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Proc Natl Acad Sci U S A. Mar 1, 1992; 89(5): 1799–1803.
PMCID: PMC48540

Evolutionary implications of the cDNA sequence of the single lactate dehydrogenase of a lamprey.

Abstract

All vertebrates other than lampreys exhibit multiple loci encoding lactate dehydrogenase +ADL-LDH; (S)-lactate:NAD+ oxidoreductase, EC 1.1.1.27+BD. Of these loci, Ldh-A is expressed predominantly in muscle, Ldh-B is expressed predominantly in heart, and Ldh-C (where present) exhibits different tissue-restricted patterns of expression depending on the taxon. To examine the relationship of the single LDH of lampreys to other vertebrate LDHs, we have determined the cDNA sequence of the LDH of the sea lamprey Petromyzon marinus and compared it to previously published sequences from bacteria, plants, and vertebrates. The lamprey sequence exhibits a mixture of features of both LDH-A and LDH-B at the amino acid level that may account for its intermediate kinetic properties. Both distance and maximum parsimony analyses strongly reject a relationship of lamprey LDH with mammalian LDH-C but do not significantly distinguish among remaining alternative phylogenetic hypotheses. Evolutionary parsimony analyses suggest that the lamprey LDH is related to Ldh-A and that the single locus condition has arisen as a result of the loss of Ldh-B (prior to the appearance of Ldh-C). The collection of LDH sequences for further studies of the evolution of the vertebrate LDH gene family will be facilitated by the PCR approach that we have used to obtain the lamprey sequence.

