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Biology subjects

Smith, G. L.

Publications and source records attributed to Smith, G. L..

At least 19 recordsLinked to original sources

A phosphorylation-dependent mechanism controls splice variant-specific S-palmitoylation of cardiac Kv4.3

S-palmitoylation modulates the activity of many cardiac ion channels, yet the upstream signals that control this post-translational modification (PTM) are poorly defined. Here we identify a phosphorylation-dependent mechanism that governs splice variant-specific S-palmitoylation of the potassium channel Kv4.3. Using Acyl-RAC in native tissue and heterologous cells, we map palmitoylation to C546/547 in the intrinsically disordered Kv4.3 C-terminal tail. The short Kv4.3 splice variant Kv4.3S is [~]2.5-3-fold more palmitoylated than the long splice variant Kv4.3L, and systematic mutagenesis localises the dominant inhibitory determinant of Kv4.3 S-palmitoylation to residues 488-498 within the Kv4.3L-specific splice insert. KChIP2.1 promotes accumulation of a post-translationally modified Kv4.3 species that is selectively S-palmitoylated, and nanobody-targeted dephosphorylation removes this species and reduces Kv4.3 S-palmitoylation. Phos-tag electrophoresis and C-terminal truncation mapping identify S538 as the principal phosphorylation site enabling Kv4.3 S-palmitoylation; mutation of S538 markedly reduces formation of the palmitoylation-competent species. TurboID proximity-labelling and biochemical assays indicate that phosphorylation enhances recruitment of Kv4.3 to zDHHC5. Acute kinase inhibition rapidly eliminates phosphorylation but only gradually reduces palmitoylation, revealing temporal uncoupling between these PTMs. Functionally, non-palmitoylatable Kv4.3S exhibits larger peak currents, faster inactivation, and a left-shifted activation curve, consistent with palmitoylation limiting channel function and modulating gating transitions. Together, these findings identify phosphorylation of S538 as a priming modification that licenses Kv4.3 S-palmitoylation at C546/547, explain splice-variant differences in S-palmitoylation, and define a PTM cascade that tunes Kv4.3 channel behaviour.

cell biology↗

Random-forest segmentation and spatial analysis of injected cardiac spheroids in optically cleared myocardium

Accurate quantification of transplanted cardiac spheroids requires three-dimensional localisation within intact myocardium, yet this remains technically challenging. Optical clearing and light-sheet microscopy enable volumetric imaging of injection sites, but automated segmentation is difficult when transplanted spheroids and host tissue are labelled with the same fluorescent markers and cannot be separated by simple thresholding. We developed a random forest based pixel classification workflow for 3D detection of injected hiPSC derived cardiomyocyte and H9c2 spheroids in optically cleared rabbit myocardium. A supervised classifier trained on intensity, edge, and texture features generated a segmentation then grouped pixels via connected component analysis to reconstruct individual spheroids. The method showed good agreement with manual annotation and enabled automated extraction of spheroid size and spatial metrics. This accessible workflow enables reproducible three-dimensional quantification of transplanted spheroids in large light-sheet microscopy datasets and provides a practical route from volumetric imaging to spatial metrics in cardiac regeneration studies.

biophysics↗

Fluorescence-lifetime optical electrophysiology in contracting cardiomyocytes

Precise monitoring of cardiac electrophysiology in vitro is crucial to understanding heart function and cardiac disease. However, high-throughput, contact-free methods for directly measuring excitation-contraction coupling remain limited. Here, we introduce a new paradigm for quantitative electrophysiological imaging that combines fluorescence lifetime and intensity information to capture dynamic cardiac signals with high fidelity. We show that lifetime measurements are intrinsically decoupled from motion artifacts and provide calibrated calcium concentration and membrane potential readouts across wide fields of view. Using a gated single-photon avalanche diode camera, we acquire fluorescence lifetime images at up to 200 frames per second with sufficient signal-to-noise ratio such that each frame contains meaningful lifetime information without temporal averaging. This approach yields spatially resolved maps of absolute voltage and calcium values across contracting cardiomyocyte monolayers, revealing heterogeneous cell behaviors within individual assays and uncovering previously unreported dynamics during late-phase repolarization for real-time analysis of excitation-contraction coupling.

