Coxsackievirus infection in skeletal muscles of mice an electron microscopic study II. Appearance and fate of virus progeny

Bienz, Kurt; Bienz-Isler, Gertrud; Egger, Denise; Weiss, Marianne; Loeffler, H.

doi:10.1007/bf01253760

Cited by 9 publications

(10 citation statements)

References 22 publications

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“…The pathogenesis and morphogenesis of the Nodamura virus observed in the larvae of G. rnellonella are similar to those described for the picornaviruses of vertebrates (7,9,13,14,15) or of invertebrates (3,25,30). The difference resides mainly in the variety of the hosts, both vertebrates and invertebrates, and in the tissue sensitivity to the Nodamura virus.…”

Section: Discussionmentioning

confidence: 73%

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Morphogenesis of the Nodamura virus in the larvae of the lepidopteranGalleria mellonella (L.)

Garzón

Charpentier

Kurstak

1978

Archives of Virology

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The pathogenesis and morphogenesis of the Nodamura virus, an insect picorna- virus which can also infect vertebrates such as newborn mice, are described in the larvae of G. mellonella. Examination of thin sections of muscle, salivary and moulting glands, hemocytes adipose tissue and hypodermis of the infected larvae of G. mellonella shows in the cytoplasm the accumulation of viral particles either dispersed or in a stringlike or paracrystalline array. These arrays of virions can be within membrane- bound vesicles. Helical filaments of 110 A of diameter can be observed inside the basal membranes and later in the cytoplasm, in relation to the infection of muscular or adipose tissues. The morphogenesis of Nodamura virus in G. mellonella or in suckling mice is very similar to that of the Coxsackie A virus observed in the mouse.

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Section: Discussionmentioning

confidence: 73%

“…The nucleus does not seem to play as an important role as in the infection with some picornaviruses (2,7,8,9).…”

Section: Discussionmentioning

confidence: 90%

Morphogenesis of the Nodamura virus in the larvae of the lepidopteranGalleria mellonella (L.)

Garzón

Charpentier

Kurstak

1978

Archives of Virology

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“…The viruses are found, successively, in string-like arrays between two smooth unit membranes, in different arrangements of 2, 3 or more rows of vesicle-bound virions, in filled vesicles and in unbound tracts [3,16,17]. Non-mitochondrial membranes are also closely associated with the replication of polioviruses [11] or coxsackie viruses [7] and may represent the site of translation and encapsidation of viral RNA for these picornaviruses [6,38]. Attempts to isolate the RNA polymerase resulted in the separation of polymerase-membrane complexes for nodaviruses [19], picornaviruses [37], and several plant viruses [12,39].…”

Section: Discussionmentioning

confidence: 99%

“…In G. mellonella salivary and moulting glands, hemocytes, adipose tissue, and hypodermis show a viral replication in association with membranes, mainly from the smooth reticulum endoplasmic, very similar to that of the family Picornaviridae [7,18], but close relationship with mitochondria was also observed in the NV-infected cells [ 17].…”

Section: Introductionmentioning

confidence: 97%

Implication of mitochondria in the replication of Nodamura virus in larvae of the Lepidoptera,Galleria mellonella (L.) and in suckling mice

Garzón

Strykowski

Charpentier

1990

Archives of Virology

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The replication of Nodamura virus, type species of the family Nodaviridae, takes place principally into the interfibrillar spaces of the sarcoplasm in close association with mitochondria in the infected muscles of both G. mellonella and suckling mice. The most striking event in infection of G. mellonella muscle cells was the aggregation and shape modification of numerous mitochondria (elongation, interdigitation, and vesiculation) at an early stage of infection. These clusters of mitochondria were cemented by a thick electron-dense material at the periphery of which viral particles undergo maturation process. In a later stage, degenerated and dilated mitochondria showed a clear assembling of virus particles on their outer membrane and occasionally on some inner membranes. These facts and the localization of RNA by RNase-gold technique in the assembling sites of viruses around and inside the mitochondria allowed us to postulate a role for the mitochondria as supports and/or energy suppliers for viral RNA synthesis and translation.

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“…The source of the membranes varies with the virus: many viral RCs are associated with modified membranes derived from the endoplasmic reticulum (ER), including members of the arteri-, bromo-, corona-, flavi-, and picornavirus families (20)(21)(22)(23)(24)(25)(26)(27)(28)(29). However, the RCs of other virus families localize to membranes derived from other organelles, including chloroplasts and peroxisomes (tombusviruses), endosomes and lysosomes (togaviruses), and mitochondria (tombus-and nodaviruses) (30)(31)(32)(33)(34).…”

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confidence: 99%

Two Membrane-Associated Regions within the Nodamura Virus RNA-Dependent RNA Polymerase Are Critical for both Mitochondrial Localization and RNA Replication

Gant

Moreno

Varela-Ramı́rez

et al. 2014

J Virol

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Viruses with positive-strand RNA genomes amplify their genomes in replication complexes associated with cellular membranes. Little is known about the mechanism of replication complex formation in cells infected with Nodamura virus. This virus is unique in its ability to lethally infect both mammals and insects. In mice and in larvae of the greater wax moth (Galleria mellonella), Nodamura virus-infected muscle cells exhibit mitochondrial aggregation and membrane rearrangement, leading to disorganization of the muscle fibrils on the tissue level and ultimately in hind limb/segment paralysis. However, the molecular basis for this pathogenesis and the role of mitochondria in Nodamura virus infection remains unclear. Here, we tested the hypothesis that Nodamura virus establishes RNA replication complexes that associate with mitochondria in mammalian cells. Our results showed that Nodamura virus replication complexes are targeted to mitochondria, as evidenced in biochemical, molecular, and confocal microscopy studies. More specifically, we show that the Nodamura virus RNA-dependent RNA polymerase interacts with the outer mitochondrial membranes as an integral membrane protein and ultimately becomes associated with functional replication complexes. These studies will help us to understand the mechanism of replication complex formation and the pathogenesis of Nodamura virus for mammals. IMPORTANCEThis study will further our understanding of Nodamura virus (NoV) genome replication and its pathogenesis for mice. NoV is unique among the Nodaviridae in its ability to infect mammals. Here we show that NoV establishes RNA replication complexes (RCs) in association with mitochondria in mammalian cells. These RCs contain newly synthesized viral RNA and feature a physical interaction between mitochondrial membranes and the viral RNA-dependent RNA polymerase (RdRp), which is mediated by two membrane-associated regions. While the nature of the interaction needs to be explored further, it appears to occur by a mode distinct from that described for the insect nodavirus Flock House virus (FHV). The interaction of the NoV RdRp with mitochondrial membranes is essential for clustering of mitochondria into networks that resemble those described for infected mouse muscle and that are associated with fatal hind limb paralysis. This work therefore provides the first link between NoV RNA replication complex formation and the pathogenesis of this virus for mice.

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Coxsackievirus infection in skeletal muscles of mice an electron microscopic study II. Appearance and fate of virus progeny

Cited by 9 publications

References 22 publications

Morphogenesis of the Nodamura virus in the larvae of the lepidopteranGalleria mellonella (L.)

Morphogenesis of the Nodamura virus in the larvae of the lepidopteranGalleria mellonella (L.)

Implication of mitochondria in the replication of Nodamura virus in larvae of the Lepidoptera,Galleria mellonella (L.) and in suckling mice

Two Membrane-Associated Regions within the Nodamura Virus RNA-Dependent RNA Polymerase Are Critical for both Mitochondrial Localization and RNA Replication

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