Cloning of bovine prolactin cDNA and evolutionary implications of its sequence

Miller, W. L.; Coit, D.; Baxter, J. D.; Martial, Joseph

doi:10.1089/dna.1.1981.1.37

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Cloning of bovine prolactin cDNA and evolutionary implications of its sequence

Miller, W. L.; Coit, D.; Baxter, J. D. et al.

1981 • In DNA, 1 (1), p. 37-50

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https://hdl.handle.net/2268/26682

DOI
10.1089/dna.1.1981.1.37

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6299665

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Keywords :

Amino Acid Sequence; Animals; Base Sequence; Cattle; *Cloning, Molecular; DNA/*metabolism; DNA Restriction Enzymes; *Evolution; Humans; Prolactin/*genetics; Protein Biosynthesis; RNA, Messenger/genetics; Rabbits; Rats; Reticulocytes/metabolism; Species Specificity

Abstract :

[en] Prolactin, growth hormone, and chorionic somatomammotropin (placental lactogen) constitute a set of related polypeptides believed to derive from a common evolutionary ancestor protein. We have cloned and sequenced DNA complementary to the mRNA coding for bovine prolactin. This cDNA contains 702 bases corresponding to 10 amino acids in the leader peptide, all 199 amino acids of the hormone, and 75 nucleotides in the 3' untranslated region of the mRNA. Nucleotide sequence analysis of this cDNA permitted the identification of 10 amino acids in the signal peptide, plus the correction or elucidation of amino acid assignments at 16 sites where aspartic and glutamic acids had not been distinguished from their amides by amino acid sequencing. Codon usage in bovine prolactin mRNA is nonrandom, but, similarly to rat and human prolactins, it does not exhibit the strong preference for G or C in codon third positions seen in bovine, rat, and human growth hormone mRNAs. The translational termination signal in bovine prolactin in UAA, also the same as in rat and human prolactins and differing from the UAG "stop" codon used in bovine, rat, and human growth hormones and human chorionic somatomammotropin. The amino acid and mRNA nucleotide sequences of bovine, rat, and human prolactins and growth hormones were compared by several techniques based on various theories of molecular evolution. The comparison of prolactin to growth hormone is consistent in all three species, suggesting that the genes for these two hormones diverged about 350 million years ago. However, comparisons among the three prolactins or among the three growth hormones to determine the times of evolutionary divergence of the three species generated values that were inconsistent with each other and with the fossil record. Analysis of these discrepancies suggests that the genes for prolactin and growth hormone may now be evolving by different mechanisms.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Miller, W. L.

Coit, D.

Baxter, J. D.

Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Language :

English

Title :

Cloning of bovine prolactin cDNA and evolutionary implications of its sequence

Publication date :

1981

Journal title :

DNA

ISSN :

0198-0238

Publisher :

Mary Ann Liebert, Inc., New York, United States - New York

Volume :

Issue :

Pages :

