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Houghton, J. W.

Publications and source records attributed to Houghton, J. W..

10 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↗

Discovery of stereoselective targeted covalent inhibitors of the RAB27-effector protein-protein interaction

RAB27A and RAB27B are homologous small GTPases that regulate intracellular vesicle trafficking, orchestrating endocytic and exocytic processes that affect cellular communication, immune responses, and dynamics of the cellular microenvironment. Through their interactions with effector proteins, RAB27A/B play roles in tumor metastasis and chronic inflammation. However, pharmacological modulation of their activity faces challenges typical of small GTPases, including a lack of well-defined pockets outside the conserved GTP binding site, and large RAB27-effector protein-protein interaction (PPI) surfaces. Here, we present the discovery and development of the first cell-active, rationally designed covalent inhibitors of the RAB27-effector interaction, targeting a non-conserved cysteine residue flanking the PPI interface. An electrophile-first biochemical screen led to a novel class of acrylamide covalent inhibitors, and X-ray crystallography structure-guided design led to optimized inhibitors and probes that enantioselectively target RAB27A/B-Cys123 in cells. Potency and selectivity were confirmed through biochemical and cellular assays, including chemical proteomics and phenotype recapitulation in melanocytes alongside a matched inactive enantioprobe control. In contrast, a previously reported compound, Nexinhib-20, was found to be toxic and to exert its activity through non-selective reactivity. This work provides the first toolbox of cell-active chemical probes for RAB27 which can be used in future studies to shed light on the function of this protein and its potential as a therapeutic target.

biochemistry↗

A host ATPase essential for rhinovirus replication is an antiviral target with a high barrier to resistance

Rhinoviruses are the leading cause of acute respiratory illnesses and comprise more than 170 types that constantly circulate in humans worldwide. Beyond common colds, rhinoviruses can trigger severe symptoms, particularly in young children, older adults and people with asthma or chronic obstructive pulmonary disease. Despite their clinical and socio-economic impact, no approved vaccine or antiviral treatment exist. Here, we uncovered the interaction of the host AAA+ ATPase RUVBL1/2 with rhinovirus non-structural protein 2C and we demonstrated that RUVBL1/2 is strictly and specifically required for the replication of the viral RNA of the most prevalent and pathogenic rhinovirus species. Pharmacological inhibition of RUVBL1/2 ATPase activity efficiently inhibited rhinovirus replication in a human nasal epithelium model, even post-infection. Moreover, serial viral passaging in the presence of a RUVBL1/2 inhibitor did not lead to the emergence of resistance. These findings reveal an unexpected and strong host dependency with promising potential for antiviral targeting.

microbiology↗

The translatome of quiescent Plasmodium falciparum gametocytes reveals parasite pyridoxal 5'-phosphate (PLP) biosynthesis is essential for efficient mosquito stage development

The ability of Plasmodium falciparum gametocytes to remain quiescent within the vertebrate host but poised for rapid onward development in the mosquito is an adaptation essential to maximise the onward spread of malaria. In this dormant state, mature infectious stage V gametocytes are largely unaffected by most antimalarial drugs and our limited understanding of how gametocytes prepare for mosquito transmission has hindered the identification of new molecular targets for transmission-blocking therapeutics. In this study, we move beyond the total proteome of gametocytes and define the translatome of mature stage V gametocytes using L-azidohomoalanine incorporation into nascent proteins, click chemistry purification and proteomic analysis. We identify the proteins and pathways that gametocytes sustain in preparation for transmission during this dormant period and through genetic disruption, we validate this approach by demonstrating the importance of parasite pyridoxal 5-phosphate biosynthesis for mosquito transmission.

microbiology↗

obABPP-HT*: A Precision-Engineered Activity Proteomics Pipeline for the Streamlined Discovery of Deubiquitinase Inhibitors

