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Article ; Online: The Mouse Cytomegalovirus G Protein-Coupled Receptor Homolog, M33, Coordinates Key Features of

Ma, Jiawei / Bruce, Kimberley / Davis-Poynter, Nicholas / Stevenson, Philip G / Farrell, Helen E

2021 Volume 96, Issue 4, Page(s) e0186721

Abstract: Common to all cytomegalovirus (CMV) genomes analyzed to date is the presence of G protein-coupled receptors (GPCR). Animal models of CMV provide insights into their role in viral fitness. The mouse cytomegalovirus (MCMV) GPCR, M33, facilitates dendritic ... ...

Abstract	Common to all cytomegalovirus (CMV) genomes analyzed to date is the presence of G protein-coupled receptors (GPCR). Animal models of CMV provide insights into their role in viral fitness. The mouse cytomegalovirus (MCMV) GPCR, M33, facilitates dendritic cell (DC)-dependent viremia, the extravasation of blood-borne infected DCs to the salivary gland, and the frequency of reactivation events from latently infected tissue explants. Constitutive G protein-coupled M33 signaling is required for these phenotypes, although the contribution of distinct biochemical pathways activated by M33 is unknown. M33 engages G
MeSH term(s)	Animals ; Cyclic AMP Response Element-Binding Protein/metabolism ; Dendritic Cells/virology ; GTP-Binding Protein alpha Subunits, Gi-Go/metabolism ; Herpesviridae Infections/metabolism ; Herpesviridae Infections/virology ; Lymph Nodes/virology ; Mice ; Mice, Inbred BALB C ; Muromegalovirus/genetics ; Muromegalovirus/metabolism ; Muromegalovirus/physiology ; Mutation ; Phospholipase C beta/metabolism ; Receptors, G-Protein-Coupled/genetics ; Receptors, G-Protein-Coupled/metabolism ; Salivary Glands/virology ; Signal Transduction ; Viral Proteins/genetics ; Viral Proteins/metabolism ; Viremia/metabolism ; Viremia/virology ; Virus Activation/genetics
Chemical Substances	Creb1 protein, mouse ; Cyclic AMP Response Element-Binding Protein ; Receptors, G-Protein-Coupled ; Viral Proteins ; Phospholipase C beta (EC 3.1.4.11) ; Plcb1 protein, mouse (EC 3.1.4.11) ; GTP-Binding Protein alpha Subunits, Gi-Go (EC 3.6.5.1)
Language	English
Publishing date	2021-12-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.01867-21
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Article ; Online: The Cytoplasmic C-Tail of the Mouse Cytomegalovirus 7 Transmembrane Receptor Homologue, M78, Regulates Endocytosis of the Receptor and Modulates Virus Replication in Different Cell Types.

Davis-Poynter, Nick / Yunis, Joseph / Farrell, Helen E

PloS one

2016 Volume 11, Issue 10, Page(s) e0165066

Abstract: Virus homologues of seven-transmembrane receptors (7TMR) are encoded by all beta- and gammaherpesviruses, suggesting important functional roles. M78 of mouse cytomegalovirus (MCMV) is representative of a family of 7TMR conserved in all betaherpesviruses. ...

