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Wilhelm, J.

Publications and source records attributed to Wilhelm, J..

At least 19 recordsLinked to original sources

Fast calcium-dependent fluorescent labeling for recording of neuronal activation

Calcium transients encode cellular and neuronal activity across timescales ranging from milliseconds to hours, yet linking these transient signals to downstream molecular states remains a major challenge. We recently introduced Caprola, a calcium-dependent protein labeling tool that converts calcium transients into permanent fluorescent marks for later analysis. In this way, Caprola enables tracking of neuronal activities in animal models as well as retrospective identification of labeled cells for isolation and transcriptomic analysis. However, the relatively slow labeling kinetics of Caprola required high concentrations of fluorophore probe and relatively long labeling times, which limits its sensitivity and applicability, in particular in vivo. To address this limitation, we generated Caprola variants with up to 29-fold faster labeling rates than their predecessor. We demonstrate that our new Caprola variants record calcium transients in cells and in zebrafish larval brains under conditions where previous Caprola variants did not show labeling. We further expand the applicability of Caprola to activity-dependent marking of postsynaptic compartments, opening new avenues for coupling functional activity histories with downstream molecular and transcriptomic analyses.

neuroscience↗

Glk1p is an actin fold metabolic enzyme whose polymerization is sensitive to nucleotide state

The actin fold is present in enzymes ranging from sugar kinases to chaperones. Previous work on the actin fold metabolic enzyme, glucokinase (Glk1p) in S. cerevisiae found it could form filaments in response to its substrates, ATP and glucose (Stoddard et al., 2020). Here, we have identified the product, glucose 6-phosphate (G6P), as a second trigger for Glk1p polymerization in vitro. Furthermore, the addition of ADP to G6P-Glk1p filaments causes filament disassembly, suggesting that polymerization is sensitive to the state of the bound nucleotide and/or the transfer of the gamma phosphate. We have also identified a specific metabolic state, the accumulation of G6P during stationary phase, that triggers Glk1p polymerization in vivo. While the structures of Glk1p filaments in either the ATP/glucose or G6P-bound form are not similar to conventional actin filaments, the sensitivity of assembly to the gamma phosphate of the nucleotide provides a conceptual bridge between the cytoskeleton and metabolic regulation via enzyme polymerization. SummaryThe yeast glucokinase, Glk1p, is an actin fold enzyme that undergoes regulated polymerization in response to ATP/glucose and glucose 6-phosphate (G6P). Elevated G6P during stationary phase triggers Glk1p filament assembly in vivo consistent with a role in regulating glycolytic flux.

cell biology↗

Fast and Luminous: CLIP-tag2

CLIP-tag is a self-labeling protein tag used for the specific fluorescence labeling of proteins. However, its low labeling speed and the poor cell permeability of its substrates result in low labeling efficiencies in live-cell applications. Here, we introduce a substrate optimized for live-cell applications, as well as an engineered CLIP-tag variant, CLIP-tag2, which reacts with the new substrate almost 1000-fold faster than the original CLIP-tag-substrate pair. CLIP-tag2 fusion proteins can be specifically and efficiently fluorescently labeled in cells within minutes at nanomolar substrate concentrations, and can be multiplexed with other self-labeling tags such as SNAP-tag2 and HaloTag7. These advances establish CLIP-tag2 as a powerful tagging platform for high-performance live-cell bioimaging.

biochemistry↗

Mitochondrial COX4I2 drives pericyte-dependent inflammation and emphysema

Chronic obstructive pulmonary disease (COPD) is characterized by neutrophilic inflammation, emphysema, and mild pulmonary hypertension (PH). Oxidative/nitrosative stress are key drivers, but specific mitochondrial mechanisms remain unclear. We show increased expression of the regulatory mitochondrial cytochrome c oxidase subunit 4 isoform 2 (COX4I2) in an early murine model and human COPD. After 8 months of cigarette smoke exposure, Cox4i2-/- mice were completely protected from emphysema but not from PH, associated with reduced nitrosative stress, inflammation, and apoptosis. Using a novel Cox4i2 reporter mouse and in situ hybridization of human lungs, COX4I2 was detected in precapillary ACTA2+ cells and capillary pericytes. COX4I2 promotes mitochondrial reactive oxygen species (mtROS) production in these cells, thereby enhancing neutrophil migration and alveolar type II cell apoptosis, and modulates angiogenesis. In contrast to Cox4i2-/-, mitochondria-targeted antioxidant MitoQ reversed emphysema and PH, suggesting pericyte-specific regulation of COPD pathologies and mtROS inhibition as a therapeutic approach in COPD. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=124 SRC="FIGDIR/small/703513v1_ufig1.gif" ALT="Figure 1"> View larger version (39K): org.highwire.dtl.DTLVardef@83bca4org.highwire.dtl.DTLVardef@d5ebaborg.highwire.dtl.DTLVardef@632d1borg.highwire.dtl.DTLVardef@1267a13_HPS_FORMAT_FIGEXP M_FIG C_FIG

