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Johnsson, K.

Publications and source records attributed to Johnsson, K..

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↗

Collective cancer cell calcium activity drives brain metastasis

Communication in multicellular networks is a cancer-intrinsic neural feature and crucial for primary brain tumor growth and resistance, but it is unclear whether brain metastases (BrM), the most common and deadliest brain malignancy, are also driven by communicating cancer networks. Using intravital two-photon microscopy in awake mice, clinical specimens, and Ca2+ integrators, we demonstrate that brain-colonizing breast and lung cancer and melanoma cells display gap-junction-dependent, coordinated Ca2+ activity in multicellular, cancer-cell intrinsic networks, which drives their proliferation. Mechanistically, Ca2+ oscillations induce transcription of immediate early genes, adoption of a neuronal expression profile, and cell cycle progression. While many of those features are enriched in BrM, all investigated cancer cell lines showed collective Ca2+ activity. Therapeutically, blocking Ca2+ activity with gap junction inhibitors reduces BrM burden in mouse models. Here we show communicating cancer cell syncytia as drivers of BrM growth, pointing to a targetable pathomechanism, and potentially a new pan-cancer hallmark. Graphical AbstractIn brief Brain metastases form gap-junction-coupled networks exhibiting spontaneous, coordinated Ca2+ activity linked to immediate early gene activation, neuronal gene programs, and cell cycle progression. Disrupting Ca2+ network communication with gap junction inhibitors induces cell cycle arrest and reduces brain metastatic burden in vivo. O_FIG O_LINKSMALLFIG WIDTH=195 HEIGHT=200 SRC="FIGDIR/small/723715v1_ufig1.gif" ALT="Figure 1"> View larger version (88K): org.highwire.dtl.DTLVardef@1130ea0org.highwire.dtl.DTLVardef@254dcdorg.highwire.dtl.DTLVardef@117021forg.highwire.dtl.DTLVardef@18c4f1e_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIBrain metastases display collective Ca2+ activity in gap-junction-coupled networks C_LIO_LICa2+ co-activity is conserved across cancers but enriched in brain metastasis C_LIO_LICa2+ oscillations robustly induce neuronal gene programs and cell cycle progression C_LIO_LIGap junction inhibition reduces brain metastasis burden in mice C_LI

cancer 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↗

Localizable fluorescent metal ion indicators with tunable colors

Elucidating the role of metal ion homeostasis in physiological and pathological processes requires detection tools with high sensitivity and selectivity, spectral versatility, and precise subcellular localization. Here, we introduce a modular strategy for generating fluorescent metal ion indicators which are comprised of a sulfonamide-functionalized chelator, a rhodamine derivative and a ligand for bioconjugation to self-labeling proteins. With a concise three-step synthesis, the design allows tuning of both the emission color and ligand specificity of the resulting indicators. Specifically, we developed a family of bright, color-tunable potassium indicators which can be selectively coupled to intra- or extracellular HaloTag and SNAP-tag fusion proteins. The increase in fluorescence upon binding to HaloTag or SNAP-tag fluorogenicity enabled wash-free live-cell imaging. The localized potassium indicators enabled the detection of dynamic potassium efflux in rat hippocampal neurons upon glutamate stimulation. Our work thus establishes a versatile platform for the generation of localizable fluorescent metal ion indicators and opens up new avenues for live-cell potassium sensing.

cell 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↗

A silicon rhodamine-fused glibenclamide to label and detect malaria-infected red blood cells

The malaria parasite Plasmodium falciparum affects the lives of millions of people worldwide every year. The detection of replicating parasites within human red blood cells is of paramount importance, requiring appropriate diagnostic tools. Herein, we design and apply a silicon rhodamine-fused glibenclamide (SiR-glib). We first test this far-red fluorescent, fluorogenic and endoplasmic reticulum-targeting sulfonylurea in mammalian cells and pancreatic tissues, before characterizing its labeling performance in red blood cells infected with the asexual developmental stages of Plasmodium falciparum. We further combine SiR-glib with a portable smartphone-based microscope to easily and rapidly identify parasitized red blood cells, providing proof of principle for diagnostic use in rural endemic areas without major healthcare facilities.

biochemistry↗

SiR-XActin: A fluorescent probe for imaging actin dynamics in live cells

Imaging actin-dependent processes in live cells is important for understanding numerous biological processes. However, currently used natural-product based fluorescent probes for actin filaments affect the dynamics of actin polymerization and can induce undesired cellular phenotypes. Here, we introduce SiR-XActin, a simplified jasplakinolide-based, far-red fluorescent probe that enables bright and photostable staining in various cell types without requiring genetic modifications. Due to its relatively weak binding affinity, the probe exhibits minimal cytotoxicity and labels actin filaments without significantly altering actin dynamics. Furthermore, SiR-XActin is suitable for time-resolved, live-cell super-resolution STED microscopy. Exchanging the SiR fluorophore in SiR-XActin for other fluorophores yields probes in different colors. All these properties make SiR-XActin and its analogs powerful tools for studying actin dynamics using live-cell fluorescence microscopy.

