Summary
The complete 129-amino-acid sequences of two rainbow trout lysozymes (I and II) isolated from kidney were established using protein chemistry microtechniques. The two sequences differ only at position 86, I having aspartic acid and II having alanine. A cDNA clone coding for rainbow trout lysozyme was isolated from a cDNA library made from liver mRNA. Sequencing of the cloned cDNA insert, which was 1 kb in length, revealed a 432-bp open reading frame encoding an amino-terminal peptide of 15 amino acids and a mature enzyme of 129 amino acids identical in sequence to II. Forms I and II from kidney and liver were also analyzed using enzymatic amplification via PCR and direct sequencing; both organs contain mRNA encoding the two lysozymes. Evolutionary trees relating DNA sequences coding for lysozymesc and α-lactalbumins provide evidence that the gene duplication giving rise to conventional vertebrate lysozymesc and to lactalbumin preceded the divergence of fishes and tetrapods about 400 Myr ago. Evolutionary analysis also suggests that amino acid replacements may have accumulated more slowly on the lineage leading to fish lysozyme than on those leading to mammal and bird lysozymes.
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Abbreviations
- cDNA:
-
complementary DNA
- Myr:
-
million years
- SSC:
-
150 mM sodium chloride, 15 mM sodium citrate pH 7.0
- PCR:
-
polymerase chain reaction
References
Aviv H, Leder P (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acidcellulose. Proc Natl Acad Sci USA 69:1408–1412
Brand SJ, Fuller PJ (1988) Differential gastrin gene expression in rat gastrointestinal tract and pancreas during neonatal development. J Biol Chem 263:5341–5347
Chen EY, Seeburg PH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170
Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299
Crestfield AM, Moore S, Stein WH (1963) The preparation and enzymatic hydrolysis of reduced and S-carboxymethylated proteins. J Biol Chem 238:622–627
Cross M, Renkawitz R (1990) Repetitive sequence involvement in the duplication and divergence of mouse lysozyme genes. EMBO J 9:1283–1288
Doherty PJ, Huesca-Contreras M, Dosch HM, Pan S (1989) Rapid amplification of complementary DNA from small amounts of unfractionated RNA. Anal Biochem 177:7–10
Duckworth ML, Gait MJ, Goelet P, Hong GF, Singh M, Titmas RC (1981) Rapid synthesis of oligodeoxyribonucleotides VI. Efficient, mechanised synthesis of heptadecadeoxyribonucleotides by an improved solid phase phosphotriester route. Nucleic Acids Res 9:1691–1706
Godovac-Zimmermann J, Conti A, Napolitano L (1988) The primary structure of donkey (Equus asinus) lysozyme contains the Ca(II) binding site of α-lactalbumin. Biol Chem Hoppe-Seyler 369:1109–1115
Grinde B, Jollès J, Jollès P (1988) Purification and characterization of two lysozymes from rainbow trout (Salmo gairdneri). Eur J Biochem 173:269–273
Gubler U, Hoffman BJ (1983) A simple and very efficient method for generating cDNA libraries. Gene 25:263–269
Higuchi R, von Beroldingen CH, Sensabaugh GF, Erlich HA (1988) DNA typing from single hairs. Nature 332:543–546
Irwin DM, Wilson AC (1989) Multiple cDNA sequences and the evolution of bovine stomach lysozyme. J Biol Chem 264: 11387–11393
Irwin DM, Wilson AC (1990) Concerted evolution of ruminant stomach lysozymes. Characterization of lysozyme cDNA clones from sheep and deer. J Biol Chem 265:4944–4952
Jollès J, Van Leemputten E, Mouton A, Jollès P (1972) Amino acid sequence of guinea-hen egg-white lysozyme. Biochim Biophys Acta 257:497–510
Jollès J, Jollès P, Bowman BH, Prager EM, Stewart C-B, Wilson AC (1989) Episodic evolution in the stomach lysozymes of ruminants. J Mol Evol 28:528–535
Jollès J, Prager EM, Alnemri ES, Jollès P, Ibrahimi IM, Wilson AC (1990) Amino acid sequences of stomach and nonstomach lysozymes of ruminants. J Mol Evol 30:370–382
Jollès P (1976) A possible physiological function of lysozyme. Biomédecine 25:275–276
Jollès P, Jollès J (1984) What's new in lysozyme research? Mol Cell Biochem 63:165–189
Kitagawa Y, Tsunasawa S, Tanaka N, Katsube Y, Sakiyama F, Asada K (1986) Amino acid sequence of coppper, zinc-superoxide dismutase from spinach leaves. J Biochem 99:1289–1298
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor NY
Nitta K, Sugai S (1989) The evolution of lysozyme and α-lactalbumin. Eur J Biochem 182:111–118
Prager EM, Wilson AC (1988) Ancient origin of lactalbumin from lysozyme: analysis of DNA and amino acid sequences. J Mol Evol 27:326–335
Reinisch CL, Litman GW (1989) Evolutionary immunobiology. Immunology Today 10:278–281
Rodríguez R, Menéndez-Arias L, González de Buitrago G, Gavilanes JG (1987) Structure of the pigeon lysozyme and its relationship with other typec lysozymes. Comp Biochem Physiol 88B:791–796
Romer AS (1966) Vertebrate paleontology, ed 3. University of Chicago Press, Chicago IL
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Stewart C-B, Schilling JW, Wilson AC (1987) Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature 330:401–404
von Heijne G (1985) Signal sequences. The limits of variation. J Mol Biol 184:99–105
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Dautigny, A., Prager, E.M., Pham-Dinh, D. et al. cDNA and amino acid sequences of rainbow trout (Oncorhynchus mykiss) lysozymes and their implications for the evolution of lysozyme and lactalbumin. J Mol Evol 32, 187–198 (1991). https://doi.org/10.1007/BF02515392
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DOI: https://doi.org/10.1007/BF02515392