Abstract	Virus homologues of seven-transmembrane receptors (7TMR) are encoded by all beta- and gammaherpesviruses, suggesting important functional roles. M78 of mouse cytomegalovirus (MCMV) is representative of a family of 7TMR conserved in all betaherpesviruses. M78 family members have been found to exhibit cell-type specific effects upon virus replication in tissue culture and to affect virus pathogenesis in vivo. We reported previously that M78, for which no ligands are known, undergoes rapid, constitutive endocytosis. In this study, we have investigated the role of the M78 cytoplasmic C-tail in mediating endocytosis and consequences of C-tail deletion upon replication and pathogenesis. Mutations of M78 (C-tail truncations or point mutations) and CCR5-M78 chimeras identified two distinct regions affecting endocytosis. The first was a classical acidic di-leucine motif (DDxxxLL), located close to the C-terminus. The second region, the activity of which was suppressed by downstream sequences, included the putative 8th helix, located close to the 7th transmembrane domain. A recombinant MCMV expressing an endocytosis-deficient M78, lacking most of the C-tail (M78_CΔ155), had a cell-type specific replication phenotype. M78_CΔ155 had restricted replication in bone marrow macrophages, indistinguishable from an M78-null recombinant. In contrast, M78_CΔ155 replicated normally or with enhanced titres to wild type virus in other tested cell-types, whereas M78-null was attenuated. Distinct phenotypes for M78_CΔ155 and M78-null suggest that the C-tail deletion resulted in M78 dysfunction, rather than complete loss of function; furthermore, they highlight a cell-type specific role of M78 during replication. Infection of mice (intranasal) demonstrated that M78_CΔ155, similar to M78-null, was cleared more rapidly from the lungs than wild type virus and was severely attenuated for replication in salivary glands. It may be speculated that attenuation of both M78_CΔ155 and M78-null for replication in macrophages may have contributed to their similar pathogenic phenotypes.
MeSH term(s)	Animals ; Cell Line ; Endocytosis ; HeLa Cells ; Humans ; Macrophages, Alveolar/virology ; Mice ; Muromegalovirus/physiology ; Protein Domains ; Protein Structure, Secondary ; Receptors, G-Protein-Coupled/chemistry ; Receptors, G-Protein-Coupled/genetics ; Receptors, G-Protein-Coupled/metabolism ; Sequence Deletion ; Viral Proteins/chemistry ; Viral Proteins/genetics ; Viral Proteins/metabolism ; Virus Replication
Chemical Substances	Receptors, G-Protein-Coupled ; Viral Proteins ; seven-transmembrane G-protein-coupled receptor
Language	English
Publishing date	2016
Publishing country	United States
Document type	Journal Article
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0165066
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Article ; Online: Human cytomegalovirus US28 allows dendritic cell exit from lymph nodes.

Farrell, Helen E / Bruce, Kimberley / Ma, Jiawei / Davis-Poynter, Nicholas / Stevenson, Philip G

The Journal of general virology

2018 Volume 99, Issue 11, Page(s) 1509–1514

Abstract: Human cytomegalovirus (HCMV) colonizes blood-borne dendritic cells (DCs). They express US28, a viral G protein-coupled receptor (GPCR). In vitro functions have been described for US28, but how it contributes to host colonization has been unclear. The ... ...

Abstract	Human cytomegalovirus (HCMV) colonizes blood-borne dendritic cells (DCs). They express US28, a viral G protein-coupled receptor (GPCR). In vitro functions have been described for US28, but how it contributes to host colonization has been unclear. The murine CMV (MCMV) M33 GPCR promotes DC recirculation. We show that US28 shares this function. Thus, DC recirculation is also available to HCMV via US28, and inhibiting US28 G protein-dependent signalling has the potential to reduce systemic infection. We show that M33 also promotes systemic infection through infected DC extravasation.
MeSH term(s)	Animal Structures/virology ; Animals ; Cell Movement ; Cells, Cultured ; Cytomegalovirus/growth & development ; Cytomegalovirus/pathogenicity ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/veterinary ; Cytomegalovirus Infections/virology ; Dendritic Cells/immunology ; Dendritic Cells/virology ; Host-Pathogen Interactions ; Humans ; Lymph Nodes/immunology ; Lymph Nodes/virology ; Mice, Inbred BALB C ; Muromegalovirus/growth & development ; Receptors, Chemokine/metabolism ; Viral Proteins/metabolism
Chemical Substances	Receptors, Chemokine ; US28 receptor, Cytomegalovirus ; Viral Proteins
Language	English
Publishing date	2018-09-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	219316-4
ISSN	1465-2099 ; 0022-1317
ISSN (online)	1465-2099
ISSN	0022-1317
DOI	10.1099/jgv.0.001154
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Article ; Online: Murine cytomegalovirus degrades MHC class II to colonize the salivary glands.