bioengineering↗

Mechanical de-skewing enables high-resolution imaging of thin tissue slices with a mesoSPIM light-sheet microscope

Optical clearing combined with light-sheet microscopy enables high-resolution imaging of extended tissue at scale. However, standard mesoSPIM systems are optimised for intact organs and are not suited to thin tissue slices. We present a no-shear imaging protocol using obliquely mounted samples held between refractive-index-matched slides in a 3D-printed frame. This enables mechanical de-skewing during acquisition, minimising post-processing requirements. We demonstrate feasibility in fluorescent bead phantoms and rabbit heart tissue, achieving a 4.8x reduction in processing time and a 1.5x improvement in axial resolution compared to the shear-method. The no-shear method extends mesoSPIMs utility to fragile, laterally extended tissue sections.

biophysics↗

Development of a replication-defective MPXV platform for fundamental and therapeutic research

The recent global outbreaks of mpox highlight the urgent need for both fundamental research and antiviral development. However, studying monkeypox virus (MPXV), with its large and complex genome, remains challenging due to the requirement for high-containment facilities. Here, we describe a novel strategy for de novo assembly of MPXV clade IIb genomes in bacterial artificial chromosomes using transformation-associated recombination cloning. Leveraging CRISPR-Cas9 and Lambda Red recombination, we engineered replication-defective MPXV particles with dual deletions of OPG96 (M2R) and OPG158 (A32.5L)--genes essential for virion assembly, that are capable of recapitulating key stages of the viral life cycle. Our work demonstrates the utility of replication-defective MPXV particles as a reliable platform for high-throughput antiviral discovery, offering significant advantages for both fundamental virology studies and therapeutic development against orthopoxviruses.

microbiology↗

Attenuation of the 2022 global outbreak monkeypox virus relative to its clade IIb ancestor

Monkeypox virus (MPXV) is a zoonotic virus endemic to Africa that has recently re-emerged, becoming the first orthopoxvirus with human-to-human transmission since smallpox eradication. The 2022 global epidemic of MPXV was caused by Clade IIb lineage B.1 virus that derives from the Clade IIb lineage A.1, which is endemic to West Africa1-3. Here we compared an early lineage B.1 virus with its closest earlier A.1 ancestor and show that despite only 46 nucleotide differences, lineage B.1 has attenuating phenotypic changes. Both B.1 and A.1 viruses replicated equivalently in cell culture, but B.1 had defects in long-range spread. MPXV B.1 also displayed defects in innate immune control, inducing higher IFN{beta}, innate immune signalling and MAPK gene expression, and a reduced capacity to suppress interleukin-1{beta}-mediated immune responses. Finally, MPXV B.1 had reduced virulence in a mouse model of MPXV infection relative to the ancestral A.1 endemic strain. Our work demonstrates biological differences between human circulating MPXV lineages that correlate with clinical observations documenting reduced in-host viral dissemination and disease severity for lineage B. Our data also reveal that the APOBEC3-like mutational footprint in MPXV is not only a signature of sustained human transmission but can also drive phenotypic changes.

microbiology↗

Automated measurement of cardiomyocyte monolayer contraction using the Exeter Multiscope

We apply a novel microscope architecture, the Exeter Multiscope, to the problem of acquiring image data in rapid succession from nine wells of a 96 well plate. We demonstrate that the new microscope can detect contraction in cardiomyocyte monolayers which have been plated into these wells. Each well is sampled using 500 x 500 pixels across a 1.4 x 1.4 mm field of view, acquired in three colours at 3.7 Hz per well. The use of multiple illumination wavelengths provides post-hoc focus selection, further increasing the level of automation. The performance of the Exeter Multiscope is benchmarked against industry standard methods using a commercial microscope with a motorised stage and demonstrates that the Multiscope can acquire data almost 40 times faster. The data from both Multiscope and the commercial systems are processed by a pixel variance algorithm that uses information from the pixel value variability over time to determine the timing and amplitude of tissue contraction. This algorithm is also benchmarked against an existing algorithm that employs an absolute difference measure of tissue contraction.

biophysics↗

A machine learning approach to predict drug-induced autoimmunity using transcriptional data.