biochemistry↗

In vivo multiplex imaging of dynamic neurochemical networks with designed far-red dopamine sensors

Neurochemical signals like dopamine (DA) play a crucial role in a variety of brain functions through intricate interactions with other neuromodulators and intracellular signaling pathways. However, studying these complex networks has been hindered by the challenge of detecting multiple neurochemicals in vivo simultaneously. To overcome this limitation, we developed a single-protein chemigenetic DA sensor, HaloDA1.0, which combines a cpHaloTag-chemical dye approach with the G protein-coupled receptor activation-based (GRAB) strategy, providing high sensitivity for DA, sub-second response kinetics, and an extensive spectral range from far-red to near-infrared. When used together with existing green and red fluorescent neuromodulator sensors, Ca2+ indicators, cAMP sensors, and optogenetic tools, HaloDA1.0 provides high versatility for multiplex imaging in cultured neurons, brain slices, and behaving animals, facilitating in-depth studies of dynamic neurochemical networks.

neuroscience↗

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↗

Molecular recording of cellular protein kinase activity with chemical labeling

Protein kinases control most cellular processes and aberrant kinase activity is involved in numerous diseases. To investigate the link between specific kinase activities and cellular phenotypes in heterogeneous cell populations and in vivo, we introduce molecular recorders of kinase activities for later analysis. Based on split-HaloTag and a phosphorylation-dependent molecular switch, our recorders become rapidly labeled in the presence of a specific kinase activity and a fluorescent HaloTag substrate. The kinase activity in a given cell controls the degree of fluorescent labeling whereas the recording window is set by the presence of the fluorescent substrate. We have designed specific recorders for four protein kinases, including protein kinase A. We apply our protein kinase A recorder for the sorting of heterogeneous cell populations and subsequent transcriptome analysis, in genome-wide CRISPR screens to discover regulators of PKA activity and for the tracking of neuromodulation in freely moving mice.

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↗

Long-term single-molecule tracking in living cells using weak-affinity protein labeling

Single-particle tracking (SPT) has become a powerful tool to monitor the dynamics of membrane proteins in living cells. However, permanent labeling strategies for SPT suffer from photobleaching as a major limitation, restricting observation times, and obstructing the study of long-term cellular processes within single living cells. Here, we use exchangeable HaloTag Ligands (xHTLs) as an easy-to-apply labeling approach for live-cell SPT and demonstrate extended observation times of individual live cells of up to 30 minutes. Using the xHTL/HT7 labeling system, we measure the ligand-induced activation kinetics of the epidermal growth factor receptor (EGFR) in single living cells. Furthermore, we generate spatial maps of receptor diffusion in cells, report non-uniform distributions of receptor activation, and the formation of spatially confined hot spots of EGFR activation. This approach represents a general strategy to monitor protein dynamics in a functional context and for extended observation times in single living cells.

biophysics↗

Impaired Suppression of Plasma Lipid Extraction and its Partitioning Away from Muscle by Insulin in Humans with Obesity

ContextHumans with obesity and insulin resistance exhibit lipid accumulation in skeletal muscle, but the underlying biological mechanisms responsible for the accumulation of lipid in the muscle of these individuals remain unknown. ObjectiveWe investigated how plasma insulin modulates the extraction of circulating triglycerides (TGs) and non-esterified fatty acids (NEFAs) from ingested and endogenous origin in the muscle of lean, insulin-sensitive humans (Lean-IS) and contrasted these responses to those in humans with obesity and insulin resistance (Obese-IR). MethodsThe studies were performed in a postprandial state associated with steady-state plasma TG concentrations. The arterio-venous blood sampling technique was employed to determine the extraction of circulating lipids across the forearm muscle before and after insulin infusion. We distinguished kinetics of TGs and NEFAs from ingested origin from those from endogenous origin across muscle by incorporating stable isotope-labeled triolein in the ingested fat. ResultsInsulin infusion rapidly suppressed the extraction of plasma TGs from endogenous, but not ingested, origin in the muscle of the Lean-IS, but this response was absent in the muscle of the Obese-IR. Furthermore, in the muscle of the Lean-IS, insulin infusion decreased the extraction of circulating NEFAs from both ingested and endogenous origin; however, this response was absent for NEFAs from ingested origin in the muscle of the Obese-IR subjects. ConclusionsPartitioning of circulating lipids away from the skeletal muscle when plasma insulin increases during the postprandial period is impaired in humans with obesity and insulin resistance.