Yunis, Joseph / Farrell, Helen E / Bruce, Kimberley / Lawler, Clara / Sidenius, Stine / Wyer, Orry / Davis-Poynter, Nicholas / Stevenson, Philip G

PLoS pathogens

2018 Volume 14, Issue 2, Page(s) e1006905

Abstract: Cytomegaloviruses (CMVs) persistently and systemically infect the myeloid cells of immunocompetent hosts. Persistence implies immune evasion, and CMVs evade CD8+ T cells by inhibiting MHC class I-restricted antigen presentation. Myeloid cells can also ... ...

Abstract	Cytomegaloviruses (CMVs) persistently and systemically infect the myeloid cells of immunocompetent hosts. Persistence implies immune evasion, and CMVs evade CD8+ T cells by inhibiting MHC class I-restricted antigen presentation. Myeloid cells can also interact with CD4+ T cells via MHC class II (MHC II). Human CMV (HCMV) attacks the MHC II presentation pathway in vitro, but what role this evasion might play in host colonization is unknown. We show that Murine CMV (MCMV) down-regulates MHC II via M78, a multi-membrane spanning viral protein that captured MHC II from the cell surface and was necessary although not sufficient for its degradation in low pH endosomes. M78-deficient MCMV down-regulated MHC I but not MHC II. After intranasal inoculation, it showed a severe defect in salivary gland colonization that was associated with increased MHC II expression on infected cells, and was significantly rescued by CD4+ T cell loss. Therefore MCMV requires CD4+ T cell evasion by M78 to colonize the salivary glands, its main site of long-term shedding.
MeSH term(s)	Animals ; BALB 3T3 Cells ; Cells, Cultured ; Cricetinae ; Embryo, Mammalian ; HEK293 Cells ; Histocompatibility Antigens Class II/metabolism ; Humans ; Immune Evasion ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Muromegalovirus/immunology ; Muromegalovirus/physiology ; NIH 3T3 Cells ; Proteolysis ; Salivary Glands/immunology ; Salivary Glands/metabolism ; Salivary Glands/pathology ; Salivary Glands/virology
Chemical Substances	Histocompatibility Antigens Class II
Language	English
Publishing date	2018
Publishing country	United States
Document type	Journal Article
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1006905
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Article: Introduction: virus stealth strategies.

Davis-Poynter, N J

Seminars in cell & developmental biology

1998 Volume 9, Issue 3, Page(s) 319

MeSH term(s)	Animals ; Humans ; Viruses/immunology
Language	English
Publishing date	1998-06
Publishing country	England
Document type	Journal Article
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1006/scdb.1998.0240
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Zs.A 2918: Show issues

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Article ; Online: Murine Cytomegalovirus Glycoprotein O Promotes Epithelial Cell Infection

Yunis, Joseph / Farrell, Helen E / Bruce, Kimberley / Lawler, Clara / Wyer, Orry / Davis-Poynter, Nicholas / Brizić, Ilija / Jonjić, Stipan / Adler, Barbara / Stevenson, Philip G

Journal of virology

2019 Volume 93, Issue 3

Abstract: Cytomegaloviruses (CMVs) establish systemic infections across diverse cell types. Glycoproteins that alter tropism can potentially guide their spread. Glycoprotein O (gO) is a nonessential fusion complex component of both human CMV (HCMV) and murine CMV ( ...

