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. 1989 Jul;86(14):5454–5458. doi: 10.1073/pnas.86.14.5454

Cloning and sequencing of cDNA encoding baboon liver alcohol dehydrogenase: evidence for a common ancestral lineage with the human alcohol dehydrogenase beta subunit and for class I ADH gene duplications predating primate radiation.

A E Trezise 1, E A Godfrey 1, R S Holmes 1, I R Beacham 1
PMCID: PMC297641  PMID: 2748595

Abstract

The baboon has at least five alcohol dehydrogenases (ADH; alcohol:NAD+ oxidoreductase, EC 1.1.1.1) and has distinct liver and kidney class I isozymes. A rat liver class I ADH partial cDNA was used to screen a baboon liver cDNA library. A cDNA clone was isolated and sequenced and found to contain the entire coding region for baboon liver ADH, 12 nucleotides of the 5' noncoding region, and 256 nucleotides of the 3' noncoding region. The amino acid sequence deduced from this cDNA most closely resembles that of human liver ADH beta subunit (ADH-beta): 363 of 374 residues were identical. This suggested that baboon liver class I ADH is of the same ancestral lineage as the human ADH-beta. In contrast to human liver, only a single ADH-beta transcript is observed in baboon liver. A comparison of human and baboon ADH 3' noncoding regions suggests that a single nucleotide change in a polyadenylylation signal consensus sequence may, in part, be responsible for the generation of ADH-beta transcripts with variable-length 3' ends in human liver. A nucleotide substitution rate of 0.5 x 10(-9) substitutions per site per year for primate class I ADH genes was deduced from the data, which suggests that the alpha-beta gamma separation of human ADH genes occurred about 60 million years ago, and that primate class I ADH gene duplications predated primate radiation.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Algar E. M., Seeley T. L., Holmes R. S. Purification and molecular properties of mouse alcohol dehydrogenase isozymes. Eur J Biochem. 1983 Dec 1;137(1-2):139–147. doi: 10.1111/j.1432-1033.1983.tb07807.x. [DOI] [PubMed] [Google Scholar]
  2. Bantle J. A., Maxwell I. H., Hahn W. E. Specificity of oligo (dT)-cellulose chromatography in the isolation of polyadenylated RNA. Anal Biochem. 1976 May 7;72:413–427. doi: 10.1016/0003-2697(76)90549-2. [DOI] [PubMed] [Google Scholar]
  3. Berger S. L., Birkenmeier C. S. Inhibition of intractable nucleases with ribonucleoside--vanadyl complexes: isolation of messenger ribonucleic acid from resting lymphocytes. Biochemistry. 1979 Nov 13;18(23):5143–5149. doi: 10.1021/bi00590a018. [DOI] [PubMed] [Google Scholar]
  4. Berget S. M. Are U4 small nuclear ribonucleoproteins involved in polyadenylation? Nature. 1984 May 10;309(5964):179–182. doi: 10.1038/309179a0. [DOI] [PubMed] [Google Scholar]
  5. Bosron W. F., Li T. K., Dafeldecker W. P., Vallee B. L. Human liver pi-alcohol dehydrogenase: kinetic and molecular properties. Biochemistry. 1979 Mar 20;18(6):1101–1105. doi: 10.1021/bi00573a026. [DOI] [PubMed] [Google Scholar]
  6. Bühler R., Hempel J., Kaiser R., de Zalenski C., von Wartburg J. P., Jörnvall H. Human liver alcohol dehydrogenase. 2. The primary structure of the gamma 1 protein chain. Eur J Biochem. 1984 Dec 17;145(3):447–453. doi: 10.1111/j.1432-1033.1984.tb08575.x. [DOI] [PubMed] [Google Scholar]
  7. Ceci J. D., Zheng Y. W., Felder M. R. Molecular analysis of mouse alcohol dehydrogenase: nucleotide sequence of the Adh-1 gene and genetic mapping of a related nucleotide sequence to chromosome 3. Gene. 1987;59(2-3):171–182. doi: 10.1016/0378-1119(87)90325-8. [DOI] [PubMed] [Google Scholar]
  8. Crabb D. W., Edenberg H. J. Complete amino acid sequence of rat liver alcohol dehydrogenase deduced from the cDNA sequence. Gene. 1986;48(2-3):287–291. doi: 10.1016/0378-1119(86)90087-9. [DOI] [PubMed] [Google Scholar]
