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A novel ancestral protein ofDrosophila alcohol dehydrogenase inStreptomyces?

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Abstract

Polyclonal antibodies raised against purifiedDrosophila alcohol dehydrogenase (ADH) were used in Western blot analyses to search for structurally and/or immunologically related proteins in prokaryotes and eukaryotes. No immunological-reactive protein was detected in a flesh fly, a locust, and butterflies. Immunological similarity with the 50-kDa PQQ-glucose dehydrogenase (GluDH)-B enzyme ofAcinetobacter calcoaceticus was found, but the cross-reactivity apparently is dependent on the high hydrophilic character of this protein. Antibodies against PQQ-GluDH did not recognizeDrosophila ADH. In five of seven species of the gram-positive soil bacteria actinomycetes tested, a protein approximately 28–30 kDa in subunit size was strongly recognized by α-DADH. It is probably not one of the two proteins with known homology toDrosophila ADH,viz., theactIII gene product and 20β-hydroxysteroid dehydrogenase. The protein is present in both the soluble and the pellet-membrane fraction of the cells. The protein has a late temporal expression in surface-grown cultures and, therefore, might be involved in secondary metabolism.

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References

  • Baker, M. E. (1990a). A common ancestor for human placental 17β-hydroxysteroid dehydrogenase,Streptomyces coelicolor actIII protein, andDrosophila melanogaster alcohol dehydrogenase.FASEB J. 4222.

    PubMed  Google Scholar 

  • Baker, M. E. (1990b). Sequence similarity betweenPseudomonas dihydrodiol dehydrogenase, part of the gene cluster that metabolizes polychlorinated biphenyls, and dehydrogenases involved in metabolism of ribitol and glucitol and synthesis of antibiotics and 17β-oestradiol, testosterone and corticosterone.Biochem. J. 267839.

    PubMed  Google Scholar 

  • Benner, S., and Ellington, A. D. (1988). Interpreting the behavior of enzymes, purpose or pedigree?CRC Crit. Rev. Biochem. 23369.

    PubMed  Google Scholar 

  • Cleton-Jansen, A.-M. (1991).A Molecular Genetic Analysis of Substrate Specificity of Quinoprotein Glucose Dehydrogenase Ph.D. thesis, University of Leiden, Leiden, The Netherlands.

    Google Scholar 

  • Cleton-Jansen, A.-M., Goosen, N., Vink, K., and van de Putte, P. (1989). Cloning, characterization and DNA sequencing of the gene encoding the Mr 50,000 quinoprotein glucose dehydrogenase fromAcinetobacter calcoaceticus.Mol. Gen. Genet. 217430.

    PubMed  Google Scholar 

  • Cundliffe, E. (1989). How antibiotic-producing organisms avoid suicide.Annu. Rev. Microbiol. 43207.

    PubMed  Google Scholar 

  • Eisses, K. Th. (1989). On the oxidation of aldehydes by alcohol dehydrogenase ofDrosophila melanogaster. Evidence for thegem-diol as the reacting substrate.Bioorg. Chem. 17268.

    Google Scholar 

  • Eisses, K. Th., Schoonen, W. G. E. J., Aben, W., Scharloo, W., and Thörig, G. E. W. (1985). Dual function of the alcohol dehydrogenase ofDrosophila melanogaster: Ethanol and acetaldehyde oxidation by two allozymes ADH-71k and ADH-F.Mol. Gen. Genet. 19976.

    PubMed  Google Scholar 

  • Freriksen, A. (1992).Metabolic Physiology and Evolution of the Alcohol Dehydrogenase Gene-Enzyme System in Drosophila, Ph.D. thesis, University of Utrecht, Utrecht, The Netherlands.

    Google Scholar 

  • Freriksen, A., Seykens, D., Scharloo, W., and Heinstra, P. W. H. (1991). Alcohol dehydrogenase controls the flux from ethanol into lipids inDrosophila larvae: A13C NMR study.J. Biol. Chem. 26621399.

    PubMed  Google Scholar 

  • Geer, B. W., Heinstra, P. W. H., Kapoun, A. M., and Van der Zel, A. (1990). Alcohol dehydrogenase and alcohol tolerance inDrosophila melanogaster. In Barker, J. S. B., Starmer, W. T., and McIntyre, R. J. (eds.),Ecological and Evolutionary Genetics of Drosophila, Plenum Press, New York, p. 231.

    Google Scholar 

  • Hallam, S. E., Malpartida, F., and Hopwood, D. A. (1988). Nucleotide sequence, transcription and deduced function of a gene involved in polyketide antibiotic synthesis inStreptomyces coelicolor.Gene 74305.