physiology↗

Gentle rhodamines for live-cell fluorescence microscopy

Rhodamines have been continuously optimized in brightness, biocompatibility, and colors to fulfill the demands of modern bioimaging. However, the problem of phototoxicity caused by the excited fluorophore under long-term illumination has been largely neglected, hampering their use in time-lapse imaging. Here we introduce cyclooctatetraene (COT) conjugated rhodamines that span the visible spectrum and exhibit significantly reduced phototoxicity. We identified a general strategy for the generation of Gentle Rhodamines, which preserved their outstanding spectroscopic properties and cell permeability while showing an efficient reduction of singlet-oxygen formation and diminished cellular photodamage. Paradoxically, their photobleaching kinetics do not go hand in hand with reduced phototoxicity. By combining COT-conjugated spirocyclization motifs with targeting moieties, these gentle rhodamines compose a toolkit for time-lapse imaging of mitochondria, DNA, and actin and synergize with covalent and exchangeable HaloTag labeling of cellular proteins with less photodamage than their commonly used precursors. Taken together, the Gentle Rhodamines generally offer alleviated phototoxicity and allow advanced video recording applications, including voltage imaging.

cell biology↗

Engineering of a biosensor for intracellular aspartate

Aspartate is a limiting metabolite in proliferating cells with its production closely linked to glutamine and mitochondrial metabolism. To date, measuring aspartate concentrations in live cells was deemed impossible. We present iAspSnFR, a genetically-encoded biosensor for intracellular aspartate, engineered by displaying and screening biosensor libraries in HEK293 cells. In live cells, iAspSnFR exhibits a dynamic range of 130% fluorescence change and detects reduced aspartate levels upon glutamine deprivation or glutaminase inhibition. Furthermore, iAspSnFR tracks aspartate uptake by excitatory amino acid transporters, or of asparagine after co-expression of an asparaginase. Importantly, iAspSnFR reports aspartate depletions upon electron transport chain inhibition, and therefore it can serve as a proxy for mitochondrial respiration. Consequently, iAspSnFR can dissect the major cellular pathways of aspartate production, offering immediate applications, particularly in cancer biology, such as screening small molecules targeting aspartate and glutamine metabolism.

cell biology↗

A general method for the development of multicolor biosensors with large dynamic ranges

Fluorescent biosensors enable to study cell physiology with spatiotemporal resolution, yet most biosensors suffer from relatively low dynamic ranges. Here, we introduce a family of designed Forster Resonance Energy Transfer (FRET) pairs with near quantitative FRET efficiencies based on the reversible interaction of fluorescent proteins with a fluorescently labeled HaloTag. These FRET pairs enabled the straightforward design of biosensors for calcium, ATP and NAD+ with unprecedented dynamic ranges. The color of each of these biosensors can be readily tuned by either changing the fluorescent protein or the synthetic fluorophore, which enabled to monitor simultaneously free NAD+ in different subcellular compartments upon genotoxic stress. Minimal modifications furthermore allow the readout of these biosensors to be switched to fluorescence intensity, lifetime or bioluminescence. These FRET pairs thus establish a new concept for the development of highly sensitive and tunable biosensors. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/518186v1_ufig1.gif" ALT="Figure 1"> View larger version (44K): org.highwire.dtl.DTLVardef@9ae8b9org.highwire.dtl.DTLVardef@250477org.highwire.dtl.DTLVardef@482d03org.highwire.dtl.DTLVardef@833397_HPS_FORMAT_FIGEXP M_FIG C_FIG

biochemistry↗

Synergizing exchangeable fluorophore labels for multi-target STED microscopy

Investigating the interplay of cellular proteins with optical microscopy requires multi-target labeling. Spectral multiplexing using high-affinity or covalent labels is limited in the number of fluorophores that can be discriminated in a single imaging experiment. Advanced microscopy methods such as STED microscopy additionally demand balanced excitation, depletion and emission wavelengths for all fluorophores, further reducing multiplexing capabilities. Non-covalent, weak-affinity labels bypass this "spectral barrier" through label exchange and sequential imaging of different targets. Here, we combine exchangeable HaloTag ligands, weak-affinity DNA hybridization and hydrophophic and protein-peptide interactions to increase labeling flexibility and demonstrate 6-target STED microscopy in single cells. We further show that exchangeable labels reduce photobleaching, facilitate long acquisition times and multi-color live-cell and high-fidelity 3D STED microscopy. The synergy of different types of exchangeable labels increase the multiplexing capabilities in fluorescence microscopy, and by that, the information content of microscopy images.

biophysics↗