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Original Articles

Growth-phase Dependent Expression of the Mevalonate Pathway in a Terpenoid Antibiotic-producing Streptomyces Strain

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Pages 808-819 | Received 12 Oct 2001, Accepted 19 Nov 2001, Published online: 22 May 2014

  • 1) Connolly, J. D. and Hill, R. A., Dictionary of terpenoids. Chapman and Hall, New York (1992).
  • 2) Porter, J. W. and Spurgeon, S. L., Biosynthesis of isoprenoid compounds, vol. 1. John Wiley & Sons, Inc., New York (1981).
  • 3) Porter, J. W. and Spurgeon, S. L., Biosynthesis of isoprenoid compounds, vol. 2. John Wiley & Sons, Inc., New York (1983).
  • 4) Chappell, J., Biochemistry and molecular biology of the isoprenoid biosynthetic pathways in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 46, 521-547 (1995).
  • 5) Servouse, M., Mons, N., Baillaargeat, J.-L., and Karst, F., Isolation and characterization of yeast mutants blocked in mevalonic acid formation. Biochem. Biophy. Res. Com., 123, 424-430 (1984).
  • 6) Eisenreich, W., Schwarz, M., Catayrade, A., Arigoni, D., Zenk, M. H., and Bacher, A., The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem. Biol., 5, R221-R233 (1998).
  • 7) Orihara, N., Furihata, K., and Seto, H., Studies on the biosynthesis of terpenoidal compounds produced by Actinomycetes. 2. Biosynthesis of carquinostatin B via the non-mevalonate pathway in Streptomyces exfoliatus. J. Antibiot., 50, 979-981 (1997).
  • 8) Rohmer, M., Knani, M., Simonin, P., Sutter, B., and Sahm, H., Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J., 295, 517-524 (1993).
  • 9) Rohmer, M., Seemann, M., Horbach, S., Bringer-Meyer, S., and Sahm, H., Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J. Am. Chem. Soc., 118, 2564-2566 (1996).
  • 10) Seto, H., Orihara, N., and Furihata, K., Studies on the biosynthesis of terpenoids produced by Actinomycetes. Part 4. Formation of BE-40644 by the mevalonate and nonmevalonate pathways. Tetrahedron Lett., 39, 9497-9500 (1998).
  • 11) Seto, H., Watanabe, H., and Furihata, K., Simultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenyl diphosphate in Streptomyces aeriouvifer. Tetrahedron Lett., 37, 7979-7982 (1996).
  • 12) Lois, L. M., Campos, N., Rosa Putra, S., Danielsen, K., Rohmer, M., and Boronat, A., Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamine, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA, 95, 2105-2110 (1998).
  • 13) Sprenger, G. A., Schorken, U., Wiegert, T., Grolle, S., DeGraaf, A. A., Taylor, S. V., Begley, T. P., Bringer-Meyer, S., and Sahm, H., Identification of a thiamine-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-D-xylulose 5-phosphate precursor to isoprenoids, thiamine, and pyridoxol. Proc. Natl. Acad. Sci. USA, 94, 12857-12862 (1997).
  • 14) Hahn, F. M., Eubanks, L. M., Testa, C. A., Blagg, B. S., Baker, J. A., and Poulter, C. D., 2001. 1-deoxy- D-xylulose 5-phosphate synthase, the gene product of open reading frame (ORF) 2816 and ORF 2895 in Rhodobacter capsulatus. J. Bacteriol., 183, 1-11.
  • 15) Altincicek, B., Hintz, M., Sanderbrand, S., Wiesner, J., Beck, E., and Jomaa, H., Tools for discovery of inhibitors of the 1-deoxy-D-xylulose-5-phosphate (DXP) synthase and DXP reductoisomerase: an approach with enzymes from the pathogenic bacterium Pseudomonas aeruginosa. FEMS Microbiol. Lett., 190, 329-333 (2000).
  • 16) Kuzuyama, T., Takagi, M., Takahashi, S., and Seto, H., Cloning and characterization of 1-deoxy-D-xylulose 5-phosphate synthase from Streptomyces sp. Strain CL190, which uses both the mevalonate and nonmevalonate pathways for isopentenyl diphosphate biosynthesis. J. Bacteriol., 182, 891-897 (2000).
  • 17) Cane, D. E., Chow, C., Lillo, A., and Kang, I., Molecular cloning, expression and characterization of the first three genes in the mevalonate-independent isoprenoid pathway in Streptomyces coelicolor. Bioorganic Medical Chem., 9, 1467-1477 (2001).
