Search bioRxiv⌕ Search

Biology subjects

Heine, M.

Publications and source records attributed to Heine, M..

16 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↗

Functional relevance of mobile and clustered CaV2.1 channels in central synapses

Reliable neurotransmitter release critically depends on the spatial relationship between voltage- gated calcium channels (VGCCs) and presynaptic release sites. Single particle tracking of endogenous CaV2.1 channels at glutamatergic synapses of hippocampal neurons revealed that apart from CaV2.1 channels aggregated in stable nanodomain clusters, a substantial fraction of Cav2.1 channels remained mobile, raising the question of whether these dispersed channels contribute to synaptic function. Mathematical modelling predicted that dispersed Cav2.1 channels cooperatively enhance release reliability. Upon repetitive stimulation, mobile CaV2.1 channels enable alternative use of release sites and thereby reduce the probability of failed presynaptic release. Both optogenetic immobilisation of CaV2.1 channels per se or activation of GABAB receptors (GABABRs) alone increase the failure rate and can lead to synaptic silencing. However, optogenetic clustering CaV2.1 channels prior to GABABR activation increases the fraction of synapses that remain active even in presence of GABABR agonist. The contribution of mobile channels to reliable neurotransmitter release is frequency-dependent and is minor at stimulation frequencies 1 Hz but becomes strong at frequencies over 10 Hz. These results demonstrate that mobile presynaptic CaV2.1 channels increase the frequency range of synaptic transmission but are particularly sensitive to metabotropic GABABR-mediated inhibition in glutamatergic hippocampal synapses.

neuroscience↗

Unreliable homeostatic action potential broadening in cultured dissociated neurons

Homeostatic plasticity preserves neuronal activity against perturbations. Recently, somatic action potential broadening was proposed as a key homeostatic adaptation to chronic inactivity in neocortical neurons. Since action potential shape critically controls calcium entry and neuronal function, broadening provides an attractive homeostatic feedback mechanism to regulate activity. Here, we report that chronic inactivity induced by sodium channel block does not broaden action potentials in neocortical neurons under a wide range of conditions. In contrast, action potentials were broadened in CA3 neurons of organotypic hippocampal cultures by chronic sodium channel block and in hippocampal dissociated cultures by chronic synaptic block. Mechanistically, BK-type potassium channels were proposed to underly inactivity-induced action potential broadening. However, BK channels did not affect action potential duration in our recordings. Our results indicate that action potential broadening can occur in specific neurons and conditions but is not a general mechanism of homeostatic plasticity in cultured neurons.

neuroscience↗

Shiny-Calorie: A context-aware application for indirect calorimetry data analysis and visualization using R

Indirect calorimetry is a cornerstone technique for metabolic phenotyping of animal models in preclinical research, with well-established experimental protocols and platforms. However, a flexible, extensible, and user-friendly software suite that enables standardized integration of data and metadata from diverse metabolic phenotyping platforms--followed by unified statistical analysis and visualization--remains absent. We present Shiny-Calorie, an open-source interactive web application for transparent data and metadata integration, comprehensive statistical data analysis, and visualization of indirect calorimetry datasets. Shiny-Calorie is compatible with data formats from widely used commercial metabolic phenotyping platforms, such as TSE and Sable Systems, and includes functionality for exporting processed data in these formats. Built using GNU R and a Shiny-based reactive interface, Shiny-Calorie enables intuitive exploration of complex, multi-modal longitudinal datasets comprising categorical, continuous, ordinal, and count variables. The platform incorporates state-of-the-art statistical methods for robust hypothesis testing, thereby facilitating biologically meaningful interpretation of energy metabolism phenotypes, including resting metabolic rate and energy expenditure. Overall, Shiny-Calorie streamlines routine analysis workflows and enhances reproducibility and transparency in metabolic phenotyping studies.

bioinformatics↗

Monoamine-induced diacylglycerol signaling rapidly accumulates Unc13 in nanoclusters for fast presynaptic potentiation

