Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Springer Nature Link
Log in

Evidence of sequences resembling avian retrovirus long terminal repeats flanking the trout protamine gene

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Additional TATA boxes are present in the flanking regions of trout protamine genes. Their activity as promoters was assayed using an in vitro transcription system. These additional TATA boxes, together with polyadenylation signals that include the consensus AATAAA and CACTG sequences very close to the promoters, suggest that these sequences may be closely related to retroviral long terminal repeat (LTR) sequences. Other features of retroviral LTRs that are also present are short inverted repeats. The LTR-like sequences flanking the trout protamine gene show significant homology to the avian sarcoma virus LTR over a 40-bp region. The trout protamine gene falls into the relatively rare intronless class of eukaryotic genes. This suggests that the gene could have been derived from a processed gene introduced into the genome by reverse transcription of a mature mRNA. The protamine-mRNA-coding region is flanked by AACA... TGTT sequences, which might represent vestigial traces of past recombination events and whose presence supports the notion that the protamine gene sequence was of foreign origin. Recent attempts in this laboratory to transfer the protamine gene into mouse cells have resulted in a high frequency of deletions similar to those observed with constructs in which a retrovirus was used as a vector to transfect foreign DNA with promoters. The distribution of protamine genes in the animal kingdom is very sporadic, which suggests that protamine genes appeared relatively late in evolution. The nonuniform occurrence of the gene among lower vertebrates may have been the result of its horizontal transmission only to certain species, possibly by infection with retroviruses that acquired it from a different species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Agarwal KL, Brundstedt J, Noyes BE (1981) A general method for detection and characterization of an mRNA using an oligonucleotide probe. J Biol Chem 256:1023–1028

    PubMed  Google Scholar 

  • Aiken JM, McKenzie D, Zhao H-Z, States JC, Dixon GH (1983) Sequence homologies in the protamine gene family of rainbow trout. Nucleic Acids Res 11:4907–4922

    PubMed  Google Scholar 

  • Alder D, Gorovsky MA (1957) Electrophoretic analysis of liver and testis histones of the frogRana pipiens. J Cell Biol 64: 389–397

    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 

  • Ando T, Yamasaki M, Suzuki K (1973) Protamines. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Bark C, Hammarstrom K, Westin G, Pettersson U (1985) Nonrandom integration of human U4 RNA pseudogenes. Mol Cell Biol 5:943–948

    PubMed  Google Scholar 

  • Beneveniste RE, Todaro GJ (1974) Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature 252:456–459

    PubMed  Google Scholar 

  • Benoist C, O'Hare K, Breathnach R, Chambon P (1980) The ovalbumin gene—sequence of putative control regions. Nucleic Acids Res 8:127–142

    PubMed  Google Scholar 

  • Berget SM (1984) Are U4 small nuclear ribonucleoproteins involved in polyadenylation? Nature 309:179–182

    PubMed  Google Scholar 

  • Bloch DP (1969) A catalog of sperm histones. Genetics 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 

  • Busslinger M, Rusconi S, Birnstiel ML (1982) An unusual evolutionary behavior of sea urchin histone gene cluster. EMBO J 1:27–33

    Google Scholar 

  • Cole N, Santagelo G (1983) Analysis in COS-1 cells of processing and polyadenylation signals by using derivatives of the herpes simplex virus type 1 thymidine kinase gene. Mol Cell Biol 3:267–279

    PubMed  Google Scholar 

  • Corden J, Wasylyk B, Buchwalder A, Sassone-Corsi P, Kedinger C, Chambon P (1980) Promoter sequences of eukaryotic protein-coding genes. Science 209:1406–1414

    PubMed  Google Scholar 

  • Dagert M, Ehrlich SD (1979) Prolonged incubation in calcium chloride improves the competence ofEscherichia coli cells. Gene 6:23–28

    PubMed  Google Scholar 

  • Donchower L, Huang A, Hager GL (1981) Regulatory and coding potential of the mouse mammary tumor virus long terminal redundancy. J Virol 37:226–238

    PubMed  Google Scholar 

  • Emerman M, Temin HM (1984) High-frequency deletion in recovered retrovirus vectors containing exogenous DNA with promoters. J Virol 50:42–49