  • 18) Miller, B., Heuser, T., and Zimmer, W., A Synechococcus leopoliensis SAUG 1402-1 operon harboring the 1-deoxyxylulose 5-phosphate synthase gene and two additional open reading frames is functionally involved in the dimethylallyl diphosphate synthesis. FEBS Lett., 460, 485-490 (1999).
  • 19) Esteves, J. M., Cantero, A., Reindl, A., Reichler, S., and Leon, P., 1-deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem., 276, 22901-22909 (2001).
  • 20) Lange, B. M., Wildrung, M. R., McCaskill, D., and Croteau, R., A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc. Natl. Acad. Sci. USA, 95, 2100-2104 (1998).
  • 21) Bouvier, F., d'Harlingue, A., Suire, C., Backhous, R. A., and Camara, B., Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant. Physiol., 117, 1423-1431 (1998).
  • 22) Lois, L. M., Rodrigues-Concepcion, Gallego, M. F., Campos, N., and Boronat, A., Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J., 22, 503-513 (2000).
  • 23) Chahed, K., Oudin, A., Guivarc'h, N., Hamdi, D., Chenieux, J. C., Rideau, M., and Clastre, M., 1-deoxy-D-xylulose 5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant Physiol. Biochem., 38, 559-566 (2000).
  • 24) Kuzuyama, T., Takahashi, S., Takagi, M., and Seto, H., Characterization of 1-deoxy-D-xylulose 5-phosphate reductoisomerase, an enzyme involved in the biosynthesis of isopentenyl diphosphate, and identification of its catalytic amino acid residues. J. Biol. Chem., 275, 19928-19932 (2000).
  • 25) Takahashi, S., Kuzuyama, T., Watanabe, H., and Seto, H., A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA, 95, 9879-9884 (1998).
  • 26) Herz, S., Wungsintaweekul, J., Schuhr, C. A., Hecht, S., Lüttgen, H., Sagner, S., Fellermeier, M., Eisenreich, W., Zenk, M. H., Bacher, A., and Rohdich, F., Biosynthesis of terpenoid: YgbB protein converts 4-diphosphocytidyl-2C-methyl-D-erythritol 2-phosphate to 2C-methyl-D-erythritol 2,4- cyclodiphosphate. Proc. Natl. Acad. Sci. USA, 97, 2486-2490 (2000).
  • 27) Lüttgen, H., Rohdich, F., Herz, S., Wungsintaweekul, J., Hecht, S., Schuhr, C. A., Fellermeier, M., Sagner, S., Zenk, M. H., Bacher, A., and Eisenreich, W., Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-phosphocytidyl-2C-methyl-D-erythritol. Proc. Natl. Acad. Sci. USA, 97, 1062-1067 (2000).
  • 28) Rohdich, F., Wungsintaweekul, J., Fellermeier, M., Sagner, S., Herz, S., Kis, K., Eisenreich, W., Bacher, A., and Zenk, M. H., Cytidine 5′-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2-C-methylerythritol. Proc. Natl. Acad. Sci. USA, 95, 11758-11763 (1999).
  • 29) Kuzuyama, T., Takagi, M., Kaneda, K., Dairi, T., and Seto, H., Formation of 4-(cytidine 5′-diphospho)-2-C-methyl-D-erythritol from 2-C-methyl-D-erythritol 4-phosphate by 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase, a new enzyme in the nonmevalonate pathway. Tetrahedron Lett., 41, 703-706 (2000).
  • 30) Kuzuyama, T., Takagi, M., Kaneda, K., Watanabe, H., Dairi, T., and Seto, H., Studies on the nonmevalonate pathway: conversion of 4-(cytidine 5′-diphospho)-2-C-methyl-D-erythritol to its 2-phospho derivative by 4-(cytidine 5′-diphospho)-2-C-methyl-D-erythritol kinase. Tetrahedron Lett., 41, 2925-2928 (2000).
  • 31) Kuzuyama, T., Takagi, M., Kaneda, K., Watanabe, H., Dairi, T., and Seto, H., Studies on the nonmevalonate pathway: Formation of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate from 2-phospho- 4-(cytidine 5′-diphospho)-2-C-methyl-D-erythritol. Tetrahedron Lett., 41, 3395-3398 (2000).
  • 32) Dairi, T., Hamano, Y., Kuzuyama, T., Itoh, N., Furihata, K., and Seto, H., Eubacterial Diterpene Cyclase Genes Essential for Production of Isoprenoid Antibiotic-terpentecin. J. Bacteriol., 183, 6085-6094 (2001).
  • 33) Dairi, T., Motohira, Y., Kuzuyama, T., Takahashi, S., Itoh, N., and Seto, H., Cloning of the gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from terpenoid antibiotics-producing Streptomyces strains. Mol. Gen. Genet., 262, 957-964 (2000).