Neuromodulators control mood, arousal, and behavior by inducing synaptic plasticity via G-protein coupled receptors. Long-term potentiation of presynaptic neurotransmitter release requires structural changes, but how fast potentiation is achieved within minutes remains enigmatic. Using the Drosophila melanogaster neuromuscular junction, we show that on the timescale of one minute, octopamine, the invertebrate analog of nor-epinephrine, rapidly potentiates evoked neurotransmitter release by a G protein coupled pathway involving presynaptic OAMB receptors and phospholipase C. No changes of presynaptic calcium influx were seen, but confocal signals of the release factor Unc13A and the scaffolding protein Bruchpilot increased within one minute of octopamine treatment. On the same timescale, live, single-molecule imaging of endogenously tagged Unc13 revealed its instantly reduced motility and its increased concentration in synaptic nanoclusters with potentiation. Presynaptic knockdown of Unc13A fully blocked fast potentiation and removal of its N-terminal localization sequence delocalized the protein fragment to the cytosol, but it was rapidly recruited to the plasma membrane by DAG analog phorbol esters and octopamine, pointing to a role in C-terminal domains. Point mutation of endogenous Unc13 disrupting diacylglycerol-binding to its C1 domain blocked plasticity-induced nanoscopic enrichment and synaptic potentiation. The mutation increased basal neurotransmission but reduced Unc13 levels, revealing a gain of function and potential homeostatic compensation. The mutation also blocked phorbol ester-induced potentiation, decreased the calcium-sensitivity of neurotransmission and caused short-term synaptic depression. At the organismal level, the mutation reduced locomotion and survival while enhancing reproduction. Thus, the Unc13 C1 domain mediates acute subsynaptic compaction of Unc13 under monoamine-induced potentiation and influences short-term plasticity, locomotion, reproduction, and survival.

neuroscience↗

Activity-Dependent Localization and Heterogeneous Dynamics of STIM1 and STIM2 at ER-PM contacts in Hippocampal Neurons.

Stromal interaction molecules (STIMs) are calcium sensors integral to store-operated calcium entry (SOCE), a process critical for non-excitable cells and contributing to homeostatic functions in neurons. Upon depletion of Ca2+ from the endoplasmic reticulum (ER), STIMs translocate to ER-plasma membrane (PM) junctions to contact the inner leaflet of the plasma membrane. Using single-particle tracking (SPT), we characterized the dynamic properties of neuronal STIM1 and STIM2 in hippocampal neurons.Our data reveal that STIMs exhibit heterogenous dynamics in dendrites and axons, while only transiently visiting synaptic compartments. A substantial fraction of STIM2 proteins define ER-PM contacts under resting conditions, whereas STIM1 proteins are recruited to ER-PM junctions during strong activation of glutamatergic synapses. Junctions organized by KV2.1 channels are not particularly enriched with STIM proteins. Activity-dependent confinement of STIM proteins is not influenced by L-type calcium channel (CaV1.2) activity. We propose that STIM proteins predominantly regulate the contact area and frequency of contacts between ER and PM.

neuroscience↗

Premature upregulation of miR-92a's target RBFOX2 hijacks PTBP splicing and impairs cortical neuronal differentiation.

