Virus factories: associations of cell organelles for viral replication and morphogenesis

Novoa, Reyes R.; Calderita, Gloria; Arranz, Rocío; Fontana, Juan; Granzow, Harald; Risco, Cristina

doi:10.1042/bc20040058

Cited by 422 publications

(415 citation statements)

References 158 publications

(193 reference statements)

Supporting

Mentioning

407

Contrasting

Unclassified

Order By: Relevance

“…Nevertheless, a cytoplasmic cycle raises intriguing questions, because the nucleus provides an optimal, ready-made site for viral replication (1). Thus, an exclusive cytoplasmic infection necessitates de novo generation of a platform that confers the machinery, ingredients, and most significantly, elaborate architecture required for replication of large DNA viruses (26,27). The recently highlighted structural complexity of vaccinia cytoplasmic factories (22) renders the spatiotemporal features that characterize the factory of the larger and more complex Mimivirus into a particularly attractive case study in self-assembly.…”

Section: Discussionmentioning

confidence: 99%

Vaccinia-like cytoplasmic replication of the giant Mimivirus

Mutsafi¹,

Zauberman²,

Sabanay

et al. 2010

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

115

127

View full text Add to dashboard Cite

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...

show abstract

Section: Discussionmentioning

confidence: 99%

Vaccinia-like cytoplasmic replication of the giant Mimivirus

Mutsafi¹,

Zauberman²,

Sabanay

et al. 2010

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

115

127

View full text Add to dashboard Cite

show abstract

“…In such cases, the structures of the factory are enclosed by a membrane to exclude cellular organelles. Ribosomes are, however, present, and the factory is dedicated to viral genome replication and virion assembly (24,25). The eukaryotic viral factories were suggested to constitute the genuine identity of viruses (26), which thus might be considered as a specific type of living organisms (26,27).…”

Section: Discussionmentioning

confidence: 99%

A unique virus release mechanism in the Archaea

Bize

Karlsson

Ekefjärd

et al. 2009

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

124

172

View full text Add to dashboard Cite

Little is known about the infection cycles of viruses infecting cells from Archaea, the third domain of life. Here, we demonstrate that the virions of the archaeal Sulfolobus islandicus rod-shaped virus 2 (SIRV2) are released from the host cell through a mechanism, involving the formation of specific cellular structures. Large pyramidal virus-induced protrusions transect the cell envelope at several positions, rupturing the S-layer; they eventually open out, thus creating large apertures through which virions escape the cell. We also demonstrate that massive degradation of the host chromosomes occurs because of virus infection, and that virion assembly occurs in the cytoplasm. Furthermore, intracellular viral DNA is visualized by flow cytometry. The results show that SIRV2 is a lytic virus, and that the host cell dies as a consequence of elaborated mechanisms orchestrated by the virus. The generation of specific cellular structures for a distinct step of virus life cycle is known in eukaryal virus-host systems but is unprecedented in cells from other domains.lysis ͉ virus factory ͉ hyperthermophile ͉ infection cycle

show abstract

“…Noteworthy, and probably unique for hepadnaviral morphogenesis, is the peculiar mixture of strategies and elements, which are not only characteristic for DNA viruses, but also for RNA viruses. 20,43 The ultrastructural analysis of DHBV-infected hepatocytes in vitro and in vivo shows a strong reorganization of endomembranes, resulting in membrane-surrounded structures occupying large regions of the cytoplasm. This finding is consistent with seminal observations reported both for DHBV and HBV in previous ultrastructural studies.…”

Section: Discussionmentioning

confidence: 99%

Assembly and budding of a hepatitis B virus is mediated by a novel type of intracellular vesicles

et al. 2007

View full text Add to dashboard Cite

Formation of enveloped viruses involves assembly and budding at cellular membranes. In this study, we elucidated the morphogenesis of hepadnaviruses on the ultrastructural and biochemical level using duck hepatitis B virus (DHBV) as a model system. Formation of virus progeny initiates at the endoplasmic reticulum (ER) and is conserved both in vitro and in vivo. The morphogenesis proceeds via membrane-surrounded vesicles containing both virions and subviral particles, indicating a common morphogenetic pathway. The virus particle-containing vesicles (VCVs) are generated and maintained by reorganization of endomembranes accompanied by a striking disorganization of the rough ER (rER). DHBV-infected hepatocytes produce not only complete virions, but also large quantities of subviral particles (SVPs). SVPs are devoid of the nucleocapsid and viral DNA, 4,5 but contain the envelope proteins. The extracellular DHB virion has a spherical structure of approximately 45 to 65 nm and contains an electron-dense nucleocapsid of about 27 nm. 6 Little is known about the morphogenesis of this virus family, but several of the following features indicate that this process is likely to be unique and complex: the DHB viral envelope proteins are multispanning transmembrane proteins, encoded by a single open reading frame, whose differential transcription results in the large (L) and the small (S) surface protein. 7 Both proteins share an identical carboxyterminal region, representing the S protein, with an additional Nterminal extension forming the preS-region of L. The ratio between the L and S proteins in the viral particles is about 1:4. 8 As the major structural component of the envelope, the S protein determines envelope curvature and is indispensable for both budding and secretion of viral particles. 9 Both surface proteins are synthesized at the rough endoplasmic reticulum (ER), or rER, and then bud into the ER lumen, forming SVPs. This budding event is autonomous and independent of all other viral components (e.g., nucleocapsid). 10,11 The intrinsic membrane-deforming activity of hepadnaviral envelope proteins is host cell-independent and conserved from yeast to

show abstract

Virus factories: associations of cell organelles for viral replication and morphogenesis

Cited by 422 publications

References 158 publications

Vaccinia-like cytoplasmic replication of the giant Mimivirus

Vaccinia-like cytoplasmic replication of the giant Mimivirus

A unique virus release mechanism in the Archaea

Assembly and budding of a hepatitis B virus is mediated by a novel type of intracellular vesicles

Contact Info

Product

Resources

About