    PubMed  Google Scholar 

  • Fiers W, Contreras R, Haegeman G, Rogiers R, Van de Voorde A, Van Heuverswyn H, Van Herreweghe J, Volckaert G, Ysebaert M (1978) Complete nucleotide sequence of SV40 DNA. Nature 273:113–120

    PubMed  Google Scholar 

  • Fitzgerald M, Shenk T (1981) The sequence 5-AAUAAA-3 forms part of the recognition site for polyadenylation of late SV40 mRNAs. Cell 24:251–260

    PubMed  Google Scholar 

  • Gedamu L, Wosnick MA, Connor W, Watson DC, Dixon GH, Iatrou K (1981) Molecular analysis of the protamine multigene family in rainbow trout testis. Nucleic Acids Res 9:1463–1482

    PubMed  Google Scholar 

  • Gregory SP, Dillon NO, Butterworth HW (1982) A comparison of the promoter strengths of two eukaryotic genesin vitro reveals a region of DNA that can influence the rate of transcription in cis over long distances. Nucleic Acids Res 10: 7581–7592

    PubMed  Google Scholar 

  • Grosveld GC, Shewmaker CK, Jat P, Flavell RA (1981) Localization of DNA sequences necessary for transcription of the rabbit beta-globin genein vitro. Cell 25:215–226

    PubMed  Google Scholar 

  • Guarante L, Laurer G, Roberts R, Ptashne M (1980) Improved methods for minimizing expression of a cloned gene: a bacterium that synthesized rabbit beta-globin. Cell 20:543–553

    PubMed  Google Scholar 

  • Hagenbuchle C, Bovey R, Yong RA (1980) Tissue-specific expression of mouse alpha-amylase genes: nucleotide sequence of isoenzyme mRNAs from pancreas and salivary gland. Cell 21:179–187

    PubMed  Google Scholar 

  • Hirose S, Takauchi K, Suzuki Y (1982)In vitro characterization of the fibroin gene promoter by the use of single-base substitution mutants. Proc Natl Acad Sci USA 79:7258–7262

    PubMed  Google Scholar 

  • Hishinuma F, DeBona PJ, Astrin S, Skalka AM (1981) Nucleotide sequence of acceptor site and termini of integrated avian endogenous provirus evl: Integration creates a 6 bp repeat of host DNA. Cell 23:155–164

    PubMed  Google Scholar 

  • Hu S-L, Manley JL (1981) DNA sequence required for initiation of transcriptionin vitro from the major late promoter of adenovirus 2. Proc Natl Acad Sci USA 78:820–824

    PubMed  Google Scholar 

  • Hughes SH (1982) Sequence of the long terminal repeat and adjacent segments of the endogenous avian virus rous-associated virus O. J Virol 43:191–200

    PubMed  Google Scholar 

  • Itin A, Keshet E (1985) Primer binding sites corresponding to several tRNA species are present in DNAs of different members of the same retrovirus-gene family (VL30). J Virol 54:236–239

    PubMed  Google Scholar 

  • Jankowski JM, Dixon GH (1984) Transcription of a trout protamine gene in vitro: the effects of alteration of promoters. Can J Biochem Cell Biol 62:291–300

    PubMed  Google Scholar 

  • Jankowski JM, Dixon GH (1985) The in vitro transcription of a rainbow trout (Salmo gairdnerii) protamine gene. II. Controlled mutation of the cap site region. Biosci Rep 5:113–120

    PubMed  Google Scholar 

  • Jankowski JM, Walczyk E, Dixon GH (1985) Functional prokaryotic gene control signals within a eukaryotic rainbow trout protamine promoter. Biosci Rep 5:453–461

    PubMed  Google Scholar 

  • Jung A, Sippel AE, Grez M, Schultz G (1980) Exons encode functional and structural units of chicken lysozyme. Proc Natl Acad Sci USA 77:5759–5763

    PubMed  Google Scholar 

  • Karin M, Richards RI (1982) Human metallothionein genesprimary structure of the metallothionein-II gene and a related processed gene. Nature 229:797–802

