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Biology subjects

Marsh, G. A.

Publications and source records attributed to Marsh, G. A..

6 recordsLinked to original sources

A protective bispecific antibody targets both Nipah virus surface glycoproteins and limits viral escape

Nipah virus (NiV) and Hendra virus (HeV) are highly pathogenic henipaviruses without approved human vaccines or therapies. Here, we report on a highly potent bispecific therapeutic that combines an anti-fusion (F) nanobody with an anti-receptor binding protein (RBP) antibody to deliver a dual-targeting biologic that is resistant to viral escape. We show that the nanobody, DS90, engages a unique, conserved site within prefusion F of NiV and HeV, and provides neutralization and complete protection from NiV disease. Bispecific engineering of DS90 with the anti-RBP mAb m102.4 results in neutralization, elimination of viral escape and superior protection from NiV disease compared to leading monovalent approaches. These findings carry implications for the development of cross-neutralizing immunotherapies that limit the emergence of henipaviral escape mutants.

microbiology↗

Antagonism of STAT3 signalling by Ebola virus

Many viruses target signal transducers and activators of transcription (STAT) 1 and 2 to antagonise antiviral interferon (IFN) signalling, but targeting of signalling by other STATs/cytokines, including STAT3/interleukin (IL-) 6 that regulate processes important to Ebola virus (EBOV) haemorrhagic fever, is poorly defined. We report that EBOV potently inhibits STAT3 responses to IL-6 family cytokines, and that this is mediated by the IFN-antagonist VP24. Mechanistic analysis indicates that VP24 effects a unique strategy combining distinct karyopherin-dependent and karyopherin-independent mechanisms to antagonise STAT3-STAT1 heterodimers and STAT3 homodimers, respectively. This appears to reflect distinct mechanisms of nuclear trafficking of the STAT3 complexes, revealed for the first time by our analysis of VP24 function. These findings are consistent with major roles for global inhibition of STAT3 signalling in EBOV infection, and provide new insights into the molecular mechanisms of STAT3 nuclear trafficking, significant to pathogen-host interactions, cell physiology and pathologies such as cancer. Author summaryEbola virus (EBOV) continues to pose a significant risk to human health globally, causing ongoing disease outbreaks with case-fatality rates between 40 and 60%. Suppression of immune responses is a critical component of EBOV haemorrhagic fever, but understanding of EBOV impact on signalling by cytokines other than interferon is limited. We find that infectious EBOV inhibits interleukin-6 cytokine signalling via antagonism of STAT3. The antagonistic strategy uniquely combines two distinct mechanisms, which appear to reflect differing nuclear trafficking mechanisms of critical STAT3 complexes. This provides fundamental insights into the mechanisms of pathogenesis of a lethal virus, and biology of STAT3, a critical player in immunity, development, growth and cancer.

microbiology↗

Bats Possess Unique Variants of the Antiviral Restriction Factor Tetherin

Bats are recognised as important reservoirs of viruses deadly to other mammals, including humans. These infections are typically non-pathogenic in bats raising questions about host response differences that might exist between bats and other mammals. Tetherin is a restriction factor which inhibits the release of a diverse range of viruses from host cells, including retroviruses, coronaviruses, filoviruses, and paramyxoviruses, some of which are deadly to humans and transmitted by bats. Here we characterise the tetherin genes from 27 species of bats, revealing that they have evolved under strong selective pressure, and that fruit bats and vesper bats express unique structural variants of the tetherin protein. Tetherin was widely and variably expressed across fruit bat tissue-types and upregulated in spleen tissue when stimulated with Toll-like receptor agonists. The expression of two computationally predicted splice isoforms of fruit bat tetherin was verified. We identified an additional third unique splice isoform which includes a C-terminal region that is not homologous to known mammalian tetherin variants but was functionally capable of restricting the release of filoviral virus-like particles. We also report that vesper bats possess and express at least five tetherin genes, including structural variants, a greater number than any other mammal reported to date. These findings support the hypothesis of differential antiviral gene evolution in bats relative to other mammals.

evolutionary biology↗

Filoviruses Can Efficiently Infect Human Neuron-Like Cells Without Genetic Adaptation