37-50

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 26 October 2009

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Bibliography

ARNHEIM, N., KRYSTAL, M., SCHMICKEL, R., WILSON, G., RYDER, O., and ZIMMER, E. (1980). Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc. Natl. Acad. Sci. USA 77, 7323–7327.
AVIV, H. and LEDER, P. (1972). Purification of biologically active globin messenger RNA by chromatography on oligothy-midylic acid-cellulose. Proc. Natl. Acad. Sci. USA 69, 1408–1412.
BLUNDELL, T.L., and WOOD, S.P. (1975). Is the evolution of insulin Darwinian or due to selectively neutral mutation? Nature 257, 197–203.
CATT, K.J., MOFFAT, B., and NIALL, H.D. (1967). Human growth hormone and placental lactogen: Structural similarity. Science 157, 321.
CHIRGWIN, J.M., PRZYBYLA, A.E., MacDONALD, R.J., and RUTTER, W.J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294–5299.
CLARKE, B. (1970). Darwinian evolution of proteins. Science 168, 1009–1011.
COOKE, N.E., COIT, D., WEINER, R.I., BAXTER, J.D., and MARTIAL, J.A. (1980). Structure of cloned DNA complementary to rat prolactin messenger RNA. J. Biol. Chem. 255, 6502–6510.
COOKE, N.E., COIT, D., SHINE, J., BAXTER, J.D., and MARTIAL, J.A. (1981). Human prolactin: cDNA structural analysis and evolutionary comparisons. J. Biol. Chem. 256, 4006–4016.
DANNIES, P.S. and TASHJIAN, A.J., Jr. (1973). Effects of thyrotropin-releasing hormone and hydrocortisone on synthesis and degradation of prolactin in a rat pituitary cell strain. J. Biol. Chem. 248, 6174–6181.
DAYHOFF, M.O., SCHWARTZ, R.M., and ORCUTT, B.C. (1978). A model of evolutionary change in proteins. In Atlas of Protein Sequence and Structure, M.O. Dayhoff, Ed. (National Biomedical Research Foundation, Washington, D.C.) Vol. 5, Suppl. 3, pp. 345–352.
DUGAICZYK, A., BOYER, H.W., and GOODMAN, H.M. (1975). Ligation of Eco RI endonuclease-generated DNA fragments into linear and circular structures. J. Mol. Biol 96, 171–184.
EFSTRATIADIS, A., POSAKONY, J.W., MANIATIS, T., LAWN, R.M., O'CONNELL, C., SPRITZ, R.A., DE RIEL, J.K., FORGET, B.G., WEISSMAN, S.M., SLIGHTOM, J.L., BLECHL, A.E., SMITHIES, O., BARALLE, F.E., SHOULDERS, C.C., and PROUDFOOT, N.J. (1980). The structure and evolution of the human beta-globin gene family. Cell 21, 653–668.
FIDDES, J.C., SEEBURG, P.H., DE NOTO, F.M., HALLE-WELL, R.A., BAXTER, J.D., and GOODMAN, H.M. (1979). Structure of genes for human growth hormone and chorionic somatomammotropin. Proc. Natl. Acad. Sci. USA 76, 4294–4298.
FIERS, W., CONTRERAS, R., DUERINICK, F., HAEGEMAN, G., ISERENTANT, D., MERREGAERT, J., JOY, W.M., MOLEMANS, F., RAEMAEKERS, A., VAN DEN BERGHE, A., VOLKAERT, G., and YSEBAERT, M. (1976). Complete nucleotide sequence of bacteriophage MS2 RNA: Primary and secondary structure of the replicase gene. Nature 260, 500–507.
FITCH, W.M. (1974). The large extent of putative secondary nucleic acid structure in random nucleotide sequences or amino acid derived messenger RNA. J. Mol. Evol. 3, 279–291.
FITCH, W.M. (1976). Is there selection against wobble in codon-anticodon pairing? Science 194, 1173–1174.
GRUNSTEIN, M., and HOGNESS, D.D. (1975). Colony hybridization: A method for the isolation of cloned DNA's that contain a specific gene. Proc. Natl. Acad. Sci. USA 72, 3961–3965.
