Distinct DNA Exit and Packaging Portals in the Virus Acanthamoeba polyphaga mimivirus

Zauberman, Nathan; Mutsafi, Yael; Halevy, Daniel Ben; Shimoni, Eyal; Klein, Eugenia; Xiao, Chuan; Sun, Siyang; Minsky, Abraham

doi:10.1371/journal.pbio.0060114

Cited by 164 publications

(203 citation statements)

References 37 publications

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“…At 2 h postinfection (PI) of Acanthamoeba polyphaga cells, Mimivirus particles are detected within host phagosomes. A large-scale opening of the viral icosahedral capsid at a unique vertex-centered structure, coined the stargate, results in the formation of a massive channel, which was previously proposed to enable delivery of the internal genome-containing Mimivirus core to the host cytoplasm (10). To appraise this conjecture, electron microscopy studies were conducted on Mimivirus-infected cells at early (2 h) PI time points.…”

Section: Resultsmentioning

confidence: 99%

“…With a genome considerably larger than all currently documented viral genomes, the hurdles inherent for DNA translocations during Mimivirus infection are unparalleled, thus rendering its replication cycle an appealing case study. It was previously shown that a large-scale opening of the Mimivirus capsid at a unique vertex, coined the stargate (10)(11)(12), enables rapid release of the genome-containing internal core into the host cytoplasm (10). Ensuing infection events remain, however, poorly understood.…”

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Vaccinia-like cytoplasmic replication of the giant Mimivirus

Mutsafi¹,

Zauberman²,

Sabanay

et al. 2010

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

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115

127

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Poxviruses are considered to be unique among all DNA viruses, because their infection cycle is carried out exclusively in the host cytoplasm. Such an infection strategy is of interest, because it necessitates generation of elaborate factories in which viral replication and assembly are promoted. By using diverse imaging techniques, we show that the infection cycle of the largest virus currently identified, the Acanthamoeba polyphaga Mimivirus, similarly occurs exclusively in the host cytoplasm. We further show that newly synthesized mRNAs accumulate at discrete cytoplasmic sites that are distinct from the sites where viral replication occurs, and this is observed in vaccinia infection. By revealing substantial physiologic similarity between poxviruses and Mimivirus and thus, implying that an entirely cytoplasmic viral replication might be more common than generally considered, these findings underscore the ability of DNA viruses to generate large and elaborate replication factories.electron tomography | nucleocytoplasmic large DNA viruses | poxviruses | viral factories W ith the single exception of poxviruses, all currently known DNA viruses carry out replication and transcription either entirely or partially within host nuclei. The overwhelming bias to nucleus-centered viral transactions is rationalized by the fact that the nucleus provides the elaborate machinery required for these processes. Moreover, by concentrating essential factors into particular intranuclear sites as well as by enabling spatiotemporal regulation of viral replication and transcription, the nuclear environment considerably enhances the efficiency of these processes (1). Such underlying benefits render the entirely cytoplasmic infection cycle of poxviruses all of the more intriguing (2, 3). Nucleus-centered viral transactions present, however, remarkable hurdles associated with the prerequisite of transporting viral genomes from their entry sites at the cell periphery to and into the nucleus. Specifically, the cellular milieu is refractory to motion of DNA molecules because of the high viscosity of the cytosol and the dense molecular sieve generated by the cytoskeleton (4). Moreover, the nuclear envelope imposes a severe barrier for both entry and exit of long DNA molecules (1).The hurdles associated with genome trafficking are particularly high for nucleocytoplasmic large DNA viruses (NCLDV), which include the eukaryote-infecting families Poxviridae, Phycodnaviridae, Iridoviridae, and Asfarviridae, all characterized by DNA genomes longer than 100 kbp (5). After entry, genomes of phycodnaviruses (6), iridoviruses (7), and the African swine fever virus (8) are released into the cytoplasm at the host cell periphery and then, are shuttled toward and transported into the nucleus where initial replication cycles occur. Viral DNA is subsequently delivered to specific cytoplasmic factories in which all transactions required for viral assembly take place. The factors that attenuate the barriers imposed by the constrained DNA motion and thus, enabl...