Abstract	Cytomegaloviruses (CMVs) establish systemic infections across diverse cell types. Glycoproteins that alter tropism can potentially guide their spread. Glycoprotein O (gO) is a nonessential fusion complex component of both human CMV (HCMV) and murine CMV (MCMV). We tested its contribution to MCMV spread from the respiratory tract.
MeSH term(s)	Animals ; Cells, Cultured ; Epithelial Cells/metabolism ; Epithelial Cells/virology ; Fibroblasts/metabolism ; Fibroblasts/virology ; Herpesviridae Infections/metabolism ; Herpesviridae Infections/virology ; Lung/metabolism ; Lung/virology ; Membrane Glycoproteins/metabolism ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Muromegalovirus/pathogenicity ; Viral Envelope Proteins/metabolism ; Virus Internalization ; Virus Replication
Chemical Substances	Membrane Glycoproteins ; Viral Envelope Proteins ; glycoprotein O, cytomegalovirus
Language	English
Publishing date	2019-01-17
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.01378-18
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Article ; Online: Luciferase-tagged wild-type and tropism-deficient mouse cytomegaloviruses reveal early dynamics of host colonization following peripheral challenge.

Farrell, Helen / Oliveira, Martha / Macdonald, Kate / Yunis, Joseph / Mach, Michael / Bruce, Kimberley / Stevenson, Philip / Cardin, Rhonda / Davis-Poynter, Nicholas

The Journal of general virology

2016 Volume 97, Issue 12, Page(s) 3379–3391

Abstract: Cytomegaloviruses (CMVs) establish persistent, systemic infections and cause disease by maternal-foetal transfer, suggesting that their dissemination is a key target for antiviral intervention. Late clinical presentation has meant that human CMV (HCMV) ... ...

Abstract	Cytomegaloviruses (CMVs) establish persistent, systemic infections and cause disease by maternal-foetal transfer, suggesting that their dissemination is a key target for antiviral intervention. Late clinical presentation has meant that human CMV (HCMV) dissemination is not well understood. Murine CMV (MCMV) provides a tractable model. Whole mouse imaging of virus-expressed luciferase has proved a useful way to track systemic infections. MCMV, in which the abundant lytic gene M78 was luciferase-tagged via a self-cleaving peptide (M78-LUC), allowed serial, unbiased imaging of systemic and peripheral infection without significant virus attenuation. Ex vivo luciferase imaging showed greater sensitivity than plaque assay, and revealed both well-known infection sites (the lungs, lymph nodes, salivary glands, liver, spleen and pancreas) and less explored sites (the bone marrow and upper respiratory tract). We applied luciferase imaging to tracking MCMV lacking M33, a chemokine receptor conserved in HCMV and a proposed anti-viral drug target. M33-deficient M78-LUC colonized normally in peripheral sites and local draining lymph nodes but spread poorly to the salivary gland, suggesting a defect in vascular transport consistent with properties of a chemokine receptor.
MeSH term(s)	Animals ; Cytomegalovirus/genetics ; Cytomegalovirus/growth & development ; Cytomegalovirus/physiology ; Cytomegalovirus Infections/virology ; Female ; Genes, Reporter ; Humans ; Luciferases/genetics ; Luciferases/metabolism ; Mice ; Mice, Inbred BALB C ; Molecular Imaging ; Recombinant Fusion Proteins/genetics ; Recombinant Fusion Proteins/metabolism ; Viral Proteins/genetics ; Viral Proteins/metabolism ; Viral Tropism
Chemical Substances	Recombinant Fusion Proteins ; Viral Proteins ; Luciferases (EC 1.13.12.-)
Keywords	covid19
Language	English
Publishing date	2016-10-26
Publishing country	England
Document type	Journal Article
ZDB-ID	219316-4
ISSN	1465-2099 ; 0022-1317
ISSN (online)	1465-2099
ISSN	0022-1317
DOI	10.1099/jgv.0.000642
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Article ; Online: Transneuronal tracing of airways-related sensory circuitry using herpes simplex virus 1, strain H129.

McGovern, A E / Davis-Poynter, N / Farrell, M J / Mazzone, S B

Neuroscience

2012 Volume 207, Page(s) 148–166

Abstract: Sensory input from the airways to suprapontine brain regions contributes to respiratory sensations and the regulation of respiratory function. However, relatively little is known about the central organization of this higher brain circuitry. We exploited ...