Alternative splicing is a crucial component of neuronal differentiation, yet the mechanisms that regulate splicing transitions during embryonic brain development remain incompletely understood. Here, we identify a post-transcriptional mechanism that times the expression of the splicing factor Rbfox2 during neurogenesis. RBFOX2 is normally expressed at low levels in neural progenitor cells (NPCs) and becomes upregulated in newborn neurons where it promotes neuronal differentiation. Unexpectedly, premature expression of Rbfox2 in NPCs of the embryonic mouse neocortex blocked their differentiation into neurons rather than promoting it. Genome-wide analysis revealed widespread alternative splicing changes enriched for NDD genes and associated with a hybrid NPC- and neuron-like splicing pattern that significantly deviates from the normal splicing developmental trajectory. Remarkably, premature Rbfox2 expression induced the inclusion of validated target exons that are otherwise repressed by PTBP2 pointing to an antagonistic splicing relationship. Integrative scRNA-seq analysis confirmed a negatively correlated expression between these two RNA-binding proteins (RBP) along differentiation pseudotime. Strikingly, we identified the NPC-specific miRNA 92a-3p as a regulator of the Rbfox2 expression switch: expression of miR-92a reduced RBFOX2 levels and reversed splicing patterns of target genes in vitro, while silencing miR-92a in vivo increased RBFOX2 expression in the embryonic cortex. Together, these findings reveal a previously unrecognized miRNA-RBP regulatory axis that ensures the proper timing of NPC-to-neuron splicing transitions in the developing cortex and provide new insights into splicing dysregulation as a contributing factor to the emergence of neurodevelopmental disorders. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=152 HEIGHT=200 SRC="FIGDIR/small/614071v3_ufig1.gif" ALT="Figure 1"> View larger version (28K): org.highwire.dtl.DTLVardef@16248caorg.highwire.dtl.DTLVardef@198dd0dorg.highwire.dtl.DTLVardef@d8887aorg.highwire.dtl.DTLVardef@1e8419e_HPS_FORMAT_FIGEXP M_FIG C_FIG Graphical Abstract Schematic representation of the proposed splicing regulation for the transition of undifferentiated NPCs to neurons in the developing cerebral cortex.

genomics↗

Specific presynaptic functions require distinct Drosophila Cav2 splice isoforms

The multiplicity of neural circuits that accommodate the sheer infinite number of computations conducted by brains requires diverse synapse and neuron types. At many vertebrate synapses release probability and other aspects of presynaptic function are tuned by different combinations of Cav2.1, Cav2.2, and Cav2.3 channels. By contrast, most invertebrate genomes contain only one Cav2 gene. The one Drosophila Cav2 homolog, cacophony (cac), localizes to presynaptic active zones (AZs) to induce synaptic vesicle release. We hypothesize that Drosophila cac functional diversity is enhanced by two specific exon pairs that are mutually exclusively spliced and not conserved in vertebrates, one in the voltage sensor and one in the intracellular loop containing the binding site(s) for Ca{beta} and G-protein {beta}{gamma} subunits. We test our hypothesis by combining opto- and electrophysiological with neuroanatomical approaches at a fast glutamatergic model synapse, the Drosophila larval neuromuscular junction. We find that alternative splicing in the voltage sensor affects channel activation voltage and is imperative for normal synapse function. Only the isoform with the higher activation voltage localizes to the presynaptic AZ and mediates evoked release. Removal of these cac splice isoforms renders fast glutamatergic synapses non-functional. By contrast, alternative splicing at the other alternative exon that encodes the intracellular loop between the first and the second homologous repeats does not affect cac presynaptic AZ localization, but it tunes multiple aspects of presynaptic function. While expression of one exon yields normal transmission, expression of the other exon reduces channel number in the AZ and thus release probability. This also abolishes presynaptic homeostatic plasticity. Moreover, reduced channel number upon selective exon excision increases paired pulse ratios and the variability of synaptic depression during low frequency stimulation trains (1 and 10 Hz), and thus affects short term plasticity. Effects on short term plasticity can be rescued by increasing the external calcium concentration to match release probability to control. In sum, in Drosophila alternative splicing provides a mechanism to regulate different aspects of presynaptic functions with only one Cav2 gene.

neuroscience↗

Neuroimage Denoiser for removing noise from transient fluorescent signals in functional imaging.