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  • Markert CL, Shaklee JB, Whitt GS. Evolution of a gene. Multiple genes for LDH isozymes provide a model of the evolution of gene structure, function and regulation. Science. 1975 Jul 11;189(4197):102–114. [PubMed]
  • Whitt GS. Genetic, developmental and evolutionary aspects of the lactate dehydrogenase isozyme system. Cell Biochem Funct. 1984 Jul;2(3):134–139. [PubMed]
  • Schär HP, Zuber H. Structure and function of L-lactate dehydrogenases from thermophilic and mesophilic bacteria. I) Isolation and characterization of lactate dehydrogenases from thermophilic and mesophilic bacilli. Hoppe Seylers Z Physiol Chem. 1979 Jul;360(7):795–807. [PubMed]
  • Hondred D, Hanson AD. Hypoxically inducible barley lactate dehydrogenase: cDNA cloning and molecular analysis. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7300–7304. [PMC free article] [PubMed]
  • Long GL. The stereospecific distribution and evolutionary significance of invertebrate lactate dehydrogenases. Comp Biochem Physiol B. 1976;55(1):77–83. [PubMed]
  • WILSON AC, KAPLAN NO, LEVINE L, PESCE A, REICHLIN M, ALLISON WS. EVOLUTION OF LACTIC DEHYDROGENASES. Fed Proc. 1964 Nov-Dec;23:1258–1266. [PubMed]
  • Markert CL. Lactate dehydrogenase. Biochemistry and function of lactate dehydrogenase. Cell Biochem Funct. 1984 Jul;2(3):131–134. [PubMed]
  • Hendriks W, Mulders JW, Bibby MA, Slingsby C, Bloemendal H, de Jong WW. Duck lens epsilon-crystallin and lactate dehydrogenase B4 are identical: a single-copy gene product with two distinct functions. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7114–7118. [PMC free article] [PubMed]
  • Millan JL, Driscoll CE, LeVan KM, Goldberg E. Epitopes of human testis-specific lactate dehydrogenase deduced from a cDNA sequence. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5311–5315. [PMC free article] [PubMed]
  • Li SS, Fitch WM, Pan YC, Sharief FS. Evolutionary relationships of vertebrate lactate dehydrogenase isozymes A4 (muscle), B4 (heart), and C4 (testis). J Biol Chem. 1983 Jun 10;258(11):7029–7032. [PubMed]
  • Baldwin J, Lake PS, Moon TW. Immunochemical evidence that the single lactate dehydrogenase of lampreys is more similar to LDHB4 than to LDHA4 of hagfish. J Exp Zool. 1987 Jan;241(1):1–8. [PubMed]
  • Crawford DL, Constantino HR, Powers DA. Lactate dehydrogenase-B cDNA from the teleost Fundulus heteroclitus: evolutionary implications. Mol Biol Evol. 1989 Jul;6(4):369–383. [PubMed]
  • Hiraoka BY, Sharief FS, Yang YW, Li WH, Li SS. The cDNA and protein sequences of mouse lactate dehydrogenase B. Molecular evolution of vertebrate lactate dehydrogenase genes A (muscle), B (heart) and C (testis). Eur J Biochem. 1990 Apr 30;189(2):215–220. [PubMed]
  • Dell'Agata M, Pannunzio G, Teichner A, Ferracin A. Lactate dehydrogenase from Lampetra planeri is composed of chains of unique type which show intermediate properties between the heart and the muscle isozymes of vertebrates. Comp Biochem Physiol B. 1988;89(2):323–327. [PubMed]
  • Loening UE. The fractionation of high-molecular-weight ribonucleic acid by polyacrylamide-gel electrophoresis. Biochem J. 1967 Jan;102(1):251–257. [PMC free article] [PubMed]
  • MacDonald RJ, Swift GH, Przybyla AE, Chirgwin JM. Isolation of RNA using guanidinium salts. Methods Enzymol. 1987;152:219–227. [PubMed]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [PubMed]
  • Minowa T, Iwata S, Sakai H, Masaki H, Ohta T. Sequence and characteristics of the Bifidobacterium longum gene encoding L-lactate dehydrogenase and the primary structure of the enzyme: a new feature of the allosteric site. Gene. 1989 Dec 21;85(1):161–168. [PubMed]
  • Ono M, Matsuzawa H, Ohta T. Nucleotide sequence and characteristics of the gene for L-lactate dehydrogenase of Thermus aquaticus YT-1 and the deduced amino acid sequence of the enzyme. J Biochem. 1990 Jan;107(1):21–26. [PubMed]
  • Kunai K, Machida M, Matsuzawa H, Ohta T. Nucleotide sequence and characteristics of the gene for L-lactate dehydrogenase of Thermus caldophilus GK24 and the deduced amino-acid sequence of the enzyme. Eur J Biochem. 1986 Oct 15;160(2):433–440. [PubMed]
  • Hensel R, Mayr U, Yang CY. The complete primary structure of the allosteric L-lactate dehydrogenase from Lactobacillus casei. Eur J Biochem. 1983 Aug 15;134(3):503–511. [PubMed]
  • Hediger MA, Frank G, Zuber H. Structure and function of L-lactate dehydrogenases from thermophilic and mesophilic bacteria, IV. The primary structure of the mesophilic lactate dehydrogenase from Bacillus subtilis. Biol Chem Hoppe Seyler. 1986 Sep;367(9):891–903. [PubMed]
