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Chapter 4 : Plasmid Rolling-Circle Replication

Authors: José A. Ruiz-Masó1, Cristina Machón2, Lorena Bordanaba-Ruiseco4, Manuel Espinosa5, Miquel Coll6, Gloria del Solar8
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Affiliations: 1: Centro de Investigaciones Biológicas (CSIC), Ramiro de Maeztu 9, 28040 Madrid, Spain; 2: Institute for Research in Biomedicine (IRB-Barcelona), Baldiri Reixac 10-12, 08028 Barcelona, Spain; 3: Institut de Biologia Molecular de Barcelona (CSIC), Baldiri Reixac 10-12, 08028 Barcelona, Spain; 4: Centro de Investigaciones Biológicas (CSIC), Ramiro de Maeztu 9, 28040 Madrid, Spain; 5: Centro de Investigaciones Biológicas (CSIC), Ramiro de Maeztu 9, 28040 Madrid, Spain; 6: Institute for Research in Biomedicine (IRB-Barcelona), Baldiri Reixac 10-12, 08028 Barcelona, Spain; 7: Institut de Biologia Molecular de Barcelona (CSIC), Baldiri Reixac 10-12, 08028 Barcelona, Spain; 8: Centro de Investigaciones Biológicas (CSIC), Ramiro de Maeztu 9, 28040 Madrid, Spain
Content Type: Monograph
Publication Year: 2015

Category: Clinical Microbiology

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Abstract:

The main features that characterize rolling-circle replication (RCR) (see Fig. 1A ) derive from its singular initiation mechanism, which relies on the sequence-specific cleavage, at the nick site of the double-strand origin (), of one of the parental DNA strands by an initiator Rep protein. This cleavage generates a 3′-OH end that allows the host DNA polymerases to initiate the leading strand replication. Therefore, the RCR initiation circumvents the synthesis of a primer RNA that is required in all other modes of replication of circular double-stranded DNA (dsDNA). Elongation of the leading strand takes place as the parental double helix is unwound by a host DNA helicase and the cleaved nontemplate strand is covered with the single-stranded DNA binding protein. Since the nascent DNA is covalently attached to the parental DNA, termination of a round of leading-strand replication implies a new cleavage event at the reconstituted nick site. This reaction is assumed to be catalyzed by the same Rep molecule that carried out the initiation cleavage and remained bound to the 5′ end of the parental strand while traveling along with the replication fork. A trans-esterification then occurs that joins this 5′ end to the 3′ end generated in the termination cleavage, releasing the displaced parental strand as a circular single-stranded DNA (ssDNA). This replicative intermediate serves as the template for the synthesis of the lagging strand, which depends solely on host-encoded enzymes and is initiated from a highly structured region of the ssDNA, termed the single-strand origin ().

Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
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Plasmid Rolling-Circle Replication
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Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
/content/10.1128/9781555818982.chap4.fig4-1
Figure 1
(A) A model for plasmid RCR based on pMV158 and pT181 replicons. Detailed information about the RCR process is given in the text. In the pMV158 replication model, a possible mechanism is shown in which, upon assembly and cleavage at the nick site, the hexameric ring of RepB encircles one of the plasmid strands within the central channel. As discussed in the text, the strand enclosure may confer high processivity to the replisome complex. The RepB-mediated mechanism that, at the termination step, yields the dsDNA replication product and the ssDNA intermediate, as well as the mechanism of RepB inactivation, remain undisclosed (dotted arrow with ? symbol). (B) Scheme of the s and of the adjacent regions of the pMV158 and pT181 RCR plasmids. The symbols used are as follows: direct repeats in the replication region are indicated by solid boxed arrows; the inverted arrows represent the two arms of the inverted repeat elements; promoters are indicated by open arrowheads. The AT- and GC-rich sequences (A+T and G+C, respectively) are also indicated. The dotted line above the pMV158 map indicates that the direct repeats of the locus are separated by 84 bp from the nick site. SSB, single-stranded DNA binding protein.
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Image of Figure 1
Figure 1

(A) A model for plasmid RCR based on pMV158 and pT181 replicons. Detailed information about the RCR process is given in the text. In the pMV158 replication model, a possible mechanism is shown in which, upon assembly and cleavage at the nick site, the hexameric ring of RepB encircles one of the plasmid strands within the central channel. As discussed in the text, the strand enclosure may confer high processivity to the replisome complex. The RepB-mediated mechanism that, at the termination step, yields the dsDNA replication product and the ssDNA intermediate, as well as the mechanism of RepB inactivation, remain undisclosed (dotted arrow with ? symbol). (B) Scheme of the s and of the adjacent regions of the pMV158 and pT181 RCR plasmids. The symbols used are as follows: direct repeats in the replication region are indicated by solid boxed arrows; the inverted arrows represent the two arms of the inverted repeat elements; promoters are indicated by open arrowheads. The AT- and GC-rich sequences (A+T and G+C, respectively) are also indicated. The dotted line above the pMV158 map indicates that the direct repeats of the locus are separated by 84 bp from the nick site. SSB, single-stranded DNA binding protein.

Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
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Figure 2
Functional organization of the RCR plasmids. Plasmids representative of the different families are shown. The arrows point to the direction of transcription (black) or the direction of replication (red) from the (leading strand) and (lagging strand). Inside the boxes, is the replication gene; represents the copy number control gene(s); is the double-strand origin of replication; is the single-strand origin of replication; and are chloramphenicol- and tetracycline-resistant genes, respectively; represents the conjugative mobilization gene; indicates an open reading frame with unknown homology. The positions of the copy number control genes and of pGA1, and of the gene of pTX14-2 are also indicated.
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Figure 2

Functional organization of the RCR plasmids. Plasmids representative of the different families are shown. The arrows point to the direction of transcription (black) or the direction of replication (red) from the (leading strand) and (lagging strand). Inside the boxes, is the replication gene; represents the copy number control gene(s); is the double-strand origin of replication; is the single-strand origin of replication; and are chloramphenicol- and tetracycline-resistant genes, respectively; represents the conjugative mobilization gene; indicates an open reading frame with unknown homology. The positions of the copy number control genes and of pGA1, and of the gene of pTX14-2 are also indicated.

Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
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Figure 3
Domain structure of the Rep proteins from RCR plasmids. Predicted and observed secondary structures of the replication proteins of different RCR plasmids and of the Rep proteins from the adeno associated virus (AAV) and bovine papillomavirus (BPV). The amino-terminal end (N) and the number of amino acids are indicated for each of the proteins analyzed. The predicted or observed α-helices and β-strands are represented as red and green bars, respectively. The 3-helices are represented as blue bars. Conserved amino acid residues of the active site involved in metal binding (HUH) and in the endonucleolytic activity are indicated in the protein maps. The conserved Walker A, B, and C motifs are indicated in the proteins with a helicase domain. The limits of the origin binding domain (OBD) and of the oligomerization domain (OD) are indicated in the protein maps of RepB, Rep68, and E1. The additional line below the sequence of RepB, Rep68, and E1 shows the secondary structure present in the crystal structure of the protein (PDB entry code is given in the figure). Plasmidic Rep proteins were aligned by the metal binding HUH motif. However, viral Reps were aligned with RepB by the all-helical OD domain due to the structural similarity found in this region.
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Figure 3

Domain structure of the Rep proteins from RCR plasmids. Predicted and observed secondary structures of the replication proteins of different RCR plasmids and of the Rep proteins from the adeno associated virus (AAV) and bovine papillomavirus (BPV). The amino-terminal end (N) and the number of amino acids are indicated for each of the proteins analyzed. The predicted or observed α-helices and β-strands are represented as red and green bars, respectively. The 3-helices are represented as blue bars. Conserved amino acid residues of the active site involved in metal binding (HUH) and in the endonucleolytic activity are indicated in the protein maps. The conserved Walker A, B, and C motifs are indicated in the proteins with a helicase domain. The limits of the origin binding domain (OBD) and of the oligomerization domain (OD) are indicated in the protein maps of RepB, Rep68, and E1. The additional line below the sequence of RepB, Rep68, and E1 shows the secondary structure present in the crystal structure of the protein (PDB entry code is given in the figure). Plasmidic Rep proteins were aligned by the metal binding HUH motif. However, viral Reps were aligned with RepB by the all-helical OD domain due to the structural similarity found in this region.

Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
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Figure 4
Cartoon representation of the structure of RepB obtained by X-ray crystallography. (A) Top (left) and side (right) views of the RepB hexamer. The locations of the OBD (continuous line) and of the OD (dotted line) are also indicated in the two views. The position of the hinge connecting both domains is indicated in the side view. (B) Top (left) and side (right) views of the electrostatic potential on the solvent-accessible surface of the RepB hexamer structure. The location of the crevice is indicated.
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Image of Figure 4
Figure 4

Cartoon representation of the structure of RepB obtained by X-ray crystallography. (A) Top (left) and side (right) views of the RepB hexamer. The locations of the OBD (continuous line) and of the OD (dotted line) are also indicated in the two views. The position of the hinge connecting both domains is indicated in the side view. (B) Top (left) and side (right) views of the electrostatic potential on the solvent-accessible surface of the RepB hexamer structure. The location of the crevice is indicated.

Citation: Ruiz-Masó J, Machón C, Bordanaba-Ruiseco L, Espinosa M, Coll M, del Solar G. 2015. Plasmid Rolling-Circle Replication, p 45-69. In Tolmasky M, Alonso J (ed), Plasmids: Biology and Impact in Biotechnology and Discovery. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PLAS-0035-2014
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