Drug-induced autoimmunity (DIA) is an idiosyncratic adverse drug reaction. Although first reported in the mid-1940s, the mechanisms underlying DIA remain unclear, and there is little understanding of why it is only associated with some drugs. Because it only occurs in a small number of patients, DIA is not normally detected until a drug has reached the market. We describe an ensemble machine learning approach using transcriptional data to predict DIA. The genes comprising the signature implicate dysregulation of cell cycling or proliferation as part of the mechanism of DIA. This approach could be adapted by pharmaceutical companies as an additional preclinical safety screen, reducing the risk of drugs with the potential to cause autoimmunity reaching the market.

pharmacology and toxicology↗

The SARS-CoV-2 protein ORF3c is a mitochondrial modulator of innate immunity

The SARS-CoV-2 genome encodes a multitude of accessory proteins. Using comparative genomic approaches, an additional accessory protein, ORF3c, has been predicted to be encoded within the ORF3a sgmRNA. Expression of ORF3c during infection has been confirmed independently by ribosome profiling. Despite ORF3c also being present in the 2002-2003 SARS-CoV, its function has remained unexplored. Here we show that ORF3c localises to mitochondria during infection, where it inhibits innate immunity by restricting IFN-{beta} production, but not NF-{kappa}B activation or JAK-STAT signalling downstream of type I IFN stimulation. We find that ORF3c acts after stimulation with cytoplasmic RNA helicases RIG-I or MDA5 or adaptor protein MAVS, but not after TRIF, TBK1 or phospho-IRF3 stimulation. ORF3c co-immunoprecipitates with the antiviral proteins MAVS and PGAM5 and induces MAVS cleavage by caspase-3. Together, these data provide insight into an uncharacterised mechanism of innate immune evasion by this important human pathogen.

microbiology↗

Transcriptional reprogramming of natural killer cells by vaccinia virus shows both distinct and conserved features with mCMV

Natural killer (NK) cells have an established role in controlling poxvirus infection and there is a growing interest to exploit their capabilities in the context of poxvirus-based oncolytic therapy and vaccination. How NK cells recognise poxvirus-infected cells to become activated remains unclear. To address this knowledge gap, we studied the NK cell response to vaccinia virus (VACV) in vivo, using a systemic infection murine model. We found broad alterations in NK cells transcriptional activity in VACV-infected mice, consistent with both direct target cell recognition and cytokine exposure. There were also alterations in the expression levels of specific NK surface receptors (NKRs), including the Ly49 family and SLAM receptors, as well as upregulation of memory-associated NK markers. Despite the latter observation, adoptive transfer of NK memory populations did not confer protection from re-infection. Comparison with the NK cell response to murine cytomegalovirus (MCMV) infection highlighted common features, but also distinct NK transcriptional programmes initiated by VACV. Finally, there was a clear overlap between the NK transcriptional response in humans vaccinated with an attenuated VACV, modified vaccinia Ankara (MVA), demonstrating conservation between the NK response in these different host species. Overall, this study provides new data about NK cell activation, function, and homeostasis during VACV infection, and may have implication for the design of VACV-based therapeutics.

immunology↗

zDHHC5 expression is increased in cardiac hypertrophy and reduced in heart failure but this does not correlate with changes in substrate palmitoylation

