DNA replication in bacteriophage φ29: The requirement of a viral-specific product for association of φ29 DNA with the cell membrane of Bacillus amyloliquefaciens

Ivarie, Robert; Pène, Jacques J.

doi:10.1016/0042-6822(73)90330-9

Cited by 38 publications

(55 citation statements)

References 23 publications

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“…Over the last decades, data have accumulated showing that prokaryotic DNA replication, including that of phage DNA, occurs at the cell membrane (for reviews, see references 75, 76, 130, and 192). The first evidence that 29 DNA replication occurs at the membrane of the infected cell was obtained by Ivarie and Pène (118). They recovered parental and replicating 29 DNA molecules together with membranes in a rapidly sedimenting complex in linear density gradients.…”

Section: Gene 167mentioning

confidence: 93%

“…They recovered parental and replicating 29 DNA molecules together with membranes in a rapidly sedimenting complex in linear density gradients. Interestingly, the formation of these complexes required an earlyexpressed viral protein(s) (118). The general view is that the DNA replication factors, probably present in an organized structure, are recruited to one or more sites on the membrane.…”

Section: Gene 167mentioning

confidence: 99%

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φ29 Family of Phages

Meijer

Horcajadas

Salas

2001

Microbiol Mol Biol Rev

184

223

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SUMMARY Continuous research spanning more than three decades has made the Bacillus bacteriophage φ29 a paradigm for several molecular mechanisms of general biological processes, such as DNA replication, regulation of transcription, phage morphogenesis, and phage DNA packaging. The genome of bacteriophage φ29 consists of a linear double-stranded DNA (dsDNA), which has a terminal protein (TP) covalently linked to its 5′ ends. Initiation of DNA replication, carried out by a protein-primed mechanism, has been studied in detail and is considered to be a model system for the protein-primed DNA replication that is also used by most other linear genomes with a TP linked to their DNA ends, such as other phages, linear plasmids, and adenoviruses. In addition to a continuing progress in unraveling the initiation of DNA replication mechanism and the role of various proteins involved in this process, major advances have been made during the last few years, especially in our understanding of transcription regulation, the head-tail connector protein, and DNA packaging. Recent progress in all these topics is reviewed. In addition to φ29, the genomes of several other Bacillus phages consist of a linear dsDNA with a TP molecule attached to their 5′ ends. These φ29-like phages can be divided into three groups. The first group includes, in addition to φ29, phages PZA, φ15, and BS32. The second group comprises B103, Nf, and M2Y, and the third group contains GA-1 as its sole member. Whereas the DNA sequences of the complete genomes of φ29 (group I) and B103 (group II) are known, only parts of the genome of GA-1 (group III) were sequenced. We have determined the complete DNA sequence of the GA-1 genome, which allowed analysis of differences and homologies between the three groups of φ29-like phages, which is included in this review.

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Section: Gene 167mentioning

confidence: 93%

Section: Gene 167mentioning

confidence: 99%

φ29 Family of Phages

Meijer

Horcajadas

Salas

2001

Microbiol Mol Biol Rev

184

223

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“…Rather, these molecules were found within the bulk of the host nucleoid (2). Finally, although the possibility, proposed by Ivarie and Pène (8), that the 29 gene 2 product, the DNA polymerase, could be directly involved in attachment of replicating 29 DNA to the membrane still holds, another perhaps more logic explanation can be considered. Replication will not occur in the absence of a functional DNA polymerase.…”

Section: Protein P167a Has No Helix-destabilizing Activity and Has Nmentioning

confidence: 99%

“…These authors showed (i) that it took at least 10 min before the parental infected 29 DNA molecules became attached to the membrane, (ii) that early expressed viral protein(s) was required for membrane association, (iii) that replicating 29 DNA molecules were attached to the membrane and that the fully replicated doublestranded 29 DNA molecules were first released from the membrane before they were packaged into the phage particles, and (iv) that phage DNA of a 29 mutant containing a temperature-sensitive mutation in gene 2 (later shown to encode the DNA polymerase) did not become associated to the membrane when infected at the non-permissive temperature. Replication of 29 DNA does not start until about 10 min after infection (2,8), implying that until this time no ssDNA-containing replication intermediates are present in the infected cell. This explains why the infecting 29 DNA molecules, present in its double-stranded form, are not associated to the membrane at the very early infection times even though p16.7 is already detected as soon as 6 min after infection (this work and Ref.…”

Section: Protein P167a Has No Helix-destabilizing Activity and Has Nmentioning

confidence: 99%

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The Bacillus subtilis Phage φ29 Protein p16.7, Involved in φ29 DNA Replication, Is a Membrane-localized Single-stranded DNA-binding Protein

Serna-Rico¹,

Salas

Meijer³

2002

Journal of Biological Chemistry

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The functional role of the 29-encoded integral membrane protein p16.7 in phage DNA replication was studied using a soluble variant, p16.7A, lacking the N-terminal membrane-spanning domain. Because of the protein-primed mechanism of DNA replication, the bacteriophage 29 replication intermediates contain long stretches of single-stranded DNA (ssDNA Studies on DNA replication and related processes have provided detailed insights in the function of many proteins involved in these processes (for review, see Ref. 1). Despite this, little is known about the in vivo organization of DNA replication. To gain a better insight in this fundamental process, we studied the in vivo DNA replication of the Bacillus subtilis bacteriophage 29 (2). The detailed knowledge of its in vitro mechanism of DNA replication (for reviews, see Refs. 3 and 4) made 29 an attractive system for this study.The genome of 29 is a linear double-stranded DNA (dsDNA) 1 of 19,285 base pairs that contains a terminal protein (TP) covalently linked at each 5Ј end. Fig. 1A shows a schematic representation of the genetic and transcriptional organization of the 29 genome. Regulation of 29 DNA transcription, which can be divided into an early and a late stage, has been studied extensively in vivo as well as in vitro (for reviews, see Refs. 3 and 5). The late expressed genes, all transcribed from a single operon present in the central part of the genome, encode the structural proteins of the phage, proteins involved in morphogenesis, and those required for lysis of the infected cell. The early expressed genes are present in two operons that flank the late operon. The early operon located at the left side of the 29 genome encodes the transcriptional regulator protein p4 and various proteins that are directly involved in phage DNA replication, such as the DNA polymerase, TP, singlestranded DNA-binding protein (SSB), double-stranded DNAbinding protein, and protein p1. The operon located at the right side of the 29 genome encodes, in addition to proteins p17 and p16.7, four putative proteins of unknown function.A schematic overview of the in vitro 29 DNA replication mechanism is shown in Fig. 1B. Initiation of 29 DNA replication occurs via a so-called protein-primed mechanism (reviewed in Refs. 3, 4, and 6). The TP-containing DNA ends constitute the origins of replication. Initiation of DNA replication starts by recognition of the origin by a heterodimer formed by the 29 DNA polymerase and the primer TP. The DNA polymerase then catalyzes the addition of the first dAMP to the primer TP. Next, after a transition step, these two proteins dissociate, and the DNA polymerase continues processive elongation until replication of the nascent DNA strand is completed. Replication, which starts at both DNA ends, is coupled to strand displacement. This results in the generation of socalled type I replication intermediates consisting of full-length double-stranded 29 DNA molecules with one or more singlestranded DNA (ssDNA) branches of varying lengths. When the two converging DNA...

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