    Google Scholar 

  • Katz L, Kingsbury D, Helinski D (1973) Stimulation by cyclic adenosine monophosphate of plasmid deoxyribonucleic acid-protein relaxation complex. J Bacteriol 114:577–591

    PubMed  Google Scholar 

  • Kennedy BP, Davies PL (1980) Acid-soluble nuclear proteins of the testis during spermatogenesis in the water flounder Loss of the high mobility group proteins. J Biol Chem 255: 2533–2539

    PubMed  Google Scholar 

  • Lewin R (1983) How mammalian RNA returns to its genome. Science 219:1052–1054

    PubMed  Google Scholar 

  • Linial M, Blair D (1982) Genetics of retroviruses. In: Weiss R, Teich N, Varmus HE, Coffin J (eds) RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 649–783

    Google Scholar 

  • Louie AJ, Dixon GH (1972) Trout testis cells. II. Synthesis and phosphorylation of histones and protamines in different cell types. J Biol Chem 247:5498–5505

    PubMed  Google Scholar 

  • Manley JL, Fire A, Cano A, Sharp PA, Gefter ML (1980) DNA-dependent transcription of adenovirus genes in a soluble wholecell extract. Proc Natl Acad Sci USA 77:3855–3859

    PubMed  Google Scholar 

  • Marushige K, Dixon GH (1969) Developmental changes in chromosomal composition and template activity during spermatogenesis in trout testis. Dev Biol 19:397–414

    PubMed  Google Scholar 

  • Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base specific chemical cleavages. Methods Enzymol 65:499–560

    PubMed  Google Scholar 

  • McMaster GK, Carmichael GG (1977) Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74:4835–4838

    PubMed  Google Scholar 

  • Mevarech M, Noyes BE, Agarwal KL (1979) Detection of gastrin-specific mRNA using oligodeoxynucleotide probes of defined sequence. J Biol Chem 254:7472–7475

    PubMed  Google Scholar 

  • Miller JN, Lebkowski JS, Greisen KS, Calos MP (1984) Specificity of mutations induced in transfected DNA by mammalian cells. EMBO J 3:3117–3121

    PubMed  Google Scholar 

  • Nakano M, Tobita T, Ando T (1985) Studies on a protamine (galline) from fowl sperm. 2. The amino acid sequence of two components of galline. Int J Pep Prot Res 7:31–46

    Google Scholar 

  • Nakano M, Tobita T, Ando T (1985) Studies on a protamine (galline) from fowl sperm. 3. The total amino acid sequence of intact galline molecule. Int J Pept Protein Res 8:565–578

    Google Scholar 

  • Parker RC, Seed B (1980) Two-dimensional agarose gel electrophoresis “Sea Plaque” agarose dimension. Methods Enzymol 65:358

    PubMed  Google Scholar 

  • Pasek M, Goto T, Gilbert W, Zinle B, Schaller H, Mackay P, Leadbetter G, Murray K (1979) Hepatitis B. virus genes and their expression inE. coli. Nature 282:575–579

    PubMed  Google Scholar 

  • Perricaudet M, Akusjarvi G, Virtanen A, Pettersson U (1979) Structure of two spliced mRNAs from the transforming region of human subgroup C adenoviruses. Nature 281:694–696

    PubMed  Google Scholar 

  • Proudfoot NJ, Brownlee GG (1974) Sequence at the 3′ end of globin mRNA shows homology with immunoglobulin light chain mRNA. Nature 252:359–362

    PubMed  Google Scholar 

  • Radloff R, Baner W, Vinograd J (1967) A dye buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells. Proc Natl Acad Sci USA 57:1514–1521

    PubMed  Google Scholar 

  • Razzaque A, Chakrabarti S, Joffee S, Seidman M (1984) Mol Cell Biol 4:441–453

    Google Scholar 

  • Reddy VB, Gosh PK, Lebovitz P, Piatek M, Weissman SJ (1979) Simian virus 40 early mRNAs. I. Genomic localization of 3′ and 5′ termini and two major splices in mRNA from transformed and lytically infected cells. J Virol 30:279–296