We developed Neuroimage Denoiser, a novel U-Net-based model that effectively removes noise from microscopic recordings of transient local fluorescent signals. The model makes the denoising process independent of the recording frequency and the kinetics of the sensor used. The framework is easy to use for denoising and training and has minimal hardware requirements, thus, making it accessible for an average laboratory to create a custom version specific to their experimental setup. Neuroimage Denoiser significantly enhances the quality of functional microscopy recordings by effectively removing noise, thereby facilitating a more accurate and reliable analysis of neural activity. Highlights- Neuroimage Denoiser is a deep learning framework to remove noise from functional microscopic recordings, particularly trained and tested for glutamate imaging - Neuroimage Denoiser balances the removal of noise while preserving the amplitude of responses - Neuroimage Denoiser operates without re-training for different sensors (when the localization is similar) and recording frequencies MotivationAccurate measurements of neuronal activity through functional imaging are critical in understanding mechanisms of synaptic plasticity and learning concerning changes in the molecular composition of single synapses. Traditional denoising methods, such as Gaussian or Median filters, indiscriminately smooth entire recordings, reducing temporal and spatial resolutions considerably. Existing frameworks are not suited to remove noise from glutamate recordings due to the fast dynamics of the sensor. Therefore, a specialized tool for the challenges imposed by glutamate recordings, i.e. faster dynamics, and synaptic localization, is needed.

bioinformatics↗

Cortexa - a comprehensive resource for studying gene expression and alternative splicing in the murine brain.

MotivationGene expression and alternative splicing are strictly regulated processes that shape brain development and determine the cellular identity of differentiated neural cell populations. Despite the availability of multiple valuable datasets, many functional implications, especially those related to alternative splicing, remain poorly understood. Moreover, neuroscientists working primarily experimentally often lack the bioinformatics expertise required to process alternative splicing data and produce meaningful and interpretable results. Notably, re-analyzing publicly available datasets and integrating them with in-house data can provide substantial novel insights. However, such analyses necessitate devel-oping harmonized data handling and processing pipelines which in turn requires considerable computational resources and in-depth bioinformatics expertise. ResultsHere, we present Cortexa - a comprehensive web-portal that incorporates RNA-sequencing datasets from the mouse cerebral cortex (longitudinal or cell-specific) and the hippocampus. Cortexa facilitates understandable visualization of the expression and alternative splicing patterns of individual genes. Our platform also provides SplicePCA - a tool that allows users to integrate their alternative splicing dataset and compare it to cell-specific or developmental neocortical splicing patterns. All gene expression and alternative splicing data have been processed in a standardized manner and they can also be downloaded for further in-depth down-stream analysis. AvailabilityThe data portal is available at https://cortexa-rna.com/ Contacthristo.todorov@uni-mainz.de.

genomics↗

Identification and characterization of a synaptic active zone assembly protein

At presynaptic active zones (AZs), scaffold proteins play a crucial role in coordinating synaptic vesicle (SV) release and forming intricate nanoarchitectures essential for synaptic function. Despite their suspected importance, factors governing the assembly of nanoscale AZ scaffolds have remained elusive. Here, we identify "Blobby" as a novel regulator of AZ nanopatterning, localized within the AZ scaffold. Genetic loss of the extended Blobby protein led to aberrant accumulation of AZ scaffold proteins ("blobs") and disrupted the nanoscale architecture of the AZ scaffold, resulting in a significant reduction in the packing density of voltage-gated Ca2+ channels at AZs, as observed through intravital single-molecule imaging. This disruption correlated with decreased evoked synaptic currents and SV release probability. Our findings suggest that Blobby plays a crucial role in switching the AZ scaffold into a state which allows to fine-tune the dynamic nanopatterning of Ca2+ channels to maintain proper release.

neuroscience↗

Homeostatic feedback between lysosomal mTORC1 and mTORC2-AKT signaling controls nutrient uptake in brown adipose tissue