Abstract	Sensory input from the airways to suprapontine brain regions contributes to respiratory sensations and the regulation of respiratory function. However, relatively little is known about the central organization of this higher brain circuitry. We exploited the properties of the H129 strain of herpes simplex virus 1 (HSV-1) to perform anterograde transneuronal tracing of the central projections of airway afferent nerve pathways. The extrathoracic trachea in Sprague-Dawley rats was inoculated with HSV-1 H129, and tissues along the neuraxis were processed for HSV-1 immunoreactivity. H129 infection appeared in the vagal sensory ganglia within 24 h and the number of infected cells peaked at 72 h. Brainstem nuclei, including the nucleus of the solitary tract and trigeminal sensory nuclei were infected within 48 h, and within 96 h infected cells were evident within the pons (lateral and medial parabrachial nuclei), thalamus (ventral posteromedial, ventral posterolateral, submedius, and reticular nuclei), hypothalamus (paraventricular and lateral nuclei), subthalamus (zona incerta), and amygdala (central and anterior amygdala area). At later times H129 was detected in cortical forebrain regions including the insular, orbital, cingulate, and somatosensory cortices. Vagotomy significantly reduced the number of infected cells within vagal sensory nuclei in the brainstem, confirming the main pathway of viral transport is through the vagus nerves. Sympathetic postganglionic neurons in the stellate and superior cervical ganglia were infected by 72 h, however, there was no evidence for retrograde transynaptic movement of the virus in sympathetic pathways in the central nervous system (CNS). These data demonstrate the organization of key structures within the CNS that receive afferent projections from the extrathoracic airways that likely play a role in the perception of airway sensations.
MeSH term(s)	Animals ; Axonal Transport/physiology ; Herpesvirus 1, Human/physiology ; Male ; Neuroanatomical Tract-Tracing Techniques/methods ; Neuronal Tract-Tracers/metabolism ; Rats ; Rats, Sprague-Dawley ; Sensory Receptor Cells/cytology ; Sensory Receptor Cells/metabolism ; Sensory Receptor Cells/virology ; Trachea/innervation ; Trachea/physiology ; Trachea/virology ; Visceral Afferents/cytology ; Visceral Afferents/metabolism ; Visceral Afferents/virology
Chemical Substances	Neuronal Tract-Tracers
Language	English
Publishing date	2012-04-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	196739-3
ISSN	1873-7544 ; 0306-4522
ISSN (online)	1873-7544
ISSN	0306-4522
DOI	10.1016/j.neuroscience.2012.01.029
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Zs.A 1215: Show issues

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Article: Analysis of the subcellular trafficking properties of murine cytomegalovirus M78, a 7 transmembrane receptor homologue.

Sharp, E L / Davis-Poynter, N J / Farrell, H E

The Journal of general virology

2009 Volume 90, Issue Pt 1, Page(s) 59–68

Abstract: Murine cytomegalovirus (MCMV) M78 is a member of the betaherpesvirus 'UL78 family' of seven transmembrane receptor (7TMR) genes. Previous studies of M78 and its counterpart in rat cytomegalovirus (RCMV) have suggested that these genes are required for ... ...