cell biology↗

PERK inhibition rewires translational and CMGC protein kinase networks into an antiviral state

Protein kinases (PKs) are central regulators of cellular signaling, yet only a small fraction of the human kinome is targeted therapeutically, and kinase-substrate relationships remain incompletely defined. Here, we systematically characterize kinome regulation during human coronavirus 229E (HCoV-229E) infection across transcriptomic, translational, proteomic, and phospho-proteomic layers. We reveal that pharmacological inhibition of the ER stress sensor kinase PERK reprograms host protein biosynthesis and phospho-proteomic landscapes, simultaneously blocking viral nucleocapsid phosphorylation and modulating multiple host kinases. This rewiring antagonizes virus-induced translational shutdown, along with pronounced regulation of the CMGC kinase family, a pattern conserved in SARS-CoV and SARS-CoV-2 infected cells. Comparative analyses with PERK depletion distinguish on-target from off-target effects of PERK inhibition. Our findings uncover the kinome-scale consequences of PERK perturbation in coronavirus infection and demonstrate how the polypharmacology of PERK inhibitors can be harnessed to establish a potent antiviral state, revealing new avenues for host-directed antiviral strategies.

systems biology↗

Cross-kingdom degradomics identifies natural plant small RNAs with disease protecting activity

RNA interference (RNAi) is a highly specific process regulating genes transcriptionally or post-transcriptionally via silencing. small regulatory RNAs (sRNAs) provide the specificity of post-transcriptional silencing by binding to complementary mRNAs leading to their degradation or translational repression. sRNAs are promising non-chemical control agents against plant pests and diseases. Their application requires, however, a deep understanding of the determinants of functional specificity and efficiency. In nature, interacting plants and pathogens follow the manipulative strategy of cross-kingdom RNAi (ckRNAi) based on the targeted transfer of sRNAs. In this study, we employed a genome-wide approach to explore the diversity of natural ck-sRNAs exchanged in the pathogenic interaction of Brachypodium distachyon with the fungal pathogen Fusarium graminearum. By deep-sequencing of the cross-kingdom sRNAome, transcriptome and degradome 258 ckRNAi-mediating sRNAs were discovered. In a simulation-based approach, specific sequence characteristics allowed categorizing sRNAs into functionality classes. Subsequent genome annotation analyses revealed the organization of plant ck-sRNAs in long non-coding RNAs. Moreover, comparative sequence analyses revealed an evolution of ck-sRNAs towards invariant mRNA target regions. Functional analyses with sRNA candidates confirmed an antipathogenic activity at exceptionally low application doses. It indicates natural sRNA as untapped resource and potential blueprint for the development of highly specific and effective plant-derived bioprotectants.

plant biology↗

Fast, Bright and Reversible Rhodamine Tags for Live-Cell Imaging

We present Rho-tag and SiR-tag, engineered protein tags derived from bacterial multidrug-resistance proteins that bind unsubstituted (silicon-) rhodamines with nanomolar affinity, enabling fast, reversible, and fluorogenic protein labeling. In live cells, Rho-tag labeling occurs within seconds -- faster than HaloTag7 -- and the tags are compatible with super-resolution methods like STED, SMLM, and MINFLUX. The high specificity of Rho-tag and SiR-tag for unsubstituted rhodamines allows their use alongside HaloTag7 and SNAP-tag. In vivo applications are demonstrated by efficient neuronal labeling in zebrafish larvae.