    PubMed  Google Scholar 

  • Heinstra, P. W. H., and Geer, B. W. (1991). Metabolic control analysis and enzyme variation: Nutritional manipulation of the flux from ethanol to lipids inDrosophila.Mol. Biol. Evol. 8703.

    PubMed  Google Scholar 

  • Heinstra, P. W. H., Aben, W. J. M., Scharloo, W., and Thörig, G. E. W. (1986a). Alcohol dehydrogenase ofDrosophila melanogaster. Metabolic differences mediated through cryptic allozymes.Heredity 5723.

    PubMed  Google Scholar 

  • Heinstra, P. W. H., Scharloo, W., and Thörig, G. E. W. (1986b). Alcohol dehydrogenase ofDrosophila: Conversion and retroconversion of isozyme patterns.Comp. Biochem. Physiol. 83B409.

    Google Scholar 

  • Heinstra, P. W. H., Scharloo, W., and Thörig, G. E. W. (1987). Physiological significance of the alcohol dehydrogenase polymorphism ofDrosophila.Genetics 11775.

    PubMed  Google Scholar 

  • Heinstra, P. W. H., Thörig, G. E. W., Scharloo, W., Drenth, W., and Nolte, R. J. M. (1988). Kinetics and thermodynamics of ethanol oxidation catalyzed by genetic variants of the alcohol dehydrogenase fromDrosophila melanogaster andD. simulans.Biochim. Biophys. Acta 976224.

    Google Scholar 

  • Heinstra, P. W. H., Geer, B. W., Seykens, D., and Langevin, M. L. (1989). The metabolism of ethanol-derived acetaldehyde by alcohol dehydrogenase (EC 1.1.1.1) and aldehyde dehydrogenase (EC 1.2.1.3) inDrosophila melanogaster larvae.Biochem. J. 259791.

    PubMed  Google Scholar 

  • Hopwood, D. A. (1988). Towards an understanding of gene switching inStreptomyces, the basis of sporulation and antibiotic production.Proc. R. Soc. Lond. B 235121.

    PubMed  Google Scholar 

  • Hopwood, D. A., Bibb, M., Chater, K., Kieser, T., Bruton, C., Kieser, H. M., Lydiate, D., Smith, C., Ward, J., and Schrempf, H. (1985). InGenetic Manipulation of Streptomyces,a Laboratory Manual, The John Innes Foundation, Norwich, UK.

    Google Scholar 

  • Horinouchi, S., Malpartida, F., Hopwood, D. A., and Beppu, T. (1989).afsB stimulates transcription of the actinorhodin biosynthetic pathway inStreptomyces coelicolor A3(2) andS. lividans.Mol. Gen. Genet. 215355.

    Google Scholar 

  • Jörnvall, H., Persson, M., and Jeffrey, J. (1981). Alcohol and polyol dehydrogenases are both divided into two protein types, and structural properties cross-relate the different enzyme activities within each type.Proc. Natl. Acad. Sci. USA 784226.

    PubMed  Google Scholar 

  • Jörnvall, H., Persson, B., Krook, M., and Kaiser, R. (1990). Alcohol dehydrogenases.Biochem. Soc. Trans. 18169.

    PubMed  Google Scholar 

  • Kreitman, M. (1983). Nucleotide polymorphism at the alcohol dehydrogenase locus ofDrosophila melanogaster.Nature 304412.

    PubMed  Google Scholar 

  • Kreitman, M., and Hudson, R. R. (1991). Inferring the evolutionary histories of theAdh andAdh-dup loci inDrosophila melanogaster from patterns of polymorphism and divergence.Genetics 127565.

    PubMed  Google Scholar 

  • Kyte, J., and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein.J. Mol. Biol. 157105.

    PubMed  Google Scholar 

  • Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227680.

    PubMed  Google Scholar 

  • Laver, W. G., Air, G. M., Webster, R. G., and Smith-Gill, S. J. (1990). Epitopes on protein antigens: Misconceptions and realities.Cell 61553.

    PubMed  Google Scholar 

  • Magnolo, S. K., Leenuthaphong, D. L., DeModena, J. A., Curtis, J. E., Bailey, J. E., Galazzo, J. L., and Hughes, D. E. (1991). Actinorhodin production byStreptomyces coelicolor and growth ofStreptomyces lividans are improved by the expression of a bacterial hemoglobin.BIO/Technology 9473.