  9. Duester G., Hatfield G. W., Bühler R., Hempel J., Jörnvall H., Smith M. Molecular cloning and characterization of a cDNA for the beta subunit of human alcohol dehydrogenase. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4055–4059. doi: 10.1073/pnas.81.13.4055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Edenberg H. J., Zhang K., Fong K., Bosron W. F., Li T. K. Cloning and sequencing of cDNA encoding the complete mouse liver alcohol dehydrogenase. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2262–2266. doi: 10.1073/pnas.82.8.2262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eklund H., Horjales E., Vallee B. L., Jörnvall H. Computer-graphics interpretations of residue exchanges between the alpha, beta and gamma subunits of human-liver alcohol dehydrogenase class I isozymes. Eur J Biochem. 1987 Sep 1;167(2):185–193. doi: 10.1111/j.1432-1033.1987.tb13322.x. [DOI] [PubMed] [Google Scholar]
  12. Eklund H., Nordström B., Zeppezauer E., Söderlund G., Ohlsson I., Boiwe T., Söderberg B. O., Tapia O., Brändén C. I., Akeson A. Three-dimensional structure of horse liver alcohol dehydrogenase at 2-4 A resolution. J Mol Biol. 1976 Mar 25;102(1):27–59. doi: 10.1016/0022-2836(76)90072-3. [DOI] [PubMed] [Google Scholar]
  13. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  14. Hedén L. O., Hög J. O., Larsson K., Lake M., Lagerholm E., Holmgren A., Vallee B. L., Jörnvall H., von Bahr-Lindström H. cDNA clones coding for the beta-subunit of human liver alcohol dehydrogenase have differently sized 3'-non-coding regions. FEBS Lett. 1986 Jan 6;194(2):327–332. doi: 10.1016/0014-5793(86)80111-9. [DOI] [PubMed] [Google Scholar]
  15. Hempel J., Bühler R., Kaiser R., Holmquist B., de Zalenski C., von Wartburg J. P., Vallee B., Jörnvall H. Human liver alcohol dehydrogenase. 1. The primary structure of the beta 1 beta 1 isoenzyme. Eur J Biochem. 1984 Dec 17;145(3):437–445. doi: 10.1111/j.1432-1033.1984.tb08573.x. [DOI] [PubMed] [Google Scholar]
  16. Hempel J., Holmquist B., Fleetwood L., Kaiser R., Barros-Söderling J., Bühler R., Vallee B. L., Jörnvall H. Structural relationships among class I isozymes of human liver alcohol dehydrogenase. Biochemistry. 1985 Sep 24;24(20):5303–5307. doi: 10.1021/bi00341a005. [DOI] [PubMed] [Google Scholar]
  17. Holmes R. S., Courtney Y. R., VandeBerg J. L. Alcohol dehydrogenase isozymes in baboons: tissue distribution, catalytic properties, and variant phenotypes in liver, kidney, stomach, and testis. Alcohol Clin Exp Res. 1986 Dec;10(6):623–630. doi: 10.1111/j.1530-0277.1986.tb05157.x. [DOI] [PubMed] [Google Scholar]
  18. Hög J. O., Hedén L. O., Larsson K., Jörnvall H., von Bahr-Lindström H. The gamma 1 and gamma 2 subunits of human liver alcohol dehydrogenase. cDNA structures, two amino acid replacements, and compatibility with changes in the enzymatic properties. Eur J Biochem. 1986 Sep 1;159(2):215–218. doi: 10.1111/j.1432-1033.1986.tb09855.x. [DOI] [PubMed] [Google Scholar]
  19. Hög J. O., von Bahr-Lindström H., Hedén L. O., Holmquist B., Larsson K., Hempel J., Vallee B. L., Jörnvall H. Structure of the class II enzyme of human liver alcohol dehydrogenase: combined cDNA and protein sequence determination of the pi subunit. Biochemistry. 1987 Apr 7;26(7):1926–1932. doi: 10.1021/bi00381a021. [DOI] [PubMed] [Google Scholar]