  • 34) Hamano, Y., Dairi, T., Yamamoto, M., Kawasaki, T., Kaneda, K., Kuzuyama, T., Itoh, N., and Seto, H., Cloning of a gene cluster encoding enzymes responsible for the mevalonate pathway from a terpenoid-antibiotic-producing Streptomyces strain. Biosci. Biotechnol. Biochem., 65, 1627-1635 (2001).
  • 35) Taylor, S. V., Vu, L. D., and Begley, T. P., Chemical and enzymatic synthesis of 1-deoxy-D-xylulose-5-phosphate. J. Org. Chem., 63, 275-2377 (1998).
  • 36) Isshiki, K., Tamamura, T., Sawa, T., Naganawa, H., Takeuchi, T., and Umezawa, H., Biosynthetic studies of terpentecin. J. Antibiot., 34, 1634-1635 (1986).
  • 37) Tamamura, T., Sawa, T., Isshiki, K., Masuda, T., Homma, Y., Iinuma, H., Naganawa, H., Hamada, M., Takeuchi, T., and Umezawa, H., Isolation and characterization of terpentecin, a new antitumor antibiotic. J. Antibiot., 38, 1664-1669 (1985).
  • 38) Hopwood, D. A., Bibb, M. J., Chater, K. F., Kieser, T., Bruton, C. J., Kieser, H. M., Lydiate, D. J., Smith, C. P., Ward, J. M., and Schremp, H., Gene manipulation of Streptomyces, a laboratory manual. The John Innes Foundation, Norwich, UK (1985).
  • 39) Dairi, T., Ohta, T., Hashimoto, E., and Hasegawa, M., Organization and nature of fortimicin A (astromicin) biosynthetic genes studied using a cosmid library of Micromonospora olivasterospora DNA. Mol. Gen. Genet., 236, 39-48 (1992).
  • 40) Sanger, F., Nicklen, S., and Coulson, A. R., DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA, 74, 5463-5467 (1977).
  • 41) Byers, L. D., Glyceraldehyde-3-phosphate dehydrogenase from yeast. Methods Enzymol., 89, 326-335 (1982).
  • 42) Dairi, T., Nakano, T., Aisaka, K., Katsumata, R., and Hasegawa, M., Cloning and nucleotide sequence of the gene responsible for chlorination of tetracycline. Biosci. Biotechnol. Biochem., 59, 1099-1106 (1995).
  • 43) Dairi, T., Ohta, T., Hashimoto, E., and Hasegawa, M., Organization and nature of fortimicin A (astromicin) biosynthetic genes studied using a cosmid library of Micromonospora olivasterospora DNA. Mol. Gen. Genet., 236, 39-48 (1992).
  • 44) Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J., Basic local alignment search tool. J. Mol. Biol., 215, 403-410 (1990).
  • 45) Pearson, W. R. and Lipman, D. J., Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA, 85, 2444-2448 (1988).
  • 46) Himmeldirk, K., Kennedy, I. A., Hill, R. E., Sayer, B. G., and Spencer, I. D., Biosynthesis of vitamins B1 and B6 in Escherichia coli: concurrent incorporation of 1-deoxy-D-xylulose into thiamine (B1) and pyridoxol (B6). Chem. Commun., 1187-1188 (1996).
  • 47) Julliard, J. and Douce, R., Biosynthesis of the thiazole moiety of thiamine (vitamin B1) in higher plant chloroplast. Proc. Natl. Acad. Sci. USA, 88, 2042-2045 (1991).
  • 48) Fröhlich, K. U., Kannwischer, R., Rudiger, M., and Mecke, D., Pentalenolactone-insensitive glyceraldehyde-3-phosphate dehydrogenase from Streptomyces arenae is closely related to GAPDH from thermostable eubacteria and plant chloroplasts. Arch. Microbiol., 165, 179-186 (1996).
  • 49) Fröhlich, K. U., Wiedmann, M., Lottspeich, F., and Mecke, D., Substitution of a pentalenolactone-sensitive glyceraldehyde-3-phosphate dehydrogenase by a genetically distinct resistant isoform accompanies pentalenolactone production in Streptomyces arenae. J. Bacteriol., 171, 6696-6702 (1989).
  • 50) Kormanec, J., Lempelová, A., Farkasovsky, M., and Homerová, D., Cloning, sequencing and expression in Escherichia coli of Streptomyces aureofaciens gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene, 165, 77-80 (1995).
  • 51) Kormanec, J., Lempel'ova, A., Novakova, R., Rezuchova, B., and Homerová, D., Expression of the Streptomyces aureofaciens glyceraldehyde-3-phosphate dehydrogenase gene (gap) is developmentally regulated and induced by glucose. Microbiol., 143, 3555-3561 (1997).

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