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Vaccinia-like cytoplasmic replication of the giant Mimivirus

Mutsafi¹,

Zauberman²,

Sabanay

et al. 2010

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

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115

127

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“…The unique features of Mimivirus revived the debate about the evolution of DNA viruses (Claverie 2006;Claverie et al 2006;Iyer et al 2006) and their position in the Tree of Life (Brüssow 2009;Claverie and Ogata 2009;Moreira and Lopez-Garcia 2009). The complex Mimivirus particle has been the object of detailed proteomic (Renesto et al 2006) and ultrastructural studies (Zauberman et al 2008;Xiao et al 2009), and several individual gene products have been characterized (for review, see Claverie and Abergel 2009); however, a systemic description of the molecular processes at work during the intracellular Mimivirus replication cycle (in particular the eclipse phase) is missing. During this phase, the Acanthamoeba cells are instructed by the infecting Mimivirus to build up a giant organelle-like ''virion factory'' that appears to centralize most of the metabolic processes leading to the synthesis of new Mimivirus particles (Suzan-Monti et al 2007;Claverie and Abergel 2009;Claverie et al 2009b).…”

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confidence: 99%

mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus

Legendre¹,

Audic²,

Poirot³

et al. 2010

Genome Res.

139

173

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Mimivirus, a virus infecting Acanthamoeba, is the prototype of the Mimiviridae, the latest addition to the nucleocytoplasmic large DNA viruses. The Mimivirus genome encodes close to 1000 proteins, many of them never before encountered in a virus, such as four amino-acyl tRNA synthetases. To explore the physiology of this exceptional virus and identify the genes involved in the building of its characteristic intracytoplasmic ''virion factory,'' we coupled electron microscopy observations with the massively parallel pyrosequencing of the polyadenylated RNA fractions of Acanthamoeba castellanii cells at various time post-infection. We generated 633,346 reads, of which 322,904 correspond to Mimivirus transcripts. This first application of deep mRNA sequencing (454 Life Sciences [Roche] FLX) to a large DNA virus allowed the precise delineation of the 59 and 39 extremities of Mimivirus mRNAs and revealed 75 new transcripts including several noncoding RNAs. Mimivirus genes are expressed across a wide dynamic range, in a finely regulated manner broadly described by three main temporal classes: early, intermediate, and late. This RNA-seq study confirmed the AAAATTGA sequence as an early promoter element, as well as the presence of palindromes at most of the polyadenylation sites. It also revealed a new promoter element correlating with late gene expression, which is also prominent in Sputnik, the recently described Mimivirus ''virophage.'' These results-validated genome-wide by the hybridization of total RNA extracted from infected Acanthamoeba cells on a tiling array (Agilent)-will constitute the foundation on which to build subsequent functional studies of the Mimivirus/Acanthamoeba system.

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“…After the discovery of a unique vertex for herpes simplex virus (HSV) (15) and mimivirus (12,16), to the best of our knowledge, PBCV-1 is the third icosahedral, eukaryotic virus that has been recognized to have a unique vertex. It would therefore be possible that many more icosahedral eukaryotic viruses may require unique vertices for the successful execution of their life cycle.…”

mentioning

confidence: 99%

“…Some icosahedral viruses, including tailed bacteriophages, HSV (15,23), mimivirus (12,16), and PRD1 (21,24), have a specialized pentameric vertex that is associated with genomic packaging and/or cell entry. Even the small icosahedral poliovirus has or develops a special pentameric vertex when delivering its genome to its host (25).…”

mentioning

confidence: 99%

An icosahedral algal virus has a complex unique vertex decorated by a spike

Cherrier

Kostyuchenko

Xiao

et al. 2009

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

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Paramecium bursaria Chlorella virus-1 is an icosahedrally shaped, 1,900-Å-diameter virus that infects unicellular eukaryotic green algae. A 5-fold symmetric, 3D reconstruction using cryoelectron microscopy images has now shown that the quasiicosahedral virus has a unique vertex, with a pocket on the inside and a spike structure on the outside of the capsid. The pocket might contain enzymes for use in the initial stages of infection. The unique vertex consists of virally coded proteins, some of which have been identified. Comparison of shape, size, and location of the spike with similar features in bacteriophages T4 and P22 suggests that the spike might be a cell-puncturing device. Similar asymmetric features may have been missed in previous analyses of many other viruses that had been assumed to be perfectly icosahedral.5-fold averaging ͉ cryoelectron microscopy reconstruction ͉ Paramecium bursaria Chlorella virus-1 ͉ cell entry ͉ specialized vertex protein

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Distinct DNA Exit and Packaging Portals in the Virus Acanthamoeba polyphaga mimivirus

Cited by 164 publications

References 37 publications

Vaccinia-like cytoplasmic replication of the giant Mimivirus

Vaccinia-like cytoplasmic replication of the giant Mimivirus

mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus

An icosahedral algal virus has a complex unique vertex decorated by a spike

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