Structural framework for DNA translocation via the viral portal protein

Лебедев, А. А.; Krause, Margret; Isidro, Anabela; Vagin, A.A.; Orlova, Elena V.; Turner, Joanne; Dodson, E.J.; Tavares, Paulo; Antson, A.A.

doi:10.1038/sj.emboj.7601643

Cited by 209 publications

(320 citation statements)

References 45 publications

(83 reference statements)

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“…3B and 5) with 12-fold symmetry (SI Appendix, Figs. S7 and S8 and Table S3), similar to other tailed phages (35)(36)(37)(38). The gateway complex has sixfold symmetry ( Fig.…”

Section: Significancementioning

confidence: 77%

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Nováček

Šiborová

Benešík

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Bacteriophages from the family Myoviridae use double-layered contractile tails to infect bacteria. Contraction of the tail sheath enables the tail tube to penetrate through the bacterial cell wall and serve as a channel for the transport of the phage genome into the cytoplasm. However, the mechanisms controlling the tail contraction and genome release of phages with “double-layered” baseplates were unknown. We used cryo-electron microscopy to show that the binding of the Twort-like phage phi812 to the Staphylococcus aureus cell wall requires a 210° rotation of the heterohexameric receptor-binding and tripod protein complexes within its baseplate about an axis perpendicular to the sixfold axis of the tail. This rotation reorients the receptor-binding proteins to point away from the phage head, and also results in disruption of the interaction of the tripod proteins with the tail sheath, hence triggering its contraction. However, the tail sheath contraction of Myoviridae phages is not sufficient to induce genome ejection. We show that the end of the phi812 double-stranded DNA genome is bound to one protein subunit from a connector complex that also forms an interface between the phage head and tail. The tail sheath contraction induces conformational changes of the neck and connector that result in disruption of the DNA binding. The genome penetrates into the neck, but is stopped at a bottleneck before the tail tube. A subsequent structural change of the tail tube induced by its interaction with the S. aureus cell is required for the genome’s release.

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“…3B and 5) with 12-fold symmetry (SI Appendix, Figs. S7 and S8 and Table S3), similar to other tailed phages (35)(36)(37)(38). The gateway complex has sixfold symmetry ( Fig.…”

Section: Significancementioning

confidence: 77%

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Nováček

Šiborová

Benešík

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…S2). This C-terminal region consists of two tandem β-strands separated by a 3 10 helix. While all the other helices are nearly ideally straight, the longest helix α4 (residues 54-76) is bent significantly by ∼45°.…”

Section: Resultsmentioning

confidence: 99%

“…Many of these features in DNA-packaging are also shared by adenoviruses (6). The x-ray structures of the catalytic component from bacteriophage T4 and the portals from various phages were previously described (7)(8)(9)(10). However, it is not known how the terminases are assembled and how they interact with the portals and procapsids.…”