  20. Ikuta T., Fujiyoshi T., Kurachi K., Yoshida A. Molecular cloning of a full-length cDNA for human alcohol dehydrogenase. Proc Natl Acad Sci U S A. 1985 May;82(9):2703–2707. doi: 10.1073/pnas.82.9.2703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ikuta T., Szeto S., Yoshida A. Three human alcohol dehydrogenase subunits: cDNA structure and molecular and evolutionary divergence. Proc Natl Acad Sci U S A. 1986 Feb;83(3):634–638. doi: 10.1073/pnas.83.3.634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jörnvall H., Hempel J., Vallee B. L., Bosron W. F., Li T. K. Human liver alcohol dehydrogenase: amino acid substitution in the beta 2 beta 2 Oriental isozyme explains functional properties, establishes an active site structure, and parallels mutational exchanges in the yeast enzyme. Proc Natl Acad Sci U S A. 1984 May;81(10):3024–3028. doi: 10.1073/pnas.81.10.3024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jörnvall H., Hempel J., von Bahr-Lindström H., Hög J. O., Vallee B. L. Alcohol and aldehyde dehydrogenases: structures of the human liver enzymes, functional properties and evolutionary aspects. Alcohol Alcohol Suppl. 1987;1:13–23. [PubMed] [Google Scholar]
  24. Koop B. F., Goodman M., Xu P., Chan K., Slightom J. L. Primate eta-globin DNA sequences and man's place among the great apes. Nature. 1986 Jan 16;319(6050):234–238. doi: 10.1038/319234a0. [DOI] [PubMed] [Google Scholar]
  25. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Li T. K., Magnes L. J. Identification of a distinctive molecular form of alcohol dehydrogenase in human livers with high activity. Biochem Biophys Res Commun. 1975 Mar 3;63(1):202–208. doi: 10.1016/s0006-291x(75)80030-1. [DOI] [PubMed] [Google Scholar]
  27. Lieber C. S., DeCarli L. M. The feeding of alcohol in liquid diets: two decades of applications and 1982 update. Alcohol Clin Exp Res. 1982 Fall;6(4):523–531. doi: 10.1111/j.1530-0277.1982.tb05017.x. [DOI] [PubMed] [Google Scholar]
  28. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  30. Nomura F., Pikkarainen P. H., Jauhonen P., Arai M., Gordon E. R., Baraona E., Lieber C. S. Effect of ethanol administration on the metabolism of ethanol in baboons. J Pharmacol Exp Ther. 1983 Oct;227(1):78–83. [PubMed] [Google Scholar]
  31. Noyes B. E., Mevarech M., Stein R., Agarwal K. L. Detection and partial sequence analysis of gastrin mRNA by using an oligodeoxynucleotide probe. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1770–1774. doi: 10.1073/pnas.76.4.1770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Parés X., Vallee B. L. New human liver alcohol dehydrogenase forms with unique kinetic characteristics. Biochem Biophys Res Commun. 1981 Jan 15;98(1):122–130. doi: 10.1016/0006-291x(81)91878-7. [DOI] [PubMed] [Google Scholar]
  33. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  34. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith M., Hopkinson D. A., Harris H. Developmental changes and polymorphism in human alcohol dehydrogenase. Ann Hum Genet. 1971 Feb;34(3):251–271. doi: 10.1111/j.1469-1809.1971.tb00238.x. [DOI] [PubMed] [Google Scholar]
  36. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weinberg R. A., Warnaar S. O., Winocour E. Isolation and characterization of simian virus 40 ribonucleic acid. J Virol. 1972 Aug;10(2):193–201. doi: 10.1128/jvi.10.2.193-201.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Woo S. L. A sensitive and rapid method for recombinant phage screening. Methods Enzymol. 1979;68:389–395. doi: 10.1016/0076-6879(79)68028-x. [DOI] [PubMed] [Google Scholar]
  39. Yokoyama S., Yokoyama R. Molecular evolution of mammalian class I alcohol dehydrogenase. Mol Biol Evol. 1987 Sep;4(5):504–513. doi: 10.1093/oxfordjournals.molbev.a040459. [DOI] [PubMed] [Google Scholar]
  40. von Bahr-Lindström H., Hög J. O., Hedén L. O., Kaiser R., Fleetwood L., Larsson K., Lake M., Holmquist B., Holmgren A., Hempel J. cDNA and protein structure for the alpha subunit of human liver alcohol dehydrogenase. Biochemistry. 1986 May 6;25(9):2465–2470. doi: 10.1021/bi00357a026. [DOI] [PubMed] [Google Scholar]

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