bioengineering↗

A high-affinity split-HaloTag for live-cell protein labeling

We introduce a high-affinity split-HaloTag comprised of a short peptide tag (Hpep, 14 residues) and a large, inactive fragment (cpHalo{Delta}3). Hpep binds to cpHalo{Delta}3 spontaneously with nanomolar affinity, enabling subsequent labeling with fluorescent HaloTag ligands. The small size of Hpep facilitates cloning-free endogenous protein tagging using CRISPR/Cas9 and the complementation of Hpep-tagged proteins can be achieved in live cells through co-expression with cpHalo{Delta}3 and in fixed cells through incubation with cpHalo{Delta}3. The approach is compatible with advanced microscopy techniques such as expansion microscopy and live-cell STED imaging. Additionally, variants of Hpep that modulate the spectral properties of labeled fluorophores enable simultaneous imaging of two different Hpep-tagged proteins via fluorescence lifetime microscopy. In summary, our high-affinity split-HaloTag is a robust and versatile tool for live-cell imaging and diverse applications in chemical biology.

biochemistry↗

Synergistic targeting of cancer cells through simultaneous inhibition of key metabolic enzymes

As cancer cell specific rewiring of metabolic networks creates potential therapeutic opportunities, we conducted a synthetic lethal screen utilizing inhibitors of metabolic pathways. Simultaneous administration of (R)-GNE-140 and BMS-986205 (Linrodostat) preferentially halted proliferation of ovarian cancer cells, but not of their non-oncogenically transformed progenitor cells. While (R)-GNE-140 inhibits lactate dehydrogenase (LDH)A/B and thus effective glycolysis, BMS-986205, in addition to its known inhibitory activity on Indoleamine 2,3-dioxygenase (IDO1), also restricts oxidative phosphorylation (OXPHOS), as revealed here. BMS-986205, which is being tested in multiple Phase III clinical trials, inhibits the ubiquinone reduction site of respiratory complex I and thus compromises mitochondrial ATP production. The energetic catastrophe caused by simultaneous interference with glycolysis and OXPHOS resulted in either cell death or the induction of senescence in tumor cells, with the latter being eliminated by senolytics. The frequent synergy observed with combined inhibitor treatment was comprehensively confirmed through testing on tumor cell lines from the DepMap panel and on human colorectal cancer organoids. These experiments revealed highly synergistic activity of the compounds in a third of the tested tumor cell lines, correlating with alterations in genes with known roles in metabolic regulation and demonstrating the therapeutic potential of metabolic intervention.

cancer biology↗

STAT3 expression is reduced in cardiac pericytes in HFpEF and its loss reduces cellular adhesion and induces pericyte senescence

Heart failure with preserved ejection fraction (HFpEF) accounts for half of heart failure cases and is characterised by reduced pericyte coverage. While the contributions of other cardiac cell types to HFpEF are well-studied, the role of pericytes remains less understood. Using murine single-nucleus RNA sequencing to study cardiac pericytes in HFpEF, we identified reduced STAT3 expression as a hallmark of HFpEF pericytes. Mechanistic studies in vitro revealed that STAT3 deletion induces cellular senescence and impairs pericyte adhesion, recapitulating HFpEF-like characteristics. These findings suggest that STAT3 is crucial for maintaining pericyte homeostasis and highlight its reduction as a potential driver of pericyte loss, a defining feature of HFpEF.

cell biology↗

Exploring the Antifibrotic Potential of the heparan sulfate mimetic OTR4120: Insights from Preclinical Models

RationaleIdiopathic pulmonary fibrosis (IPF) is a debilitating lung disease characterized by excessive deposition of extracellular matrix (ECM), resulting in lung function impairment. Heparan sulfate mimetics (HSm) have been suggested to have potential antifibrotic effects by regulating ECM. This study aims to investigate the impact of a specific HSm named OTR4120 on fibrotic processes in ex vivo, in vitro and in vivo models. MethodsHuman Precision Cut Lung Slices (hPCLS) treated with a fibrotic cocktail alone or with OTR4120 were evaluated using second-harmonic imaging microscopy (SHIM) to assess collagen deposition. Human embryonic fibroblast WI-38 cell line and primary fibroblasts obtained from human donors were differentiated into myofibroblasts (MYF) using TGF-{beta}1 and treated with OTR4120 or a control vehicle. Gene expression analysis for MYF markers was performed using quantitative PCR (qPCR). Protein expression of MYF markers was evaluated using immunofluorescence techniques. Bulk-RNA sequencing analysis on WI-38 cells cultured under different experimental conditions was conducted. Finally, the therapeutic effects of OTR4120 on a bleomycin-induced fibrosis mouse model were investigated. ResultsSHIM analysis on OTR4120-treated hPCLS showed a decrease in collagen deposition. OTR4120 treatment of primary fibroblasts and WI-38 cells exposed to TGF-{beta}1 significantly reduced the expression of MYF markers. Bulk-RNA sequencing analysis on OTR4120-treated WI-38 cells showed significant impacts on fibrosis-related processes. Therapeutic application of OTR4120 in vivo to bleomycin-induced fibrosis mice resulted in enhanced fibrosis resolution. ConclusionOTR4120 has potential therapeutic benefits as an antifibrotic agent in the context of lung fibrosis. Further investigations are necessary to understand the precise mechanism through which OTR4120 exerts its antifibrotic effects.

