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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
Altman S, Model P, Dixon GH, Wosnick MA (1981) AnE. coli gene coding for a protamine-like protein. Cell 26:299–304
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
Berlot-Picard F, Vodjdani G, Doly J (1986) Nucleotide sequence of a cDNA clone encodingScylliorhinus caniculus protamine Z2. Eur J Biochem 160:305–310
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
Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Clayton J, Kedes L (1982) GEL, a DNA sequencing project management system. Nucleic Acids Res 10:305–321
Dayhoff M (1978) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Silver Spring MD
Dingwall C, Laskey RA (1986) Protein import into the cell nucleus. Annu Rev Cell Biol 2:367–390
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
Dynan WS, Tjian R (1985) Control of eucaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316:774–778
Fitch WM, Langley CH (1976) Protein evolution and the molecular clock. Fed Proc 35:2092–2097
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
Gedamu L, Davies PL, Dixon GH (1977) Identification and isolation of protamine messenger ribonucleoprotein particles from rainbow trout testis. Biochemistry 16:1383–1391
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
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
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
Kleene KC, Distel RJ, Hecht NB (1985) Nucleotide sequence of a cDNA clone encoding mouse protamine 1. Biochemistry 24:719–722
Krawetz SA, Connor W, Dixon GH (1987) Cloning of bovine P1 protamine cDNA and the evolution of vertebrate P1 protamines. DNA 6:47–57
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
Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441
Maniatis T, Goodbourn S, Fischer JA (1987) Regulation of inducible and tissue-specific gene expression. Science 236: 1237–1245
Mazrimas JA, Corzett M, Campos C, Balhorn R (1986) A corrected primary sequence for bull protamine. Biochim Biophys Acta 872:11–15
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
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
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
Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459–472
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
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
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
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
Sinclair GD, Dixon GH (1982) Purification and characterization of cytoplasmic protamine messenger ribonucleoprotein particles from rainbow trout testis cells. Biochemistry 21: 1869–1877
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
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
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02101190