Deubiquitinases (DUBs), and the dysregulation thereof, are implicated in human disease. The recent inclusion of selective DUB inhibitors in clinical trials has heightened interest in DUB-focused drug discovery. Current DUB screening methods remain constrained, however, as they often rely on recombinant proteins that are truncated or derived from non-human sources, typically necessitating extensive optimisation of initial hits. We introduce a high-throughput, endogenous human DUB-focused activity proteomics workflow designed for the simultaneous screening and profiling of small, targeted libraries of catalytic group-reactive compounds. In a proof-of-concept screen, this innovative platform expanded the repertoire of electrophilic groups targeting DUBs, leading to the discovery of potent and selective inhibitors for USP47, OTUD7B, and USP5. Remarkably, these inhibitors required minimal or no optimisation to confirm the previously reported biological roles of the three DUBs, underscoring the advantages of this methodology for drug discovery applications.

biochemistry↗

A spatiotemporally resolved GPCR interactome reveals novel mediators of receptor agonism

Cellular signaling by membrane G protein-coupled receptors (GPCRs) is orchestrated by a complex and diverse array of mechanisms. The dynamics of a GPCR interactome as it evolves over time and space in response to an agonist can offer a unique window on pleiotropic signaling decoding and functional selectivity at a cellular level. In this study, we employed proximity-based APEX2 proteomics to interrogate the interaction network of the GPCR for luteinizing hormone (LHR) on a minute-to-minute timescale. We developed an analytical approach integrating quantitative multiplexed proteomics and temporal reference profiles, providing a platform to identify the proteomic environment of APEX2-tagged LHR at the nanometer scale. LHR activity is exquisitely regulated at a spatial level, leading to identification of novel putative interactors including the Ras-related GTPase RAP2B that modulate both receptor signaling and post-endocytic trafficking, and providing a resource for spatiotemporal nanodomain mapping of LHR interactors across subcellular compartments. SignificanceG-protein coupled receptors (GPCRs) are the largest family of membrane proteins in the human body. GPCRs have established themselves as key drug targets, playing central roles in health and disease. The activity of this superfamily of receptors is highly dynamic, integrating diverse signaling pathways over time and across multiple subcellular compartments. Quantitative proximity proteomics using engineered ascorbate peroxidase (APEX2) has emerged as a powerful tool to map GPCR-protein interaction landscapes in both time and space. However, resolving these networks at a sub-minute timescale remains challenging, particularly for poorly characterized GPCRs with limited pharmacological tools or complex trafficking patterns. In this study, we applied APEX2 proximity proteomics to resolve at nanoscale the agonist (LH)-induced interactome of the luteinizing hormone receptor (LHR), a key GPCR in human reproduction. LHR undergoes rapid endocytosis upon LH stimulation, trafficking to a poorly understood compartment termed the very early endosome (VEE), where it engages in G protein signaling and post-endocytic sorting. Harnessing the temporal profile of GIPC1 protein, a key known interactor of LHR in the VEE pathway, we developed an analytical pipeline to identify novel endocytic interactors of LHR. Using our platform, we identified RAP2B and RAB38 as potential modulators of LHR signaling and trafficking. Overall, we present an APEX2 pipeline optimized for interrogating complex datasets, particularly for GPCRs, and potentially other membrane receptors, with limited known interactome data and minimal pharmacological tools. Our findings highlight both the complexity of GPCR interaction networks and an effective strategy to deconvolute them, providing a comprehensive resource to advance understanding of this large family of receptors. O_FIG O_LINKSMALLFIG WIDTH=199 HEIGHT=200 SRC="FIGDIR/small/599010v2_ufig1.gif" ALT="Figure 1"> View larger version (71K): org.highwire.dtl.DTLVardef@13badf7org.highwire.dtl.DTLVardef@11a5182org.highwire.dtl.DTLVardef@dd5453org.highwire.dtl.DTLVardef@cb2c27_HPS_FORMAT_FIGEXP M_FIG C_FIG

biochemistry↗

HOXA9 forms a repressive complex with nuclear matrix-associated protein SAFB to maintain acute myeloid leukemia