GUBBINS, E.J., MAURER, R.A., LAGRIMINI, M., ERWIN, C.R., and DONELSON, J.E. (1980). Structure of the rat prolactin gene. J. Biol. Chem. 255, 8655–8662.
HASEGAWA, M., YASUNAGA, T. and MIYATA, T. (1980). Secondary structure of MS2 phage RNA and bias in code word usage. Nucleic Acids Res. 7, 2073–2079.
HENSGENS, L.A.M., GRIVELL, L.A., BORST, P., and BOS, J.L. (1979). Nucleotide sequence of the mitochondrial structural gene for subunit 9 of yeast ATPase complex. Proc. Natl. Acad. Sci. USA 76, 1663–1667.
HOOD, L., CAMPBELL, J.H., and ELGIN, S.C.R. (1975). The organization, expression, and evolution of antibody genes and other multigene families. Ann. Rev. Genet. 9, 305–353.
KESSLER, S.W. (1976). Cell membrane antigen isolation with the staphylococcal protein A-antibody adsorbent. J. Immunol. 117, 1482–1490.
KIMURA, M. (1979). The neutral theory of molecular evolution. Sci. Am. 241, 98–126.
KIMURA, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120.
KIMURA, M. (1981). Estimation of evolutionary distances between homologous nucleotide sequences. Proc. Natl. Acad. Sci. USA 78, 454–458.
KRONENBERG, H.M., McDEVITT, B.E., MAJZOUB, J.A., NATHANS, J., SHARP, P.A., POTTS, J.T., and RICH, A. (1979). Cloning and nucleotide sequence of DNA coding for bovine preproparathyroid hormone. Proc. Natl. Acad. Sci. USA 76, 4981–4985.
LAEMMLI, U.K. (1970). Cleavage of structural proteins during the assembly of the heard of bacteriophage T4. Nature 227, 680–685.
LI, C.H., DIXON, J.S., LO, T.B., PANKOV, Y.M., and SCHMIDT, K.D. (1967). Amino acid sequence of ovine lactogenic hormone. Nature 224, 695–696.
LIEBHABER, S.A., GOOSSENS, M., and KAN, Y.W. (1981). Homology and concerted evolution at the alpha-1 and alpha-2 loci of human alpha globin. Nature 290, 26–29.
MARTIAL, J.A., HALLEWELL, R.A., BAXTER, J.D., and GOODMAN, H.M. (1979). Human growth hormone: Complementary DNA cloning and expression in bacteria. Science 205, 602–607.
MAXAM, A.M. and GILBERT, W. (1977). A new method for sequencing DNA. Proc. Natl. Acad. Sci. USA 74, 560–564.
MILLER, W.L. and McCARTHY, B.J. (1979). Gene expression in rfbrmal and regenerating mouse kidney. J. Biol. Chem. 254, 724–748.
MILLER, W.L., MARTIAL, J.A., and BAXTER, J.D. (1980a). Molecular cloning of DNA complementary to bovine growth hormone mRNA. J. Biol. Chem. 255, 7521–7524.
MILLER, W.L., THIRION, J.P., and MARTIAL, J.A. (1980b). Cloning of DNA complementary to bovine prolactin mRNA. Endocrinology 107, 851–854.
MILLER, W.L., JOHNSON, L.K., BAXTER, J.D., and ROBERTS, J.L. (1980c). Processing of the precursor to corticotropin and beta-lipotropin in man. Proc. Natl. Acad. Sci. USA 77,5211–5215.
MIYATA, T., MIYAZAWA, S. and YASUNAGA, T. (1979). Two types of amino substitutions in protein evolution. J. Mol. Evol. 12, 219–236.
NAKANISHI, S., INOUE, A., KITA, T., NAKAMURA, M., CHANG, A.C.Y., COHEN, S.N., and NUMA, S. (1979). Nucleotide sequence of cloned cDNA for bovine corticotropin-beta-lipotropin. Nature 278, 423–427.
NIALL, H.D., HOGAN, M.L., SAYER, R., ROSENBLUM, I.Y., and GREENWOOD, F.C. (1971). Sequences of pituitary and placental lactogenic and growth hormones: Evolution from a primordial peptide by gene duplication. Proc. Natl. Acad. Sci. USA 68, 866–869.
OWERBACH, D., RUTTER, W.J., MARTIAL, J.A., BAXTER, J.D., and SHOWS, T.B. (1980). Genes for growth hormone, chorionic somatomammotropin, and growth hormone-like gene on chromosome 17 in humans. Science 209, 289–292.