S-palmitoylation is an essential lipid modification catalysed by zDHHC-palmitoyl acyltransferases that regulates the localisation and activity of substrates in every class of protein and tissue investigated to date. In the heart, S-palmitoylation regulates sodiumcalcium exchanger (NCX1) inactivation, phospholemman (PLM) inhibition of the Na+/K+ ATPase, Nav1.5 influence on membrane excitability and membrane localisation of heterotrimeric G-proteins. The cell surface localised enzyme zDHHC5 palmitoylates NCX1 and PLM and is implicated in injury during anoxia/reperfusion. Information is lacking about how palmitoylation remodels in cardiac diseases. We investigated expression of zDHHC5 in animal models of left ventricular hypertrophy (LVH) and heart failure (HF), along with HF tissue from humans. zDHHC5 expression was rapidly elevated during onset of LVH, whilst HF was associated with decreased zDHHC5 expression. Paradoxically, palmitoylation of the zDHHC5 substrate NCX1 was significantly reduced in LVH but increased in human HF. Overexpression of zDHHC5 in rabbit ventricular cardiomyocytes was not sufficient to drive changes in palmitoylation of zDHHC5 substrates or overall cardiomyocyte contractility, suggesting changes in zDHHC5 expression in disease may not be a primary driver of pathology. zDHHC5 itself is regulated by post-translational modifications, including palmitoylation in its Cterminal tail, and we found the palmitoylation of zDHHC5 may be increased in heart failure in the same manner as NCX1, suggesting additional regulatory mechanisms such as acyl-CoA availability may be involved. Importantly, this study provides the first evidence that palmitoylation of cardiac substrates is altered in the setting of HF, and that expression of zDHHC5 is dysregulated in both hypertrophy and HF.

biochemistry↗

Cardiac myosin binding protein-C palmitoylation is associated with increased myofilament affinity, reduced myofilament Ca2+ sensitivity and is increased in ischaemic heart failure.

Cardiac myosin binding protein-C (cMyBP-C) is an essential regulator of cardiac contractility through its interactions with the thick and thin filament. cMyBP-C is heavily influenced by post-translational modifications, including phosphorylation which improves cardiac inotropy and lusitropy, and S-glutathionylation, which impairs phosphorylation and is increased in heart failure. Palmitoylation is an essential cysteine modification that regulates the activity of cardiac ion channels and soluble proteins, however, its relevance to myofilament proteins has not been investigated. In the present study, we purified palmitoylated proteins from ventricular cardiomyocytes and identified that cardiac actin, myosin and cMyBP-C are palmitoylated. The palmitoylated form of cMyBP-C was more resistant to salt extraction from the myofilament lattice than the non-palmitoylated form. Isometric tension measurements suggest c-MyBP-C palmitoylation reduces myofilament Ca2+ sensitivity, with no change to maximum force or passive tension. Importantly, cMyBP-C palmitoylation levels are reduced at the site of injury in a rabbit model of heart failure but increased in samples from patients with ischaemic heart failure. Identification of cMyBP-C palmitoylation site revealed S-glutathionylated cysteines C635 and C651 are required for cMyBP-C palmitoylation, suggesting an interplay between the modifications at these sites. We conclude that structural and contractile proteins within the myofilament lattice are palmitoylated, with important functional consequences for cardiac contractile performance.

cell biology↗

The crystal structure of vaccinia virus protein E2 and perspectives on the prediction of novel viral protein folds

The morphogenesis of vaccinia virus (VACV, family Poxviridae), the smallpox vaccine, is a complex process involving multiple distinct cellular membranes and resulting in multiple different forms of infectious virion. Efficient release of enveloped virions, which promote systemic spread of infection within hosts, requires the VACV protein E2 but the molecular basis of E2 function remains unclear and E2 lacks sequence homology to any well-characterised family of proteins. We solved the crystal structure of VACV E2 to 2.3 [A] resolution, revealing that it comprises two domains with novel folds: an N-terminal annular (ring) domain and a C-terminal head domain. The C-terminal head domain displays weak structural homology with cellular (pseudo)kinases but lacks conserved surface residues or kinase features, suggesting that it is not enzymatically active, and possesses a large surface basic patch that might interact with phosphoinositide lipid headgroups. Recent deep learning methods have revolutionised our ability to predict the three-dimensional structures of proteins from primary sequence alone. VACV E2 is an exemplar difficult viral protein target for structure prediction, being comprised of multiple novel domains and lacking sequence homologues outside Poxviridae. AlphaFold2 nonetheless succeeds in predicting the structures of the head and ring domains with high and moderate accuracy, respectively, allowing accurate inference of multiple structural properties. The advent of highly accurate virus structure prediction marks a step-change in structural virology and beckons a new era of structurally-informed molecular virology.

