Abstract
Escherichia coli bacteriophage PRD1 and its relatives contain linear double-stranded DNA genomes, the replication of which proceeds via a protein-primed mechanism. Characteristically, these molecules contain 5'-covalently bound terminal proteins and inverted terminal nucleotide sequences (inverted terminal repeats [ITRs]). The ITRs of each PRD1 phage species have evolved in parallel, suggesting communication between the molecule ends during the life cycle of these viruses. This process was studied by constructing chimeric PRD1 phage DNA molecules with dissimilar end sequences. These molecules were created by combining two closely related phage genomes (i) in vivo by homologous recombination and (ii) in vitro by ligation of appropriate DNA restriction fragments. The fate of the ITRs after propagation of single genomes was monitored by DNA sequence analysis. Recombinants created in vivo showed that phages with nonidentical genome termini are viable and relatively stable, and hybrid phages made in vitro verified this observation. However, genomes in which the dissimilar DNA termini had regained identical sequences were also detected. These observations are explained by a DNA replication model involving two not mutually exclusive pathways. The generality of this model in protein-primed DNA replication is discussed.
Full text
PDF![4696](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/b9af28295e01/jvirol00029-0252.png)
![4697](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/cfcb1d3292a9/jvirol00029-0253.png)
![4698](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/bd351678527d/jvirol00029-0254.png)
![4699](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/ddf7c668544a/jvirol00029-0255.png)
![4700](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/de24c90168a8/jvirol00029-0256.png)
![4701](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/b2b682b496f5/jvirol00029-0257.png)
![4702](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/e9be519a777a/jvirol00029-0258.png)
![4703](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/887a/237855/07ec75e85a2a/jvirol00029-0259.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bamford D. H., Mindich L. Characterization of the DNA-protein complex at the termini of the bacteriophage PRD1 genome. J Virol. 1984 May;50(2):309–315. doi: 10.1128/jvi.50.2.309-315.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bamford D. H., Rouhiainen L., Takkinen K., Söderlund H. Comparison of the lipid-containing bacteriophages PRD1, PR3, PR4, PR5 and L17. J Gen Virol. 1981 Dec;57(Pt 2):365–373. doi: 10.1099/0022-1317-57-2-365. [DOI] [PubMed] [Google Scholar]
- Bamford D., McGraw T., MacKenzie G., Mindich L. Identification of a protein bound to the termini of bacteriophage PRD1 DNA. J Virol. 1983 Aug;47(2):311–316. doi: 10.1128/jvi.47.2.311-316.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bamford J. K., Bamford D. H. Capsomer proteins of bacteriophage PRD1, a bacterial virus with a membrane. Virology. 1990 Aug;177(2):445–451. doi: 10.1016/0042-6822(90)90508-o. [DOI] [PubMed] [Google Scholar]
- Bamford J. K., Bamford D. H. Large-scale purification of membrane-containing bacteriophage PRD1 and its subviral particles. Virology. 1991 Mar;181(1):348–352. doi: 10.1016/0042-6822(91)90501-2. [DOI] [PubMed] [Google Scholar]
- Bamford J. K., Hänninen A. L., Pakula T. M., Ojala P. M., Kalkkinen N., Frilander M., Bamford D. H. Genome organization of membrane-containing bacteriophage PRD1. Virology. 1991 Aug;183(2):658–676. doi: 10.1016/0042-6822(91)90995-n. [DOI] [PubMed] [Google Scholar]
- Bradley D. E., Rutherford E. L. Basic characterization of a lipid-containing bacteriophage specific for plasmids of the P, N, and W compatibility groups. Can J Microbiol. 1975 Feb;21(2):152–163. doi: 10.1139/m75-023. [DOI] [PubMed] [Google Scholar]
- Coetzee W. F., Bekker P. J. Pilus-specific, lipid-containing bacteriophages PR4 and PR772: comparison of physical characteristics of genomes. J Gen Virol. 1979 Oct;45(1):195–200. doi: 10.1099/0022-1317-45-1-195. [DOI] [PubMed] [Google Scholar]