cell biology↗

Improving Split-HaloTag through Computational Protein Engineering

Split-HaloTag can be used to transform transient molecular interactions into permanent marks through chemical labeling, thereby enabling the recording of transient physiological events in individual cells. However, applications of split-HaloTag-based recorders can be limited by slow labeling rates. To address this issue, we have engineered an improved version of cpHalo{Delta}, the larger fragment of the split-HaloTag system. Using computational techniques, we identified stabilizing point mutations and designed a structured linker connecting the original N and C termini of the circular permutated protein, thereby significantly improving thermostability and activity of cpHalo{Delta}. These modifications decrease the time and substrate concentrations required for split-HaloTag-based assays and can expand their dynamic range and sensitivity.

biochemistry↗

SNAP-tag2: faster and brighter protein labeling

SNAP-tag is a powerful tool for labeling proteins with synthetic fluorophores in bioimaging. However, its utility in live-cell applications can be constrained by its relatively slow labeling kinetics and the limited cell permeability of its substrates. Here we introduce new labeling substrates and an engineered SNAP-tag for faster labeling in vitro and in live cells. SNAP-tag2 presents a second-order rate constant with rhodamine substrates that approaches 107 s-1 M-1, a 100-fold improvement over the corresponding SNAP-tag-substrate pairs. When labeled with highly fluorogenic dyes, SNAP-tag2 also shows a 5-fold increase in fluorescence brightness relative to currently used SNAP-tag. The increased labeling kinetics and brightness of SNAP-tag2 translates into a greatly improved performance in various live-cell (super-resolution) imaging applications.

biochemistry↗

Adventitial fibroblasts direct smooth muscle cell-state transition in pulmonary vascular disease

Pulmonary vascular remodeling is a progressive pathological process characterized by functional alterations within pulmonary artery smooth muscle cells (PASMC) and adventitial fibroblasts (PAAF). Mechanisms driving the transition to a diseased phenotype remain elusive. Utilizing a combination of transcriptomic and proteomic profiling, along with phenotyping of source-matched cells from healthy controls and individuals with idiopathic pulmonary arterial hypertension (IPAH), our investigation uncovered that while PASMC and PAAF retained their original cellular identities, they acquired distinct disease-associated states. Though both cell types exhibited reduced mitochondrial content and hyperpolarization, IPAH-PASMC displayed heightened glycosaminoglycan production and downregulation of contractile machinery, contrasting a hyperproliferative phenotype of IPAH-PAAF. We investigated the involvement of cellular crosstalk in regulating cell state dynamics and identified pentraxin-3 and hepatocyte growth factor as potential modulators of PASMC phenotypic transition orchestrated by PAAF. Our findings contribute to a deeper understanding of pulmonary vascular mesenchyme dynamics in disease pathogenesis.

cell biology↗

The proximity-based protein interaction landscape of the transcription factor p65 NF-kappaB/RELA and its gene-regulatory logics

The protein interactome of p65 / RELA, the most active subunit of the transcription factor (TF) NF-{kappa}B, has not been previously determined in living cells. Using p65-miniTurbo fusion proteins, we identified by biotin tagging > 350 RELA interactors from untreated and IL-1-stimulated cells, including many TFs (47 % of all interactors) and > 50 epigenetic regulators belonging to different classes of chromatin remodeling complexes. According to point mutants of p65, the interactions primarily require intact dimerization rather than DNA binding properties. A targeted RNAi screen for 38 interactors and subsequent functional transcriptome and bioinformatics studies identified gene regulatory (sub)networks, each controlled by RELA in combination with one of the TFs ZBTB5, GLIS2, TFE3 / TFEB or S100A8 / A9. The remarkably large, dynamic and versatile high resolution interactome of RELA and its gene-regulatory logics provides a rich resource and a new framework for explaining how RELA cooperativity determines gene expression patterns. HighlightsO_LIIdentification of > 350 largely dimerization-dependent interactors of p65 / RELA by miniTurboID C_LIO_LIThe interactome is dominated by transcription factors and epigenetic regulator complexes C_LIO_LIFunctional validation of 38 high confidence interactors by targeted siRNA screen C_LIO_LIIdentification of genetic networks regulated by RELA and six of its interactors in the IL-1 response C_LI