  • Waldvogel S, Weber H, Zuber H. Structure and function of L-lactate dehydrogenases from thermophilic and mesophilic bacteria. VII. Nucleotide sequence of the lactate dehydrogenase gene from the mesophilic bacterium Bacillus megaterium. Preparation and properties of a hybrid lactate dehydrogenase comprising moieties of the B. megaterium and B. stearothermophilus enzymes. Biol Chem Hoppe Seyler. 1987 Oct;368(10):1391–1399. [PubMed]
  • Zülli F, Weber H, Zuber H. Structure and function of L-lactate dehydrogenases from thermophilic and mesophilic bacteria, VI. Nucleotide sequences of lactate dehydrogenase genes from the thermophilic bacteria Bacillus stearothermophilus, B. caldolyticus and B. caldotenax. Biol Chem Hoppe Seyler. 1987 Sep;368(9):1167–1177. [PubMed]
  • Barstow DA, Murphy JP, Sharman AF, Clarke AR, Holbrook JJ, Atkinson T. Amino acid sequence of the L-lactate dehydrogenase of Bacillus caldotenax deduced from the nucleotide sequence of the cloned gene. Eur J Biochem. 1987 Jun 15;165(3):581–586. [PubMed]
  • Taylor SS. Amino acid sequence of dogfish muscle lactate dehydrogenase. J Biol Chem. 1977 Mar 10;252(5):1799–1806. [PubMed]
  • Hirota Y, Katsumata A, Takeya T. Nucleotide and deduced amino acid sequences of chicken lactate dehydrogenase-A. Nucleic Acids Res. 1990 Nov 11;18(21):6432–6432. [PMC free article] [PubMed]
  • Ishiguro N, Osame S, Kagiya R, Ichijo S, Shinagawa M. Primary structure of bovine lactate dehydrogenase-A isozyme and its synthesis in Escherichia coli. Gene. 1990 Jul 16;91(2):281–285. [PubMed]
  • Kiltz HH, Keil W, Griesbach M, Petry K, Meyer H. The primary structure of porcine lactate dehydrogenase: isoenzymes M4 and H4. Hoppe Seylers Z Physiol Chem. 1977 Jan;358(1):123–127. [PubMed]
  • Sass C, Briand M, Benslimane S, Renaud M, Briand Y. Characterization of rabbit lactate dehydrogenase-M and lactate dehydrogenase-H cDNAs. Control of lactate dehydrogenase expression in rabbit muscle. J Biol Chem. 1989 Mar 5;264(7):4076–4081. [PubMed]
  • Tsujibo H, Tiano HF, Li SS. Nucleotide sequences of the cDNA and an intronless pseudogene for human lactate dehydrogenase-A isozyme. Eur J Biochem. 1985 Feb 15;147(1):9–15. [PubMed]
  • Sakai I, Sharief FS, Pan YC, Li SS. The cDNA and protein sequences of human lactate dehydrogenase B. Biochem J. 1987 Dec 15;248(3):933–936. [PMC free article] [PubMed]
  • Fukasawa KM, Li SS. Complete nucleotide sequence of the mouse lactate dehydrogenase-A functional gene: comparison of the exon-intron organization of dehydrogenase genes. Genetics. 1987 May;116(1):99–105. [PMC free article] [PubMed]
  • Pan YC, Sharief FS, Okabe M, Huang S, Li SS. Amino acid sequence studies on lactate dehydrogenase C4 isozymes from mouse and rat testes. J Biol Chem. 1983 Jun 10;258(11):7005–7016. [PubMed]
  • Sakai I, Sharief FS, Li SS. Molecular cloning and nucleotide sequence of the cDNA for sperm-specific lactate dehydrogenase-C from mouse. Biochem J. 1987 Mar 1;242(2):619–622. [PMC free article] [PubMed]
  • Matrisian LM, Rautmann G, Magun BE, Breathnach R. Epidermal growth factor or serum stimulation of rat fibroblasts induces an elevation in mRNA levels for lactate dehydrogenase and other glycolytic enzymes. Nucleic Acids Res. 1985 Feb 11;13(3):711–726. [PMC free article] [PubMed]
  • Feng DF, Doolittle RF. Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol. 1987;25(4):351–360. [PubMed]
  • Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. [PubMed]
  • Lake JA. A rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol Biol Evol. 1987 Mar;4(2):167–191. [PubMed]
  • Eventoff W, Rossmann MG, Taylor SS, Torff HJ, Meyer H, Keil W, Kiltz HH. Structural adaptations of lactate dehydrogenase isozymes. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2677–2681. [PMC free article] [PubMed]
  • Grau UM, Trommer WE, Rossmann MG. Structure of the active ternary complex of pig heart lactate dehydrogenase with S-lac-NAD at 2.7 A resolution. J Mol Biol. 1981 Sep 15;151(2):289–307. [PubMed]
  • Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. [PubMed]
  • Edwards YH, Povey S, LeVan KM, Driscoll CE, Millan JL, Goldberg E. Locus determining the human sperm-specific lactate dehydrogenase, LDHC, is syntenic with LDHA. Dev Genet. 1987;8(4):219–232. [PubMed]
  • Kanno T, Sudo K, Kitamura M, Miwa S, Ichiyama A, Nishimura Y. Lactate dehydrogenase A-subunit and B-subunit deficiencies: comparison of the physiological roles of LDH isozymes. Isozymes Curr Top Biol Med Res. 1983;7:131–150. [PubMed]
  • Zuckerkandl E. Multilocus enzymes, gene regulation, and genetic sufficiency. J Mol Evol. 1978 Oct 27;12(1):57–89. [PubMed]
  • Sidell BD, Beland KF. Lactate dehydrogenases of Atlantic hagfish: physiological and evolutionary implications of a primitive heart isozyme. Science. 1980 Feb 15;207(4432):769–770. [PubMed]

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