- Daniell E. Genome structure of incomplete particles of adenovirus. J Virol. 1976 Aug;19(2):685–708. doi: 10.1128/jvi.19.2.685-708.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Escarmís C., Guirao D., Salas M. Replication of recombinant phi 29 DNA molecules in Bacillus subtilis protoplasts. Virology. 1989 Mar;169(1):152–160. doi: 10.1016/0042-6822(89)90051-2. [DOI] [PubMed] [Google Scholar]
- Gerendasy D., Ito J. Nucleotide sequence and transcription of the right early region of bacteriophage PRD1. J Bacteriol. 1990 Apr;172(4):1889–1898. doi: 10.1128/jb.172.4.1889-1898.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gutiérrez C., Sogo J. M., Salas M. Analysis of replicative intermediates produced during bacteriophage phi 29 DNA replication in vitro. J Mol Biol. 1991 Dec 20;222(4):983–994. doi: 10.1016/0022-2836(91)90589-x. [DOI] [PubMed] [Google Scholar]
- Haj-Ahmad Y., Graham F. L. Characterization of an adenovirus type 5 mutant carrying embedded inverted terminal repeats. Virology. 1986 Aug;153(1):22–34. doi: 10.1016/0042-6822(86)90004-8. [DOI] [PubMed] [Google Scholar]
- Harding N. E., Ito J. DNA replication of bacteriophage phi 29: characterization of the intermediates and location of the termini of replication. Virology. 1980 Jul 30;104(2):323–338. doi: 10.1016/0042-6822(80)90337-2. [DOI] [PubMed] [Google Scholar]
- Hay R. T., McDougall I. M. Viable viruses with deletions in the left inverted terminal repeat define the adenovirus origin of DNA replication. J Gen Virol. 1986 Feb;67(Pt 2):321–332. doi: 10.1099/0022-1317-67-2-321. [DOI] [PubMed] [Google Scholar]
- Hay R. T., Stow N. D., McDougall I. M. Replication of adenovirus mini-chromosomes. J Mol Biol. 1984 Jun 5;175(4):493–510. doi: 10.1016/0022-2836(84)90181-5. [DOI] [PubMed] [Google Scholar]
- Hsieh J. C., Jung G. H., Leavitt M. C., Ito J. Primary structure of the DNA terminal protein of bacteriophage PRD1. Nucleic Acids Res. 1987 Nov 11;15(21):8999–9009. doi: 10.1093/nar/15.21.8999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hu C. H., Xu F. Y., Wang K., Pearson A. N., Pearson G. D. Symmetrical adenovirus minichromosomes have hairpin replication intermediates. Gene. 1992 Jan 15;110(2):145–150. doi: 10.1016/0378-1119(92)90641-2. [DOI] [PubMed] [Google Scholar]
- Inciarte M. R., Salas M., Sogo J. M. Structure of replicating DNA molecules of Bacillus subtilis bacteriophage phi 29. J Virol. 1980 Apr;34(1):187–199. doi: 10.1128/jvi.34.1.187-199.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jung G. H., Leavitt M. C., Hsieh J. C., Ito J. Bacteriophage PRD1 DNA polymerase: evolution of DNA polymerases. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8287–8291. doi: 10.1073/pnas.84.23.8287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lechner R. L., Kelly T. J., Jr The structure of replicating adenovirus 2 DNA molecules. Cell. 1977 Dec;12(4):1007–1020. doi: 10.1016/0092-8674(77)90165-9. [DOI] [PubMed] [Google Scholar]
- Lippé R., Graham F. L. Adenoviruses with nonidentical terminal sequences are viable. J Virol. 1989 Dec;63(12):5133–5141. doi: 10.1128/jvi.63.12.5133-5141.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lyra C., Savilahti H., Bamford D. H. High-frequency transfer of linear DNA containing 5'-covalently linked terminal proteins: electroporation of bacteriophage PRD1 genome into Escherichia coli. Mol Gen Genet. 1991 Aug;228(1-2):65–69. doi: 10.1007/BF00282449. [DOI] [PubMed] [Google Scholar]
- Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
- McGraw T., Yang H. L., Mindich L. Establishment of a physical and genetic map for bacteriophage PRD1. Mol Gen Genet. 1983;190(2):237–244. doi: 10.1007/BF00330646. [DOI] [PubMed] [Google Scholar]
- Meinhardt F., Kempken F., Kämper J., Esser K. Linear plasmids among eukaryotes: fundamentals and application. Curr Genet. 1990 Feb;17(2):89–95. doi: 10.1007/BF00312851. [DOI] [PubMed] [Google Scholar]
- Mindich L., Bamford D., Goldthwaite C., Laverty M., Mackenzie G. Isolation of nonsense mutants of lipid-containing bacteriophage PRD1. J Virol. 1982 Dec;44(3):1013–1020. doi: 10.1128/jvi.44.3.1013-1020.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mindich L., Cohen J., Weisburd M. Isolation of nonsense suppressor mutants in Pseudomonas. J Bacteriol. 1976 Apr;126(1):177–182. doi: 10.1128/jb.126.1.177-182.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mindich L., McGraw T. Molecular cloning of bacteriophage PRD1 genomic fragments. Mol Gen Genet. 1983;190(2):233–236. doi: 10.1007/BF00330645. [DOI] [PubMed] [Google Scholar]