OWERBACH, D., RUTTER, W.J., COOKE, N.E., MARTIAL, J.A., and SHOWS, T.B. (1981). The prolactin gene is located on chromosome 6 in humans. Science 212, 815–816.
PARKS, J.S., HERD, J.E., and WURZEL, J.M. (1981). Human growth hormone (HGH) deficiency and polymorphism within the HGH and human placental lactogen (HPL) gene cluster. Pediatr. Res. 15, 513 (Abstract 437).
PELHAM, H.R.B., and JACKSON, R.J. (1976). An efficient mRNA-dependent translation system from reticulocyte lysates. Eur. J. Biochem. 67, 247–256.
PERLER, F., EFSTRATIADIS, A., LOMEDICO, P., GILBERT, W., KOLODNER, R., and DODGSON, J. (1980). The evolution of genes: The chicken proinsulin gene. Cell 20, 555–566.
PHILLIPS, J.A., PLOTNICK, L.P., SEEBURG, P.H., ZACH-MANN, M., THOMPSON, R.G., KOWARSKI, A.A., MIGEON, C.J., and BLIZZARD, R.M. (1981). Restriction endonuclease studies of inactive growth hormone genes. Pediatr. Res. 15, 567 (Abstract 750).
POST, L.E., STRYCHARZ, G.D., NOMURA, M., LEWIS, H. and DENNIS, P.P. (1979). Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc. Natl. Acad. Sci. USA 76, 1697–1701.
RICHMOND, R.C. (1970). Non-Darwinian evolution: A critique. Nature 225, 1025–1028.
ROYCHOUDHURY, R., JAY, E., and WU, R. (1976). Terminal labeling and addition of homopolymeric tracts to duplex DNA fragments by terminal deoxynucleotidyl transferase. Nucleic Acids Res. 3, 863–877.
SANGER, F., NICKLEN, S., and COULSON, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463–5467.
SEEBURG, P.H., SHINE, J., MARTIAL, J.A., ULLRICH, A., BAXTER, J.D., and GOODMAN, H.M. (1977a). Nucleotide sequence of part of the gene for human chorionic somatomammotropin: Purification of DNA complementary to predominant mRNA species. Cell 12, 157–165.
SEEBURG, P.H., SHINE, J., MARTIAL, J.A. BAXTER, J.D., and GOODMAN, H.M. (1977b). Nucleotide sequence and amplification in bacteria of the structural gene for rat growth hormone. Nature 270, 486–494.
SHERWOOD, L.M. (1967). Similarities in the chemical structure of human placental lactogen and pituitary growth hormone. Proc. Natl. Acad. Sci. USA 58, 2307–2314.
SHINE, J., SEEBURG, P.H., MARTIAL, J., BAXTER, J.D., and GOODMAN, H.M. (1977). Construction and analysis of recombinant DNA for human chorionic somatomammotropin. Nature 270, 494–499.
SOUTHERN, E.M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98,503–517.
SUEOKA, N. (1961). Variation and heterogeneity of base composition of deoxyribonucleic acids: A compilation of old and new data. J. Mol. Biol. 3, 31–40.
ULLRICH, A., SHINE, J., CHIRGWIN, J., PICTET, R., TISCHER, E., RUTTER, W.J., and GOODMAN, H.M. (1977). Rat insulin genes: Construction of plasmids containing the coding sequences. Science 196, 1313–1319.
VILLA-KOMAROFF, L., EFSTRATIADIS, A., BROOME, S., LOMEDICO, P., TIZARD, R., NABER, S.P., CHICK, W.L., and GILBERT, W. (1978). A bacterial clone synthesizing proinsulin. Proc. Natl. Acad. Sci. USA 75, 3727–3731.
WALLIS, M. (1974). The primary structure of bovine prolactin. FEBS Lett. 44, 205–207.
WILSON, A.C., CARLSON, S.S., and WHITE, T.J. (1977). Biochemical evolution. Annu. Rev. Biochem. 46, 573–639.
ZIMMER, E.A., MARTIN, S.L., BEVERLEY, S.M., KAN, Y.W., and WILSON, A.C. (1980). Rapid duplication and loss of genes coding for the apha-chains of hemoglobin. Proc. Natl. Acad. Sci. USA 77, 2158–2162.