HOXA9 is commonly upregulated in acute myeloid leukemia (AML), where it confers poor prognosis. Characterising the protein interactome of endogenous HOXA9 in human AML, we identified a chromatin complex of HOXA9 with the nuclear matrix attachment protein-SAFB. SAFB perturbation phenocopied HOXA9 knockout to decrease AML proliferation, increase differentiation and apoptosis in vitro and prolonged survival in vivo. Integrated genomic, transcriptomic and proteomic analyses further demonstrated that the HOXA9-SAFB-chromatin complex associates with NuRD and HP1{gamma} to repress the expression of factors associated with differentiation and apoptosis, including NOTCH, CEBP{delta}, S100A8, and CDKN1A. Chemical or genetic perturbation of NuRD and HP1{gamma} catalytic activity also triggered differentiation, apoptosis and the induction of these tumor-suppressive genes. Importantly, this mechanism is operative in other HOXA9-dependent AML genotypes. This mechanistic insight demonstrates active HOXA9-dependent differentiation block as a potent mechanism of disease maintenance in AML, that may be amenable to therapeutic intervention via therapies targeting the HOXA9/SAFB interface and/or NuRD and HP1{gamma} activity. Key Points- Identification of the endogenous human HOXA9 protein interactome in AML - HOXA9 forms a repressive complex with S/MAR binding protein (SAFB) that is critical for the maintenance of AML by facilitating proliferation and preventing differentiation and cell death. - The HOXA9/SAFB (H9SB) complex represses gene expression via recruitment of NuRD and HP1{gamma}.

cancer biology↗

Agonists of orally expressed TRP channels stimulate salivary secretion and modify the salivary proteome

Natural compounds that can stimulate salivary secretion are of interest in developing treatments for xerostomia, the perception of a dry mouth, that affects between 10 and 30% of the adult and elderly population. Chemesthetic transient receptor potential (TRP) channels are expressed in the surface of the oral mucosa. The TRPV1 agonists capsaicin and piperine have been shown to increase salivary flow when introduced into the oral cavity but the sialogogic properties of other TRP channel agonists have not been investigated. In this study we have determined the influence of different TRP channel agonists on the flow and protein composition of saliva.Mouth rinsing with the TRPV1 agonist nonivamide or menthol, a TRPM8 agonist, increased whole mouth saliva (WMS) flow and total protein secretion compared to unstimulated saliva, the vehicle control mouth rinse or cinnamaldehyde, a TRPA1 agonist. Nonivamide also increased the flow of labial minor gland saliva but parotid saliva flow rate was not increased. The influence of TRP channel agonists on the composition and function of the salivary proteome was investigated using a multi-batch quantitative mass spectrometry method novel to salivary proteomics. Inter-personal and inter-mouth rinse variation was observed in the secreted proteomes and, using a novel bioinformatics method, inter-day variation was identified with some of the mouth rinses. Significant changes in specific salivary proteins were identified after all mouth rinses. In the case of nonivamide, these changes were attributed to functional shifts in the WMS secreted, primarily the over representation of salivary and non-salivary cystatins which was confirmed by immunoassay.This study provides new evidence of the impact of TRP channel agonists on the salivary proteome and the stimulation of salivary secretion by a TRPM8 channel agonist, which suggests that TRP channel agonists are potential candidates for developing treatments for sufferers of xerostomia.AbbreviationsCARD10CAspase Recruitment Domain-containing protein 10DTTDiThioThreitolLC-MS/MSLiquid Chromatography - tandem Mass SpectrometryGOGene OntologyIEFIsoElectric FocusingLDSLithium Dodecyl SulphateMSMass SpectrometryPGPropylene GlycolPGK1PhosphoGlycerate Kinase 1TCEPTris (2-CarboxyEthyl) PhosphineTEABTriEthylAmmonium BicarbonateTMTTandem Mass TagTRPTransient Receptor PotentialTRPA1Transient Receptor Potential cation channel, subfamily A, member 1TRPM8Transient Receptor Potential cation channel subfamily M member 8TRPV1Transient Receptor Potential cation channel subfamily V member 1WMSWhole Mouth SalivaUWMSUnstimulated Whole Mouth SalivaView Full Text

physiology↗

ABHD11 regulates 2-oxoglutarate abundance by protecting mitochondrial lipoylated proteins from lipid peroxidation damage