- Olsen R. H., Siak J. S., Gray R. H. Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage. J Virol. 1974 Sep;14(3):689–699. doi: 10.1128/jvi.14.3.689-699.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pakula T. M., Caldentey J., Gutiérrez C., Olkkonen V. M., Salas M., Bamford D. H. Overproduction, purification, and characterization of DNA-binding protein P19 of bacteriophage PRD1. Gene. 1993 Apr 15;126(1):99–104. doi: 10.1016/0378-1119(93)90595-t. [DOI] [PubMed] [Google Scholar]
- Pakula T. M., Caldentey J., Serrano M., Gutierrez C., Hermoso J. M., Salas M., Bamford D. H. Characterization of a DNA binding protein of bacteriophage PRD1 involved in DNA replication. Nucleic Acids Res. 1990 Nov 25;18(22):6553–6557. doi: 10.1093/nar/18.22.6553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pakula T. M., Savilahti H., Bamford D. H. The organization of the right-end early region of bacteriophage PRD1 genome. Gene. 1989 Dec 21;85(1):53–58. doi: 10.1016/0378-1119(89)90463-0. [DOI] [PubMed] [Google Scholar]
- Sakaguchi K. Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements, and genomes of adeno-type viruses. Microbiol Rev. 1990 Mar;54(1):66–74. doi: 10.1128/mr.54.1.66-74.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salas M. Protein-priming of DNA replication. Annu Rev Biochem. 1991;60:39–71. doi: 10.1146/annurev.bi.60.070191.000351. [DOI] [PubMed] [Google Scholar]
- Savilahti H., Bamford D. H. Linear DNA replication: inverted terminal repeats of five closely related Escherichia coli bacteriophages. Gene. 1986;49(2):199–205. doi: 10.1016/0378-1119(86)90280-5. [DOI] [PubMed] [Google Scholar]
- Savilahti H., Bamford D. H. The complete nucleotide sequence of the left very early region of Escherichia coli bacteriophage PRD1 coding for the terminal protein and the DNA polymerase. Gene. 1987;57(1):121–130. doi: 10.1016/0378-1119(87)90183-1. [DOI] [PubMed] [Google Scholar]
- Savilahti H., Caldentey J., Bamford D. H. Bacteriophage PRD1 terminal protein: expression of gene VIII in Escherichia coli and purification of the functional P8 product. Gene. 1989 Dec 21;85(1):45–51. doi: 10.1016/0378-1119(89)90462-9. [DOI] [PubMed] [Google Scholar]
- Savilahti H., Caldentey J., Lundström K., Syväoja J. E., Bamford D. H. Overexpression, purification, and characterization of Escherichia coli bacteriophage PRD1 DNA polymerase. In vitro synthesis of full-length PRD1 DNA with purified proteins. J Biol Chem. 1991 Oct 5;266(28):18737–18744. [PubMed] [Google Scholar]
- Sogo J. M., García J. A., Peñalva M. A., Salas M. Structure of protein-containing replicative intermediates of Bacillus subtilis phage phi 29 DNA. Virology. 1982 Jan 15;116(1):1–18. doi: 10.1016/0042-6822(82)90398-1. [DOI] [PubMed] [Google Scholar]
- Stanisich V. A. The properties and host range of male-specific bacteriophages of Pseudomonas aeruginosa. J Gen Microbiol. 1974 Oct;84(2):332–342. doi: 10.1099/00221287-84-2-332. [DOI] [PubMed] [Google Scholar]
- Stow N. D. The infectivity of adenovirus genomes lacking DNA sequences from their left-hand termini. Nucleic Acids Res. 1982 Sep 11;10(17):5105–5119. doi: 10.1093/nar/10.17.5105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang K., Pearson G. D. Adenovirus sequences required for replication in vivo. Nucleic Acids Res. 1985 Jul 25;13(14):5173–5187. doi: 10.1093/nar/13.14.5173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang K., Xu F. Y., Ahern K. G., Pearson G. D. Inverted repeats direct repair of adenovirus minichromosome ends. Virology. 1991 Jul;183(1):44–51. doi: 10.1016/0042-6822(91)90116-s. [DOI] [PubMed] [Google Scholar]
- Wong F. H., Bryan L. E. Characteristics of PR5, a lipid-containing plasmid-dependent phage. Can J Microbiol. 1978 Jul;24(7):875–882. doi: 10.1139/m78-145. [DOI] [PubMed] [Google Scholar]
- Yoo S. K., Ito J. Protein-primed replication of bacteriophage PRD1 genome in vitro. Virology. 1989 Jun;170(2):442–449. doi: 10.1016/0042-6822(89)90435-2. [DOI] [PubMed] [Google Scholar]
- Yoo S. K., Ito J. Sequence requirements for protein-primed DNA replication of bacteriophage PRD1. J Mol Biol. 1991 Apr 20;218(4):779–789. doi: 10.1016/0022-2836(91)90266-9. [DOI] [PubMed] [Google Scholar]