molecular biology↗

NAD+ metabolism is a key modulator of bacterial respiratory epithelial infections

1.Lower respiratory tract infections caused by StreptococcusOpneumoniae (Spn) are a leading cause of death globally. Here we investigate the bronchial epithelial response to Spn infection on a transcriptomic, proteomic and metabolic level. We found the NAD+ salvage pathway to be dysregulated upon infection in a cell line model, primary human lung tissue and in vivo in rodents, leading to a reduced production of NAD+. Knockdown of NAD+ salvage enzymes (NAMPT, NMNAT1) increased bacterial replication. NAD+ treatment of Spn inhibited its growth while growth of other respiratory pathogens improved. Boosting NAD+ production increased NAD+ levels in immortalized and primary cells and decreased bacterial replication upon infection. NAD+ treatment of Spn dysregulated the bacterial metabolism and reduced intrabacterial ATP. Enhancing the bacterial ATP metabolism abolished the antibacterial effect of NAD+. Thus, we identified the NAD+ salvage pathway as an antibacterial cascade in Spn infections, predicting a novel antibacterial mechanism of NAD+.

immunology↗

Neutrophil efferocytosis reprograms mitochondrial metabolism to switch alveolar macrophages to a pro-resolution phenotype at the cost of bacterial control

Resolution of lung injuries is vital to maintain gas exchange. Concurrently, there is an increased risk of secondary bacterial infections. Alveolar macrophages (AMs) are crucial to clear bacteria and control initiation and resolution of inflammation, but environmental cues that switch functional phenotypes of AMs remain elusive. Here, we discovered an incapacity of AMs to mount an effective immune response to bacteria during resolution of inflammation. AM efferocytosis of neutrophils (PMNs), a hallmark of resolution of inflammation, switched mitochondrial metabolism to shift AM functions. Mechanistically, PMN-derived myeloperoxidase (MPO) fueled canonical glutaminolysis via uncoupling protein 2 (UCP2) resulting in decreased mtROS-dependent killing of bacteria and secretion of pro-inflammatory cytokines. Instead, MPO-enhanced UCP2 expression inhibited mitochondrial hyperpolarization and boosted efferocytosis irrespective of the presence of bacterial pathogens. In contrast, efferocytosis of epithelial cells resulted in a distinct anti-inflammatory phenotype of AMs maintaining phenotypic plasticity towards bacteria. Overall, uptake of apoptotic PMNs switches AMs to prioritize resolution of inflammation over antibacterial responses and similarly affects murine macrophages at extra-pulmonary sites, and human AMs. One sentence summaryNeutrophil efferocytosis reprograms mitochondrial metabolism to switch alveolar macrophages to a pro-resolution phenotype at the cost of bacterial control.

immunology↗

Exchangeable HaloTag Ligands (xHTLs) for multi-modal super-resolution fluorescence microscopy

We introduce exchangeable ligands for fluorescence labeling of HaloTag7 as an alternative to covalently bound probes. The exchangeable ligands open up new possibilities in imaging for a widely used labeling approach, including applications in points accumulation for imaging in nanoscale topography (PAINT), MINFLUX and live-cell, multi-frame stimulated emission depletion (STED) microscopy. We furthermore introduce orthogonal pairs of exchangeable ligands and HaloTags for dual-color PAINT and STED microscopy. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=142 SRC="FIGDIR/small/496706v1_ufig1.gif" ALT="Figure 1"> View larger version (63K): org.highwire.dtl.DTLVardef@1e7d689org.highwire.dtl.DTLVardef@1b5db18org.highwire.dtl.DTLVardef@433efaorg.highwire.dtl.DTLVardef@dbbd61_HPS_FORMAT_FIGEXP M_FIG C_FIG

biochemistry↗