Recent large-scale Ebola outbreaks, combined with improved follow-up of survivors, has permitted the observation of common long-term neurological sequelae in patients that have survived Ebola virus infection. To date there have been few studies into neurological infections by Ebola or related filoviruses, however, recent studies have isolated infectious virus from patients cerebrospinal fluid months after being discharged from the treatment facility. In order to determine whether different filoviruses were capable of infecting human neurons, the human neuroblastoma cell lines, SH-SY5Y and M17, were chemically-differentiated into more neuron-like cells using established protocols. The neuron-like profiles of the differentiated cells were confirmed by the determination of expression of a range of neuron-specific markers. Zaire ebolavirus, Reston ebolavirus, and Marburg virus were serially-passaged in both cell lines to determine permissiveness of the cells, as well as permit the acquisition of adaptive mutations in the viral genomes. Whilst Marburg virus grew to high titres in both cell lines, Zaire ebolavirus only grew in SH-SY5Y cells, and Reston ebolavirus rapidly died out in both cell lines. Whole-genome sequencing of the passaged viruses revealed two consensus-level non-coding mutations in the SH-SY5Y-passaged Marburg virus. Viral growth kinetics were determined for pre- and post-passaging Zaire ebolavirus and Marburg virus in both human neuronal cell lines, as well as the human hepatocyte cell line, Huh7. Growth kinetics were similar for both the pre- and post-passaged viruses, suggesting that adaptive mutations were not required for efficient growth in these cells. This study is the first to demonstrate that filoviruses are capable of infecting human neuron-like cells in a species-specific manner. Marburg virus-infected cells remained alive up to Day 21 post-infection, suggesting that long-term neurological sequelae following filovirus infection may be a result of direct neuronal infection, and that infection of neurons might contribute to viral persistence in survivors. Author SummaryFiloviruses, including Ebola and Marburg viruses, have been traditionally considered "haemorrhagic fever" viruses, with infections causing bleeding and frequently death. Recent large-scale outbreaks in Africa have challenged these assumptions due to a significant number of patients reporting neurological symptoms sometimes months after infection. In many of these patients, virus was present at detectable levels in the fluid surrounding the brain. There has been significant debate about the ability of Ebola and Marburg viruses to infect and grow in human neurons (brain cells), and evidence has been lacking due to the lack of feasibility in taking brain samples. Our study demonstrates that both Zaire ebolavirus and Marburg virus are capable of infecting cells derived from human brains without needing to change, and without killing the cells. Reston ebolavirus, a related virus that appears not to cause disease in humans, was not able to grow efficiently in these cells. Our findings show that these viruses might be capable of living in the brains of survivors for long periods of time, similar to previous observations in the eye and testes. In addition, the response of the body to these infected cells might account for the neurological symptoms described by patients.

microbiology↗

Pan-filovirus one-step reverse transcription-polymerase chain reaction screening assay

Five species within the genera Ebolavirus and Marburgvirus of the family Filoviridae are known to cause severe hemorrhagic fever with high mortality rates in humans and non-human primates. Recent large outbreaks of Ebola virus disease in West Africa (2014 - 2016) and the Democratic Republic of the Congo (2018 - ongoing) have demonstrated the epidemic potential with devastating public health consequences. Several known and novel filovirus species have been found in bats in recent years. However, the role of each virus species in the disease ecology of human disease is still unclear. In particular, the transmission mechanism from potential animal hosts to humans is not known. Therefore, a simple, flexible, cost-effective screening tool for detecting the presence of any (putative) member of the filovirus family in animal samples is needed. In this study, a one-step conventional pan-filovirus RT-PCR assay was developed. The designed universal consensus primers of this screening test target two highly conserved regions of the nucleoprotein (NP) of all currently known filoviruses. The assay was capable of specific amplification of viral RNA of all six primate-pathogenic (human and non-human) filovirus species and resulted in 317 bp long RT-PCR products. This amplicon length renders the assay suitable for flexible application as conventional reverse transcription polymerase chain reaction (RT-PCR) as well as for future use as rapid real-time quantitative reverse transcription polymerase chain reaction (RT-qPCR).

molecular biology↗

Viral hijacking of the nucleolar DNA-damage response machinery: a novel mechanism to regulate host cell biology

Recent landmark studies indicate that nucleoli play critical roles in the DNA-damage response (DDR) via interaction of DDR machinery including NBS1 with nucleolar Treacle protein, a key mediator of ribosomal RNA (rRNA) transcription and processing, implicated in Treacher-Collins syndrome. Here, using proteomics, confocal/super-resolution imaging, and infection under BSL-4 containment, we present the first report that this nucleolar DDR pathway is targeted by infectious pathogens. We find that Treacle has antiviral activity, but that matrix protein of Henipaviruses and P3 protein of rabies virus, highly pathogenic viruses of the order Mononegavirales, interact with Treacle and inhibit its function, thereby silencing rRNA biogenesis, consistent with mimicking NBS1-Treacle interaction during a DDR. These data identify a novel mechanism for viral modulation of host cells by appropriating the nucleolar DDR; this appears to have developed independently in different viruses, and represents, to our knowledge, the first direct intra-nucleolar function for proteins of any mononegavirus.

microbiology↗