    PubMed  Google Scholar 

  • Marekov, L., Krook, M., and Jörnvall, H. (1990). Prokaryotic 20β-hydroxysteroid dehydrogenase is an enzyme of the “short-chain, non-metalloenzyme” alcohol dehydrogenase type.FEBS Lett. 26651.

    PubMed  Google Scholar 

  • Maser, E., Oppermann, U. C. T., Bannenberg, G., and Netter, K. J. (1992). Functional and immunological relationships between metyrapone reductase from mouse liver microsomes and 3α-hydroxysteroid dehydrogenase fromPseudomonas testosteroni.FEBS Lett. 297196.

    PubMed  Google Scholar 

  • McDonald, J. H., and Kreitman, M. (1991). Adaptive protein evolution at theAdh locus inDrosophila.Nature 351652.

    PubMed  Google Scholar 

  • Parmeggiani, A., and Swart, G. W. M. (1985). Mechanism of action of kirromycin-like antibiotics.Annu. Rev. Microbiol. 39557.

    PubMed  Google Scholar 

  • Pellequer, J. L., Westhof, E., and Van Regenmortel, M. H. V. (1991). Predicting location of continuous epitopes in proteins from their primary structures. In Langone, J. J. (ed.),Methods in Enzymology, Vol. 203 Academic Press, New York, p. 176.

    Google Scholar 

  • Persson, B., Krook, M., and Jörnvall, H. (1991). Characteristics of short-chain alcohol dehydrogenases and related enzymes.Eur. J. Biochem. 200537.

    PubMed  Google Scholar 

  • Place, A. R., Benyajati, C., and Sofer, W. (1987). Molecular consequences of two formaldehyde-induced mutations in the alcohol dehydrogenase gene ofDrosophila melanogaster.Biochem. Genet. 25621.

    PubMed  Google Scholar 

  • Rat, L., Veuille, M., and Lepesant, J.-A. (1991).Drosophila fat body protein P6 and alcohol dehydrogenase are derived from a common ancestral protein.J. Mol. Evol. 33194.

    PubMed  Google Scholar 

  • Schlaman, H. R. M., Horvath, B., Vijgenboom, E., Okker, R. J. H., and Lugtenberg, B. J. J. (1991). Suppression of nodulation gene expression in bacteroids ofRhizobium leguminosarum Biovar viciae.J. Bacteriol. 1734277.

    PubMed  Google Scholar 

  • Sullivan, D. T., Atkinson, P. W., and Starmer, W. T. (1990). Molecular evolution of the alcohol dehydrogenase genes in the genusDrosophila.Evol. Biol. 24107.

    Google Scholar 

  • Taylor, S. S., Rigby, P. W. J., and Hartley, B. S. (1974). Ribitol dehydrogenase formKlebsiella aerogenes.Biochem. J. 141693.

    PubMed  Google Scholar 

  • Thörig, G. E. W., Schoone, A. A., and Scharloo, W. (1975). Variation between electrophoretically identical alleles at the alcohol dehydrogenase locus inDrosophila melanogaster.Biochem. Genet. 13721.

    PubMed  Google Scholar 

  • Wills, C. (1976). Production of yeast alcohol dehydrogenase isozymes by selection.Nature 26126.

    PubMed  Google Scholar 

  • Winberg, J.-O., Thatcher, D. R., and McKinley-McKee, J. S. (1982). Alcohol dehydrogenase from the fruit fly,Drosophila melanogaster. Substrate specificity of the alleloenzymesAdh S andAdh UF.Biochim. Biophys. Acta 7047.

    PubMed  Google Scholar 

  • Zwiebel, L. J., Cohn, V. H., Wright, D. R., and Moore, G. P. (1982). Evolution of the single-copy DNA and the ADH gene in seven Drosophilids.J. Mol. Evol. 1962.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Ecology and Evolutionary Biology, Section of Evolutionary Genetics, University of Utrecht, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Astrid Freriksen & Pieter W. H. Heinstra

  2. Department of Biochemistry, Gorlaeus Laboratories, Leiden University, 2333 CC, Leiden, The Netherlands

    Pieter W. H. Heinstra

Authors
  1. Astrid Freriksen
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  2. Pieter W. H. Heinstra
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This research was supported by Grant 436-186 from the Foundation of Biological Research (BION), which is subsidized by the Netherlands Organization for Scientific Research (NWO).

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Freriksen, A., Heinstra, P.W.H. A novel ancestral protein ofDrosophila alcohol dehydrogenase inStreptomyces? . Biochem Genet 31, 393–407 (1993). https://doi.org/10.1007/BF00553457

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