Altered budding site of a pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells

Tashiro, Masato; Yamakawa, Makoto; Tobita, Kiyotake; Seto, J. T.; Klenk, Hans Dieter; Rott, R.

doi:10.1128/jvi.64.10.4672-4677.1990

Cited by 56 publications

(42 citation statements)

References 27 publications

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“…Basolateral virus release is thought to contribute to systemic spread, while apical virus shedding from the epithelia causes primarily local infections restricted to mucosal surfaces. In keeping with this model, the budding of wild-type SeV is restricted to the apical surface and thus causes a local respiratory infection, while mutation in the M protein has been shown to disrupt the cellular polarity and cause bipolar budding of the virus, resulting in a systemic infection in mice (40,41). In the case of the MuV infection, apical release supports efficient virus replication in the glandular epithelium, especially the parotid gland, and virus shedding in saliva, leading to person-to-person transmission.…”

Section: Discussionmentioning

confidence: 95%

Mumps Virus Is Released from the Apical Surface of Polarized Epithelial Cells, and the Release Is Facilitated by a Rab11-Mediated Transport System

Katoh

Nakatsu

Kubota

et al. 2015

J Virol

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Mumps virus (MuV) is an airborne virus that causes a systemic infection in patients.In vivo, the epithelium is a major replication site of MuV, and thus, the mode of MuV infection of epithelial cells is a subject of interest. Our data in the present study showed that MuV entered polarized epithelial cells via both the apical and basolateral surfaces, while progeny viruses were predominantly released from the apical surface. In polarized cells, intracellular transport of viral ribonucleoprotein (vRNP) complexes was dependent on Rab11-positive endosomes, and vRNP complexes were transported to the apical membrane. Expression of a dominant negative form of Rab11 (Rab11S25N) reduced the progeny virus release in polarized cells but not in nonpolarized cells. Although in this way these effects were correlated with cell polarity, Rab11S25N did not modulate the direction of virus release from the apical surface. Therefore, our data suggested that Rab11 is not a regulator of selective apical release of MuV, although it acts as an activator of virus release from polarized epithelial cells. In addition, our data and previous studies on Sendai virus, respiratory syncytial virus, and measles virus suggested that selective apical release from epithelial cells is used by many paramyxoviruses, even though they cause either a systemic infection or a local respiratory infection. IMPORTANCE Mumps virus (MuV) is the etiological agent of mumps and causes a systemic infection.However, the precise mechanism by which MuV breaks through the epithelial barriers and achieves a systemic infection remains unclear. In the present study, we show that the entry of MuV is bipolar, while the release is predominantly from the apical surface in polarized epithelial cells. In addition, the release of progeny virus was facilitated by a Rab11-positive recycling endosome and microtubule network. Our data provide important insights into the mechanism of transmission and pathogenesis of MuV. Mumps is a common childhood illness characterized by painful swelling of the parotid glands and is often accompanied by severe complications such as orchitis, aseptic meningitis, pancreatitis, and deafness (1). However, despite the prevalence and seriousness of the disease, the molecular basis of the pathogenesis of mumps is still poorly understood.Mumps virus (MuV), which belongs to the genus Rubulavirus within the family Paramyxoviridae, is the causative agent of mumps (2). The virus infection of cells is initiated by the binding of the hemagglutinin-neuraminidase (HN) protein to sialic acids of the cell surface (3). After receptor binding, the fusion (F) protein induces pH-independent fusion of the viral envelope with the host plasma membrane, and the viral genomic RNA is released into the cytoplasm (4). The viral genomic RNA encapsidated by the nucleocapsid (N) protein forms an active template for RNA replication and transcription, a viral ribonucleoprotein (vRNP), with viral polymerases composed of the phosphoprotein (P protein) and large (L) protein (5...

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Section: Discussionmentioning

confidence: 95%

Mumps Virus Is Released from the Apical Surface of Polarized Epithelial Cells, and the Release Is Facilitated by a Rab11-Mediated Transport System

Katoh

Nakatsu

Kubota

et al. 2015

J Virol

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“…As epithelial cells are primary target cells for coronaviruses such as PEDV and also essential entities required for virus pathogenesis (Tashiro et al, 1990), we explored the interaction of PEDV with polarized Vero E6 cells and IECs. Our data demonstrate that PEDV enters Vero E6 and IECs preferentially via the apical plasma membrane and is also released from this site of polarized epithelial cells.…”

Section: Discussionmentioning

confidence: 99%

Porcine aminopeptidase N mediated polarized infection by porcine epidemic diarrhea virus in target cells

