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Sequence similarities of the protamine genes: Implications for regulation and evolution

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Summary

With the recent availability of the primary structural data for the trout, bovine, and mouse protamine genes, a detailed comparison of their structures has been made. This has revealed extensive conservation of potentially biologically significant regions. An inverse correlation is apparent between gene copy number and the number of sequence-distinct protamines synthesized with the number of CP-box-like (CCYPCCC) putative transcription modulating sequences situated 5′ to these genes. A common nucleotide sequence 5′ to the CP-box-like putative transcription modulating sequence(s) at the end of a common region has been identified. It is postulated that this is the testis-specific protamine P1 transcription regulator sequence. Evidence based on sequence similarity is also provided for the existence of a primordial protamine gene and a scheme for the evolution of vertebrate protamine genes is proposed.

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References

  • Aiken JM, McKenzie D, Zhao HZ, States JC, Dixon GH (1983) Sequence homologies in the protamine gene family of rainbow trout. Nucleic Acids Res 11:4907–4992

    PubMed  Google Scholar 

  • Altman S, Model P, Dixon GH, Wosnick MA (1981) AnE. coli gene coding for a protamine-like protein. Cell 26:299–304

    PubMed  Google Scholar 

  • Bellvé AR, McKay DJ, Renaux BS, Dixon GH (1988) Purification and characterization of mouse protamines P1 and P2. Amino acid sequence of P2. Biochemistry 27:2890–2897

    PubMed  Google Scholar 

  • Berlot-Picard F, Vodjdani G, Doly J (1986) Nucleotide sequence of a cDNA clone encodingScylliorhinus caniculus protamine Z2. Eur J Biochem 160:305–310

    PubMed  Google Scholar 

  • Bionet (1987) IntelliGenetics Inc. core programs SEQ and IFIWD version 5.1

  • Bloch DP (1969) A catalog of sperm histones. Genetics (Suppl) 61:93–111

    PubMed  Google Scholar 

  • Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    PubMed  Google Scholar 

  • Clayton J, Kedes L (1982) GEL, a DNA sequencing project management system. Nucleic Acids Res 10:305–321

    PubMed  Google Scholar 

  • Dayhoff M (1978) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Silver Spring MD

    Google Scholar 

  • Dingwall C, Laskey RA (1986) Protein import into the cell nucleus. Annu Rev Cell Biol 2:367–390

    PubMed  Google Scholar 

  • Dixon GH, Aiken JM, Jankowski JM, McKenzie DI, Moir R, States JC (1986) Organization and evolution of the protamine genes of salmonid fishes. In: Reeck GR, Goodwin GA, Puigdomenech P (eds) Chromosomal proteins and gene expression. Plenum, New York, pp 287–314

    Google Scholar 

  • Dynan WS, Tjian R (1985) Control of eucaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316:774–778

    PubMed  Google Scholar 

  • Fitch WM, Langley CH (1976) Protein evolution and the molecular clock. Fed Proc 35:2092–2097

    PubMed  Google Scholar 

  • Galibert F, Chen TN, Mandart E (1982) Nucleotide sequence of a cloned woodchuck hepatitis virus genome: comparison with the hepatitis b virus sequence. J Virol 41:51–65

    PubMed  Google Scholar 

  • Gedamu L, Davies PL, Dixon GH (1977) Identification and isolation of protamine messenger ribonucleoprotein particles from rainbow trout testis. Biochemistry 16:1383–1391

    PubMed  Google Scholar 

  • GenBank (1987) The Los Alamos National Laboratory Release 52. Bilofsky HS, Burks C, Fickett JW, Goad WB, Lewitter FI, Rindone WP, Swindell CD, Tung CS (1986) The GenBank (R) genetic sequence database. Nucleic Acids Res 14:1–4. Burks C, Fickett JW, Goad WB, Kanehisa M, Lewitter FI, Rindone WP, Swindell CD, Bilofsky HS (1985) The GenBank nucleic acid sequence database. Computer Applications in the Biosciences 1:225–233

  • Iatrou K, Spira AW, Dixon GH (1978) Protamine messenger RNA: evidence for early synthesis and accumulation during spermatogenesis in rainbow trout. Dev Biol 64:82–98

    PubMed  Google Scholar 

  • Jankowski JM, States JC, Dixon GH (1986) Evidence of sequences resembling avian retrovirus long terminal repeats flanking the trout protamine gene. J Mol Evol 23:1–10