mentioning

confidence: 99%

Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine

Zhao

Finch

Sequeira

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

101

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In herpesviruses and many bacterial viruses, genome-packaging is a precisely mediated process fulfilled by a virally encoded molecular machine called terminase that consists of two protein components: A DNA-recognition component that defines the specificity for packaged DNA, and a catalytic component that provides energy for the packaging reaction by hydrolyzing ATP. The terminase docks onto the portal protein complex embedded in a single vertex of a preformed viral protein shell called procapsid, and pumps the viral DNA into the procapsid through a conduit formed by the portal. Here we report the 1.65 Å resolution structure of the DNA-recognition component gp1 of the Shigella bacteriophage Sf6 genomepackaging machine. The structure reveals a ring-like octamer formed by interweaved protein monomers with a highly extended fold, embracing a tunnel through which DNA may be translocated. The N-terminal DNA-binding domains form the peripheral appendages surrounding the octamer. The central domain contributes to oligomerization through interactions of bundled helices. The C-terminal domain forms a barrel with parallel beta-strands. The structure reveals a common scheme for oligomerization of terminase DNA-recognition components, and provides insights into the role of gp1 in formation of the packaging-competent terminase complex and assembly of the terminase with the portal, in which ring-like protein oligomers stack together to form a continuous channel for viral DNA translocation.terminase | DNA-packaging | oligomer | bacteriophage | protein:DNA interaction I n many tailed double-stranded DNA (dsDNA) bacteriophages and herpesvirus, the newly synthesized viral DNA in the infected host cell is present as a concatemer that is comprised of multiple copies of unit-length genome. The concatemeric DNA is packaged into a preformed capsid precursor termed procapsid through a channel formed by a portal protein complex embedded in a unique vertex of the procapsid (1-5). The DNApackaging process involves a precisely coordinated sequence of molecular events, driven by a molecular machine called terminase consisting of two proteins: A DNA-recognition component and a catalytic component, also known as the "small" and "large" subunit, respectively. The terminase specifically binds to concatemeric viral DNA through the DNA-recognition component and cleaves it using the catalytic component, generating a new terminus for the DNA. This terminus is threaded through the portal protein channel embedded in the procapsid, and the catalytic component pumps the DNA into the procapsid in an ATP-dependent manner. When an appropriate amount of DNA is inserted, the terminase cuts the DNA again, dissociates from the procapsid, and can start the next cycle of DNA-packaging. Many of these features in DNA-packaging are also shared by adenoviruses (6). The x-ray structures of the catalytic component from bacteriophage T4 and the portals from various phages were previously described (7-10). However, it is not known how the terminases are assembled and h...

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“…The Araucaria portal (ORF52) exhibits weak sequence similarity with the HK97 portal sequence using the FFAS03 server (41) and HHpred (42) ( Table 4). We used instead the structure of the described SPP1 dodecameric portal (43) to fit into the proximal region of the connector reconstruction. The two proteins contain similar numbers of amino acids (617 for Araucaria and 503 for SPP1).…”

Section: Genome Characteristics Of Mycobacteriophagementioning

confidence: 99%

The First Structure of a Mycobacteriophage, the Mycobacterium abscessus subsp. bolletii Phage Araucaria

Sassi

Bebeacua

Drancourt

et al. 2013

J Virol

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The unique characteristics of the waxy mycobacterial cell wall raise questions about specific structural features of their bacteriophages. No structure of any mycobacteriophage is available, although ϳ3,500 have been described to date. To fill this gap, we embarked in a genomic and structural study of a bacteriophage from Mycobacterium abscessus subsp. bolletii, a member of the Mycobacterium abscessus group. This opportunistic pathogen is responsible for respiratory tract infections in patients with lung disorders, particularly cystic fibrosis. M. abscessus subsp. bolletii was isolated from respiratory tract specimens, and bacteriophages were observed in the cultures. We report here the genome annotation and characterization of the M. abscessus subsp. bolletii prophage Araucaria, as well as the first single-particle electron microscopy reconstruction of the whole virion. Araucaria belongs to Siphoviridae and possesses a 64-kb genome containing 89 open reading frames (ORFs), among which 27 could be annotated with certainty. Although its capsid and connector share close similarity with those of several phages from Gram-negative (Gram ؊ ) or Gram ؉ bacteria, its most distinctive characteristic is the helical tail decorated by radial spikes, possibly host adhesion devices, according to which the phage name was chosen. Its host adsorption device, at the tail tip, assembles features observed in phages binding to protein receptors, such as phage SPP1. All together, these results suggest that Araucaria may infect its mycobacterial host using a mechanism involving adhesion to cell wall saccharides and protein, a feature that remains to be further explored.

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Structural framework for DNA translocation via the viral portal protein

Cited by 209 publications

References 45 publications

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Structure and genome release of Twort-like Myoviridae phage with a double-layered baseplate

Crystal structure of the DNA-recognition component of the bacterial virus Sf6 genome-packaging machine

The First Structure of a Mycobacteriophage, the Mycobacterium abscessus subsp. bolletii Phage Araucaria

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