Cong

Bai

et al. 2015

Virology

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a b s t r a c tInfection of polarized intestinal epithelial cells by porcine epidemic diarrhea virus (PEDV) was characterized. Indirect immunofluorescence assay, real-time PCR, and transmission electron microscopy confirmed PEDV can be successfully propagated in immortalized swine small intestine epithelial cells (IECs). Infection involved porcine aminpeptidase N (pAPN), a reported cellular receptor for PEDV, transient expression of pAPN and siRNA targeted pAPN increased and decreased the infectivity of PEDV in IECs, respectively. Subsequently, polarized entry into and release from both Vero E6 and IECs was analyzed. PEDV entry into polarized cells and pAPN grown on membrane inserts occurs via apical membrane. The progeny virus released into the medium was also quantified which demonstrated that PEDV is preferentially released from the apical membrane. Collectively, our data demonstrate that pAPN, the cellular receptor for PEDV, mediates polarized PEDV infection. These results imply the possibility that PEDV infection may proceed by lateral spread of virus in intestinal epithelial cells.

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“…Many viruses exploit this polarization by recognizing receptor molecules that are localized at the respective site of contact with the epithelial layer (7,11,32). It is further speculated that virus dissemination either by lateral cell-to-cell fusion or by polarized virus release from epithelia contributes to virulence (5,9,13,30).…”

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confidence: 99%

Canine Distemper Virus Matrix Protein Influences Particle Infectivity, Particle Composition, and Envelope Distribution in Polarized Epithelial Cells and Modulates Virulence

Dietzel

Anderson

Castan

et al. 2011

J Virol

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In paramyxoviruses, the matrix (M) protein mediates the interaction between the envelope and internal proteins during particle assembly and egress. In measles virus (MeV), M mutations, such as those found in subacute sclerosing panencephalitis (SSPE) strains, and differences in vaccine and wild-type M proteins can affect the strength of interaction with the envelope glycoproteins, assembly efficiency, and spread. However, the contribution of the M protein to the replication and pathogenesis of the closely related canine distemper virus (CDV) has not been characterized. To this end this, we generated a recombinant wild-type CDV carrying a vaccine strain M protein. The recombinant virus retained the parental growth phenotype in VerodogSLAMtag cells, but displayed an increased particle-to-infectivity ratio very similar to that of the vaccine strain, likely due to inefficient H protein incorporation. Even though infectious virus was released only from the apical surface, consistent with the release polarity of the wild-type CDV strain, envelope protein distribution in polarized epithelial cells reproduced the bipolar pattern seen in vaccine strain-infected cells. Most notably, the chimeric virus was completely attenuated in ferrets and caused only a mild and transient leukopenia, indicating that the differences in particle infectivity and envelope protein sorting mediated by the vaccine M protein contribute importantly to vaccine strain attenuation.Morbilliviruses are enveloped negative-strand RNA viruses that cause severe disease in their respective hosts. Pathogenesis studies of measles virus (MeV) in nonhuman primates and canine distemper virus (CDV) in ferrets reveal that wild-type strains initially target immune cells and then spread to epithelia and in some cases to the central nervous system (6,23,34). This dissemination requires the transition of the respiratory mucosa at the initial infection stage, subsequent spread to lymphoid and epithelial tissues throughout the body, and finally virus release via the epithelia of the respiratory, gastrointestinal, and urinary tracts for shedding and transmission.Polarized epithelia form barriers that separate compartments within the organism, as well as the organism and the environment (22). Consequently, replication in epithelia constitutes an integral part of the life cycle of many viruses. The polarization of the epithelial layer results in distinct apical and basolateral domains that are separated by tight junctions, and membrane proteins are transported to the apical or basolateral surface based on sorting signals in their sequences (14). Many viruses exploit this polarization by recognizing receptor molecules that are localized at the respective site of contact with the epithelial layer (7,11,32). It is further speculated that virus dissemination either by lateral cell-to-cell fusion or by polarized virus release from epithelia contributes to virulence (5, 9, 13, 30).The matrix (M) protein plays an essential role in paramyxovirus assembly by mediating the interac...

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Altered budding site of a pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells

Abstract: A protease activation mutant of Sendai virus, Fl-R, causes a systemic infection in mice, whereas wild-type virus is exclusively pneumotropic (M.

Cited by 56 publications

References 27 publications

Mumps Virus Is Released from the Apical Surface of Polarized Epithelial Cells, and the Release Is Facilitated by a Rab11-Mediated Transport System

Mumps Virus Is Released from the Apical Surface of Polarized Epithelial Cells, and the Release Is Facilitated by a Rab11-Mediated Transport System

Porcine aminopeptidase N mediated polarized infection by porcine epidemic diarrhea virus in target cells

Canine Distemper Virus Matrix Protein Influences Particle Infectivity, Particle Composition, and Envelope Distribution in Polarized Epithelial Cells and Modulates Virulence

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