Abstract	Murine cytomegalovirus (MCMV) M78 is a member of the betaherpesvirus 'UL78 family' of seven transmembrane receptor (7TMR) genes. Previous studies of M78 and its counterpart in rat cytomegalovirus (RCMV) have suggested that these genes are required for efficient cell-cell spread of their respective viruses in tissue culture and demonstrated that gene knockout viruses are significantly attenuated for replication in vivo. However, in comparison with other CMV 7TMRs, relatively little is known about the basic biochemical properties and subcellular trafficking of the UL78 family members. We have characterized MCMV M78 in both transiently transfected and MCMV-infected cells to determine whether M78 exhibits features in common with cellular 7TMR. We obtained preliminary evidence that M78 formed dimers, a property that has been reported for several cellular 7TMR. M78 traffics to the cell surface, but was rapidly and constitutively endocytosed. Antibody feeding experiments demonstrated co-localization of M78 with markers for both the clathrin-dependent and lipid raft/caveolae-mediated internalization pathways. In MCMV-infected cells, the subcellular localization of M78 was modified during the course of infection, which may be related to the incorporation of M78 into the virion envelope during the course of virion maturation.
MeSH term(s)	Animals ; Cell Line ; Cells, Cultured ; Cricetinae ; Dimerization ; Endocytosis ; Humans ; Membrane Proteins/metabolism ; Mice ; Muromegalovirus/physiology ; Protein Transport ; Viral Proteins/metabolism
Chemical Substances	Membrane Proteins ; Viral Proteins
Language	English
Publishing date	2009-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	219316-4
ISSN	1465-2099 ; 0022-1317
ISSN (online)	1465-2099
ISSN	0022-1317
DOI	10.1099/vir.0.004853-0
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Article ; Online: Distinct brainstem and forebrain circuits receiving tracheal sensory neuron inputs revealed using a novel conditional anterograde transsynaptic viral tracing system.

McGovern, Alice E / Driessen, Alexandria K / Simmons, David G / Powell, Joseph / Davis-Poynter, Nicholas / Farrell, Michael J / Mazzone, Stuart B

The Journal of neuroscience : the official journal of the Society for Neuroscience

2015 Volume 35, Issue 18, Page(s) 7041–7055

Abstract: Sensory nerves innervating the mucosa of the airways monitor the local environment for the presence of irritant stimuli and, when activated, provide input to the nucleus of the solitary tract (Sol) and paratrigeminal nucleus (Pa5) in the medulla to drive ...

Abstract	Sensory nerves innervating the mucosa of the airways monitor the local environment for the presence of irritant stimuli and, when activated, provide input to the nucleus of the solitary tract (Sol) and paratrigeminal nucleus (Pa5) in the medulla to drive a variety of protective behaviors. Accompanying these behaviors are perceivable sensations that, particularly for stimuli in the proximal end of the airways, can be discrete and localizable. Airway sensations likely reflect the ascending airway sensory circuitry relayed via the Sol and Pa5, which terminates broadly throughout the CNS. However, the relative contribution of the Sol and Pa5 to these ascending pathways is not known. In the present study, we developed and characterized a novel conditional anterograde transneuronal viral tracing system based on the H129 strain of herpes simplex virus 1 and used this system in rats along with conventional neuroanatomical tracing with cholera toxin B to identify subcircuits in the brainstem and forebrain that are in receipt of relayed airway sensory inputs via the Sol and Pa5. We show that both the Pa5 and proximal airways disproportionately receive afferent terminals arising from the jugular (rather than nodose) vagal ganglia and the output of the Pa5 is predominately directed toward the ventrobasal thalamus. We propose the existence of a somatosensory-like pathway from the proximal airways involving jugular ganglia afferents, the Pa5, and the somatosensory thalamus and suggest that this pathway forms the anatomical framework for sensations arising from the proximal airway mucosa.
MeSH term(s)	Animals ; Brain Stem/chemistry ; Brain Stem/physiology ; Herpesvirus 1, Human ; Male ; Nerve Net/chemistry ; Nerve Net/physiology ; Neuroanatomical Tract-Tracing Techniques/methods ; Prosencephalon/chemistry ; Prosencephalon/physiology ; Rats ; Rats, Sprague-Dawley ; Sensory Receptor Cells/chemistry ; Sensory Receptor Cells/physiology ; Synapses/chemistry ; Synapses/physiology ; Trachea/chemistry ; Trachea/innervation ; Trachea/physiology
Language	English
Publishing date	2015-04-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.5128-14.2015
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