman Corporation, assignee. Recombinant vector capable of increasing secretion of Koji mold protease. United States patent US 7842799 B2. 2010 Nov 30.
  • Gomi K, Iimura Y, Hara S. Integrative transformation of Aspergillus oryzae with a plasmid containing the Aspergillus nidulans argB gene. Agric Biol Chem. 1987;51:2549–2555.
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685.10.1038/227680a0
  • Kuratsu M, Taura A, Shoji JY, et al. Systematic analysis of SNARE localization in the filamentous fungus Aspergillus oryzae. Fungal Genet Biol. 2007;44:1310–1323.10.1016/j.fgb.2007.04.012
  • Takaya K, Higuchi Y, Kitamoto K, et al. A cytosolic phospholipase A2-like protein in the filamentous fungus Aspergillus oryzae localizes to the intramembrane space of the mitochondria. FEMS Microbiol Lett. 2009;301:201–209.10.1111/fml.2009.301.issue-2
  • Maruyama J, Nakajima H, Kitamoto K. Visualization of nuclei in Aspergillus oryzae with EGFP and analysis of the number of nuclei in each conidium by FACS. Biosci Biotechnol Biochem. 2001;65:1504–1510.10.1271/bbb.65.1504
  • Alberti F, Foster GD, Bailey AM. Natural products from filamentous fungi and production by heterologous expression. Appl Microbiol Biotechnol. 2017;101:493–500.10.1007/s00253-016-8034-2
  • Koning AJ, Roberts CJ, Wright RL. Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations. Mol Biol Cell. 1996;7:769–789.10.1091/mbc.7.5.769
  • Saikia S, Scott B. Functional analysis and subcellular localization of two geranylgeranyl diphosphate synthases from Penicillium paxilli. Mol Genet Genomics. 2009;282:257–271.10.1007/s00438-009-0463-5
  • Albermann S, Linnemannstöns P, Tudzynski B. Strategies for strain improvement in Fusarium fujikuroi: overexpression and localization of key enzymes of the isoprenoid pathway and their impact on gibberellin biosynthesis. Appl Microbiol Biotechnol. 2013;97:2979–2995.10.1007/s00253-012-4377-5
  • Okada K, Saito T, Nakagawa T, et al. Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol. 2000;122:1045–1056.10.1104/pp.122.4.1045
  • Beck G, Coman D, Herren E, et al. Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol Biol. 2013;82:393416.
  • Black SD. Membrane topology of the mammalian P450 cytochromes. FASEB J. 1992;6:680–685.
  • Nair U, Thumm M, Klionsky DJ, et al. GFP-Atg8 protease protection as a tool to monitor autophagosome biogenesis. Autophagy. 2011;7:1546–1550.10.4161/auto.7.12.18424
  • Choe YJ, Park SH, Hassemer T, et al. Failure of RQC machinery causes protein aggregation and proteotoxic stress. Nature. 2016;531:191–195.10.1038/nature16973
  • Cullin C. Two distinct sequences control the targeting and anchoring of the mouse P450 1A1 into the yeast endoplasmic reticulum membrane. Biochem Biophys Res Commun. 1992;184:1490–1495.10.1016/S0006-291X(05)80051-8
  • Pernecky SJ, Larson JR, Philpot RM, et al. Expression of truncated forms of liver microsomal P450 cytochromes 2B4 and 2E1 in Escherichia coli: influence of NH2-terminal region on localization in cytosol and membranes. Proc Nat Acad Sci USA. 1993;90:2651–2655.10.1073/pnas.90.7.2651
  • Sagara Y, Barnes HJ, Waterman MR. Expression in Escherichia coli of functional cytochrome P450c17 lacking its hydrophobic amino-terminal signal anchor. Arch Biochem Biophys. 1993;304:272–278.10.1006/abbi.1993.1349
  • Cosme J, Johnson EF. Engineering microsomal cytochrome P450 2C5 to be a soluble, monomeric enzyme. Mutations that alter aggregation, phospholipid dependence of catalysis, and membrane binding. J Biol Chem. 2000;275:2545–2553.10.1074/jbc.275.4.2545
  • Williams PA, Cosme J, Sridhar V, et al. The crystallographic structure of a mammalian microsomal cytochrome P450 monooxygenase: structural adaptations for membrane binding and functional diversity. Mol Cell. 2000;5:121–131.10.1016/S1097-2765(00)80408-6
  • Ozalp C, Szczesna-Skorupa E, Kemper B. Identification of membrane-contacting loops of the catalytic domain of cytochrome P450 2C2 by tryptophan fluorescence scanning. Biochemistry. 2006;45:4629–4637.10.1021/bi051372t
  • Mast N, Liao WL, Pikuleva IA, et al. Combined use of mass spectrometry and heterologous expression for identification of membrane-interacting peptides in cytochrome P450 46A1 and NADPH-cytochrome P450 oxidoreductase. Arch Biochem Biophys. 2009;483:81–89.10.1016/j.abb.2009.01.002
  • Kempf AC, Zanger UM, Meyer UA. Truncated human P450 2D6: expression in Escherichia coli, Ni(2+)-chelate affinity purification, and characterization of solubility and aggregation. Arch Biochem Biophys. 1995;321:277–288.10.1006/abbi.1995.1396
  • Li YC, Chiang JY. The expression of a catalytically active cholesterol 7α-hydroxylase cytochrome P450 in Escherichia coli. J Biol Chem. 1991;266:19186–19191.

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