2-oxoglutarate (2-OG or -ketoglutarate) relates mitochondrial metabolism to cell function by modulating the activity of 2-OG dependent dioxygenases (2-OG DDs) involved in the hypoxia response and DNA/histone modifications. However, metabolic pathways that regulate these oxygen and 2-OG sensitive enzymes remain poorly understood. Here, using CRISPR Cas9 genome-wide mutagenesis to screen for genetic determinants of 2-OG levels, we uncover a redox sensitive mitochondrial lipoylation pathway, dependent on the mitochondrial hydrolase ABHD11, that signals changes in mitochondrial 2-OG metabolism to 2-OG DD function. ABHD11 loss or inhibition drives a rapid increase in 2-OG levels by impairing lipoylation of the 2-OG dehydrogenase complex (OGDHc) - the rate limiting step for mitochondrial 2-OG metabolism. Rather than facilitating lipoate conjugation, ABHD11 protects the catalytic lipoyl domain from lipid peroxidation products formed by oxidative damage, demonstrating a requirement for a lipoyl repair pathway in human cells, and highlighting how the redox sensitivity of lipoylation modulates 2-OG metabolism.

cell biology↗

Structure of herpes simplex virus pUL7:pUL51, a conserved complex required for efficient herpesvirus assembly

Herpesviruses are an ancient family of highly-prevalent human and animal pathogens that acquire their membrane envelopes in the cytoplasm of infected cells. While multiple conserved viral proteins are known to be required for efficient herpesvirus production, many of these proteins lack identifiable structural homologues and the molecular details of herpesvirus assembly remain unclear. We have characterized the complex of assembly proteins pUL7 and pUL51 from herpes simplex virus (HSV)-1, an -herpesvirus, using multi-angle light scattering and small-angle X-ray scattering with chemical crosslinking. HSV-1 pUL7 and pUL51 form a stable 1:2 complex that is capable of higher-order oligomerization in solution. We solved the crystal structure of this complex, revealing a core heterodimer comprising pUL7 bound to residues 41-125 of pUL51. While pUL7 adopts a previously-unseen compact fold, the extended helix-turn-helix conformation of pUL51 resembles the cellular endosomal complex required for transport (ESCRT)-III component CHMP4B, suggesting a direct role for pUL51 in promoting membrane scission during virus assembly. We demonstrate that the interaction between pUL7 and pUL51 homologues is conserved across human -, {beta}- and {gamma}-herpesviruses, as is their association with trans-Golgi membranes in cultured cells. However, pUL7 and pUL51 homologues do not form complexes with their respective partners from different virus families, suggesting that the molecular details of the interaction interface have diverged. Our results demonstrate that the pUL7:pUL51 complex is conserved across the herpesviruses and provide a structural framework for understanding its role in herpesvirus assembly.\n\nSignificance StatementHerpesviruses are extremely common human pathogens that cause diseases ranging from cold sores to cancer. Herpesvirus acquire their membrane envelope in the cytoplasm via a conserved pathway, the molecular details of which remain unclear. We have solved the structure of a complex between herpes simplex virus (HSV)-1 proteins pUL7 and pUL51, two proteins that are required for efficient HSV-1 assembly. We show that formation of this complex is conserved across distantly-related human herpesviruses, as is the association of these homologues with cellular membranes that are used for virion assembly. While pUL7 adopts a previously-unseen fold, pUL51 resembles key cellular membrane-remodeling complex components, suggesting that the pUL7:pUL51 complex may play a direct role in deforming membranes to promote virion assembly.

microbiology↗