microbiology↗

Selective modulation of cell surface proteins during vaccinia infection: implications for immune evasion strategies

The interaction between immune cells and virus-infected targets involves multiple plasma membrane (PM) proteins. A systematic study of PM protein modulation by vaccinia virus (VACV), the paradigm of host regulation, has the potential to reveal not only novel viral immune evasion mechanisms, but also novel factors critical in host immunity. Here, >1000 PM proteins were quantified throughout VACV infection, revealing selective downregulation of known T and NK cell ligands including HLA-C, downregulation of cytokine receptors including IFNAR2, IL-6ST and IL-10RB, and rapid inhibition of expression of certain protocadherins and ephrins, candidate activating immune ligands. Downregulation of most PM proteins occurred via a proteasome-independent mechanism. Upregulated proteins included a decoy receptor for TRAIL. Twenty VACV-encoded PM proteins were identified, of which five were not recognised previously as such. Collectively, this dataset constitutes a valuable resource for future studies on antiviral immunity, host-pathogen interaction, poxvirus biology, vector-based vaccine design and oncolytic therapy.

microbiology↗

Smallpox vaccination induces a substantial increase in commensal skin bacteria that promote pathology and enhance immunity

Interactions between pathogens, host microbiota and the immune system influence many physiological and pathological processes. In the 20th century, widespread dermal vaccination with vaccinia virus (VACV) led to the eradication of smallpox but how VACV interacts with the microbiota and whether this influences the efficacy of vaccination are largely unknown. Here we report that intradermal vaccination with VACV induces a large increase in the number of commensal bacteria in infected tissue, which enhance recruitment of inflammatory cells, promote tissue damage and increase immunity. Treatment of vaccinated specific-pathogen-free (SPF) mice with antibiotic, or infection of genetically-matched germ-free (GF) animals caused smaller lesions without alteration in virus titre. Tissue damage correlated with enhanced neutrophil and T cell infiltration and levels of pro-inflammatory tissue cytokines and chemokines. One month after vaccination, GF mice had reduced VACV-neutralising antibodies compared to SPF mice; while numbers of VACV-specific CD8+ T cells were equal in all groups of animals. Thus, skin microbiota may provide an adjuvant-like stimulus during vaccination with VACV. This observation has implications for dermal vaccination with live vaccines. Author SummarySmallpox was caused by variola virus and was eradicated by widespread dermal vaccination with vaccinia virus (VACV), a related orthopoxvirus of unknown origin. Eradication was declared in 1980 without an understanding of the immunological correlates of protection, or knowledge of the effect of smallpox vaccination on the local microbiota. Here we demonstrate that intradermal infection of mice with VACV induces a [~]1000-fold expansion of commensal skin bacteria that influence the recruitment of inflammatory cells into the infected tissue and enhance the size of the vaccination lesion. Antibiotic treatment reduced lesion size without changing virus titres. The bacterial expansion also contributes to the level of neutralizing antibodies at one month post vaccination, because genetically matched germ-free mice developed lower neutralizing antibodies than specific pathogen free controls. Thus, dermal infection by VACV enhanced bacterial growth and these bacteria promote pathology and enhance the antibody response. This finding has implication for dermal vaccination with live vaccines.

microbiology↗

A strategy to suppress STAT1 signalling conserved in pathogenic poxviruses and paramyxoviruses