    PubMed  Google Scholar 

  • Kleene KC, Distel RJ, Hecht NB (1984) Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev Biol 105:71–91

    PubMed  Google Scholar 

  • Kleene KC, Distel RJ, Hecht NB (1985) Nucleotide sequence of a cDNA clone encoding mouse protamine 1. Biochemistry 24:719–722

    PubMed  Google Scholar 

  • Krawetz SA, Connor W, Dixon GH (1987) Cloning of bovine P1 protamine cDNA and the evolution of vertebrate P1 protamines. DNA 6:47–57

    PubMed  Google Scholar 

  • Krawetz SA, Connor W, Dixon GH (1988) Bovine protamine genes contain a single intron: the structures of the two alleles. J Biol Chem 263:321–326

    PubMed  Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441

    PubMed  Google Scholar 

  • Maniatis T, Goodbourn S, Fischer JA (1987) Regulation of inducible and tissue-specific gene expression. Science 236: 1237–1245

    PubMed  Google Scholar 

  • Mazrimas JA, Corzett M, Campos C, Balhorn R (1986) A corrected primary sequence for bull protamine. Biochim Biophys Acta 872:11–15

    PubMed  Google Scholar 

  • McKay DJ, Renaux BS, Dixon GH (1986a) Rainbow trout protamines amino acid sequences of six distinct proteins from a single testis. Eur J Biochem 158:361–366

    PubMed  Google Scholar 

  • McKay DJ, Renaux BS, Dixon GH (1986b) Human sperm protamines amino-acid sequences of two forms of protamine P2. Eur J Biochem 156:5–8

    PubMed  Google Scholar 

  • Moir RD, Dixon GH (1988) A repetitive DNA sequence in the salmonid fishes similar to a retroviral long terminal repeat. J Mol Evol 27:1–7

    PubMed  Google Scholar 

  • Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459–472

    PubMed  Google Scholar 

  • National Biomedical Research Foundation (1987) PIR Release 12. Georgetown University. George DG, Barker WC, Hunt LT (1986) The protein identification resource (PIR). Nucleic Acids Res 14:11–15

    Google Scholar 

  • Oliva R, Bazett-Jones D, Mezquita C, Dixon GH (1987) Factors affecting nucleosome disassembly by protaminesin vitro: histone hyperacetylation and chromatin structure, time dependence and the size of the sperm nuclear proteins. J Biol Chem 262:17016–17025

    PubMed  Google Scholar 

  • Peschon JJ, Behringer RR, Brinster RL, Palmiter RD (1987) Spermatid-specific expression of protamine 1 in transgenic mice. Proc Natl Acad Sci USA 84:5316–5319

    PubMed  Google Scholar 

  • Seeger C, Ganem D, Varmus HE (1984), Nucleotide sequence of an infectious molecularly cloned genome of ground squirrel hepatitis virus. J Virol 51:367–375

    PubMed  Google Scholar 

  • Sinclair GD, Dixon GH (1982) Purification and characterization of cytoplasmic protamine messenger ribonucleoprotein particles from rainbow trout testis cells. Biochemistry 21: 1869–1877

    PubMed  Google Scholar 

  • States JC, Connor W, Wosnick MA, Aiken JM, Gedamu L, Dixon GH (1982) Nucleotide sequence of a protamine component CII gene ofSalmo gairdnerii. Nucleic Acids Res 10:4551–4563

    PubMed  Google Scholar 

  • Yelick PC, Balhorn R, Johnson PA, Corzett M, Mazrimas JA, Kleene KC, Hecht NB (1987) Mouse protamine 2 is synthesized as a precursor whereas mouse protamine 1 is not. Mol Cell Biol 7:2173–2179

    PubMed  Google Scholar 

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  1. Department of Medical Biochemistry, Faculty of Medicine, University of Calgary, 3330 Hospital Drive N.W., T2N 4N1, Calgary, Alberta, Canada

    Stephen A. Krawetz & Gordon H. Dixon

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  1. Stephen A. Krawetz
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  2. Gordon H. Dixon
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Krawetz, S.A., Dixon, G.H. Sequence similarities of the protamine genes: Implications for regulation and evolution. J Mol Evol 27, 291–297 (1988). https://doi.org/10.1007/BF02101190

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  • DOI: https://doi.org/10.1007/BF02101190

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