    PubMed  Google Scholar 

  • Reddy R, Henning D, Bush H (1981) The primary nucleotide sequence of U4 RNA. J Biol Chem 256:3532–3538

    PubMed  Google Scholar 

  • Santangelo GM, Cole CN (1983) Preparation of “functional library” of African green monkey DNA fragments which substitute for the processing/polyadenylation signals in the herpes simplex gene. Mol Cell Biol 3:643–653

    PubMed  Google Scholar 

  • Schwartz DE, Zamecnik PC, Weith HL (1977) Rous sarcoma virus genome is terminally redundant: the 3′ sequence. Proc Natl Acad Sci USA 74:994–998

    PubMed  Google Scholar 

  • Sharp P (1983) Conversion of RNA to DNA in mammals: Alulike elements and pseudogenes. Nature 301:471–472

    PubMed  Google Scholar 

  • Shimotohno K, Mizutani S, Temin HM (1980) Sequence of retrovirus provirus resembles that of bacterial transposable elements. Nature 285:550–554

    PubMed  Google Scholar 

  • Shoemaker C, Goff S, Gilboa E, Paskind M, Mitra SW, Baltimore D (1980) Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci USA 77:3932–3936

    PubMed  Google Scholar 

  • Sober HA, (ed) (1968) Handbook of biochemistry. Selected data for molecular biology. CRC Press, Cleveland

    Google Scholar 

  • Sorge J, Hughes SH (1982) Polypurine tract adjacent to the U3 region of the Rous sarcoma virus genome provides a cis-acting function. J Virol 43:482–488

    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 

  • Subirana, JA, Puigjaner LC, Roca J, Llopis R, Suan P (1975) The structure and function of chromatin. Ciba Found Symp 28:157

    Google Scholar 

  • Swanstrom R, DeLorbe W, Bishop JM, Varmus HE (1981) Nucleotide sequence of cloned unintegrated avian sarcoma virus DNA: Viral DNA contains direct and inverted repeats similar to those in transposable elements. Proc Natl Acad Sci USA 78:124–128

    PubMed  Google Scholar 

  • Temin HM (1982) Function of the retrovirus long terminal repeat. Cell 28:3–5

    PubMed  Google Scholar 

  • Varmus HE (1982) Form and function of retroviral proviruses. Science 216:812–820

    PubMed  Google Scholar 

  • Vendrely R, Knoblock-Mazen A, Vendrely C (1960) Donnees biochimiques recentes sur la relation entre acide desoxyribonucleique et proteins basiques dans le noyau. Biochem Pharmacol 4:19–28

    PubMed  Google Scholar 

  • Wagner MJ, Sharp JA, Summers WC (1981) Nucleotide sequence of the thymidine kinase gene of herpes simplex virus type 1. Proc Natl Acad Sci USA 78:1441–1445

    PubMed  Google Scholar 

  • Weiss R, Teich N, Varmus HE, Coffin J (eds) (1982) Appendix. In: RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Zirkin BR (1971) The fine structure of nuclei in mature sperm. I. Application of the Langmuir trough-critical point method to histone-containing sperm nuclei. J Ultrastruct Res 36:237–248

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. J. M. Jankowski & J. C. States

    Present address: IDR-704, Children's Hospital Research Foundation, Elland and Bethesda Avenues, 45229, Cincinnati, Ohio, USA

Authors and Affiliations

  1. Department of Medical Biochemistry, Health Sciences Centre, University of Calgary, 3330 Hospital Drive NW, T2N 4N1, Calgary, Alberta, Canada

    J. M. Jankowski, J. C. States & G. H. Dixon

Authors
  1. J. M. Jankowski
    View author publications

    Search author on:PubMed Google Scholar

  2. J. C. States
    View author publications

    Search author on:PubMed Google Scholar

  3. G. H. Dixon
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jankowski, J.M., States, J.C. & Dixon, G.H. Evidence of sequences resembling avian retrovirus long terminal repeats flanking the trout protamine gene. J Mol Evol 23, 1–10 (1986). https://doi.org/10.1007/BF02100993

Download citation

  • Received:

  • Revised:

  • Issue date:

  • DOI: https://doi.org/10.1007/BF02100993

Key words