The induction of interferon-stimulated genes by signal transducer and activator of transcription (STAT) proteins, is a critical host defence to fight virus infections. Here, a highly expressed poxvirus protein 018 is shown to inhibit IFN-induced signalling by binding the SH2 domain of STAT1 to prevent STAT1 association with an activated IFN receptor. Despite the presence of additional inhibitors of IFN-induced signalling, a poxvirus lacking 018 was attenuated in mice. The 2.0 [A] crystal structure of the 018:STAT1 complex reveals a mechanism for a high-affinity, pTyr-independent mode of binding to an SH2 domain. Furthermore, the STAT1 binding motif of 018 shows sequence similarity to the STAT1-binding proteins from Nipah virus, which like 018, block the association of STAT1 with an IFN receptor. Taken together, these results provide detailed mechanistic insight into a potent mode of STAT1 antagonism, found to exist in genetically diverse virus families.

microbiology↗

Viral mimicry of p65/RelA transactivation domain to inhibit NF-κB activation

Sensing of virus infection activates NF-{kappa}B to induce the expression of interferons, cytokines and chemokines to initiate the antiviral response. Viruses antagonise these antiviral defences by interfering with immune sensing and blocking the actions of antiviral and inflammatory molecules. Here, we show that a viral protein mimics the transactivation domain of the p65 subunit of NF-{kappa}B. The C terminus of vaccinia virus (VACV) protein F14 (residues 51-73) activates transcription when fused to a DNA-binding domain-containing protein and F14 associates with NF-{kappa}B co-activator CBP, disrupting p65-CBP interaction. Consequently, F14 diminishes CBP-mediated acetylation of p65 and the downstream recruitment of the transcriptional regulator BRD4 to the promoter of the NF-{kappa}B-responsive genes CXCL10 and CCL2, hence inhibiting their expression. Conversely, the recruitment of BRD4 to the promoters of NFKBIA, which encodes the inhibitor of NF-{kappa}B (I{kappa}B), and CXCL8 remains unaffected in the presence of either F14 or JQ1, a competitive inhibitor of BRD4 bromodomains, indicating its recruitment is acetylation-independent. Therefore, unlike other viral NF-{kappa}B antagonists, F14 is a selective inhibitor of NF-{kappa}B-dependent gene expression. A VACV strain lacking F14 showed that it contributes to virulence in an intradermal model of infection. Our results uncover a mechanism by which viruses disarm the antiviral defences through molecular mimicry of a conserved host protein and provide insight into the regulation of NF-{kappa}B-dependent gene expression by BRD4.

microbiology↗

Spir-1 promotes IRF3 activation and is targetted by vaccinia virus protein K7

Cellular proteins often have multiple and diverse functions. This is illustrated with protein Spir-1 that is an actin nucleator, but, as shown here, also functions to enhance IRF3 activation downstream of RNA sensing by RIG-I/MDA-5. In human and mouse cells lacking Spir-1, IRF3 activation is impaired, whereas Spir-1 overexpression enhanced IRF3 activation. Furthermore in Spir-1-/- cells, the infectious virus titres and sizes of plaques formed by two viruses that are sensed by RIG-I, vaccinia virus (VACV) and Zika virus, are increased. These observations demonstrate the biological importance of Spir-1 in the response to virus infection. Like cellular proteins, viral proteins also have multiple and diverse functions. Here, we also show that VACV virulence factor K7 binds directly to Spir-1 and that a diphenylalanine motif of Spir-1 is needed for this interaction and for Spir-1-mediated enhancement of IRF3 activation. Thus, Spir-1 is a new virus restriction factor and is targeted directly by an immunomodulatory viral protein that enhances virus virulence and diminishes IRF3 activation. Author SummaryInfection of cells by viruses is sensed by host molecules called pattern recognition receptors (PRRs) that activate signalling pathways leading to an anti-viral response. In turn, viruses express proteins that negate these host responses to mediate escape from the anti-viral response. Here, we report that protein K7 from a large DNA virus called vaccinia virus (VACV), binds to a host cell protein called Spir-1. Spir-1 is known to regulate the assembly of actin filaments inside cells, but here we show that Spir-1 also functions to activate the host response to virus infection and to limit the replication and spread of both RNA and DNA viruses. Thus, this study has uncovered new functions of cellular protein Spir-1 as an activator of innate immunity and as a restriction factor for diverse viruses. Further, it shows that Spir-1 is targeted by a virus protein during infection.

microbiology↗