In brown adipose tissue (iBAT), the balance of lipid/glucose uptake and lipolysis is regulated by insulin signaling. Downstream of the insulin receptor, PDK1 and mTORC2 phosphorylate AKT, which activates glucose uptake and lysosomal mTORC1 signaling. The latter requires the late endosomal/lysosomal adaptor and MAPK and mTOR activator (LAMTOR/Ragulator). Deletion of LAMTOR2 (and thereby loss of the LAMTOR complex) in mouse adipocytes resulted in insulin-independent AKT hyperphosphorylation in iBAT, causing increased glucose and fatty acid uptake as evidenced by massively enlarged lipid droplets. As LAMTOR2 was essential for the upregulation of de novo lipogenesis, LAMTOR2 deficiency triggered exogenous glucose storage as glycogen in iBAT. These effects are cell autonomous, since AKT hyperphosphorylation was reversed by PI3K inhibition or by deletion of the mTORC2 component Rictor in LAMTOR2-deficient mouse embryonic fibroblasts. We identified a homeostatic circuit connecting LAMTOR-mTORC1 signaling with PI3K-mTORC2-AKT signaling downstream of the insulin receptor to maintain iBAT metabolism.

cell biology↗

Inhibiting presynaptic calcium channel mobility in the auditory cortex suppresses synchronized input processing

The emergent coherent population activity from thousands of stochastic neurons in the brain is believed to constitute a key neuronal mechanism for salient processing of external stimuli and its link to internal states like attention and perception. In the sensory cortex, functional cell assemblies are formed by recurrent excitation and inhibitory influences. The stochastic dynamics of each cell involved is largely orchestrated by presynaptic CAV2.1 voltage-gated calcium channels (VGCCs). Cav2.1 VGCCs initiate the release of neurotransmitters from the presynaptic compartment and are therefore able to add variability into synaptic transmission which can be partly explained by their mobile organization around docked vesicles. To investigate the relevance of Cav2.1 channel surface mobility for the input processing in the primary auditory cortex (A1) in vivo, we make use of a new optogenetic system which allows us to acutely cross-link Cav2.1 VGCCs via a photo-cross-linkable cryptochrome mutant, CRY2olig. In order to map neuronal activity across all cortical layers of the A1, we performed laminar current-source density (CSD) recordings with varying auditory stimulus sets in transgenic mice with a citrine tag on the N-terminus of the VGCCs. Clustering VGCCs suppresses overall sensory-evoked population activity, particularly when stimuli lead to a highly synchronized distribution of synaptic inputs. Our findings reveal the importance of membrane dynamics of presynaptic calcium channels for sensory encoding by dynamically adjusting network activity across a wide range of synaptic input strength. Statement of SignificanceVoltage Gated Calcium Channel (VGCC) mobility plays an important role in neuronal firing dynamics. Failure of these channels to function or be regulated has been linked to migraine and ataxia. We here link the microscopic process of VGCC mobility to the mesoscopic population dynamics as a mechanism to regulate and appropriately amplify synaptic inputs of different strengths to the mouse primary auditory cortex. We also demonstrate a novel and effective technique with which VGCC function can be further explored in meso- or macroscopic scales and with behaving subjects. We believe that this is of importance to the broader scientific community in aspects of non-linear scaling in the brain, potential translational applications, and basic research on cortical mechanisms of physiological function.

neuroscience↗

High-throughput super-resolution single particle trajectory analysis reconstructs organelle dynamics and membrane re-organization

Super-resolution imaging can generate thousands of single-particle trajectories. These data can potentially reconstruct subcellular organization and dynamics, as well as measure disease-linked changes. However, computational methods that can derive quantitative information from such massive datasets are currently lacking. Here we present data analysis and algorithms that are broadly applicable to reveal local binding and trafficking interactions and organization of dynamic sub-cellular sites. We applied this analysis to the endoplasmic reticulum and neuronal membrane. The method is based on spatio-temporal time window segmentation that explores data at multiple levels and detects the architecture and boundaries of high density regions in areas that are hundreds of nanometers. By statistical analysis of a large number of datapoints, the present method allows measurements of nano-region stability. By connecting highly dense regions, we reconstructed the network topology of the ER, as well as molecular flow redistribution, and the local space explored by trajectories. Segmenting trajectories at appropriate scales extracts confined trajectories, allowing quantification of dynamic interactions between lysosomes and the ER. A final step of the method reveals the motion of trajectories relative to the ensemble, allowing reconstruction of dynamics in normal ER and the atlastin-null mutant. Our approach allows users to track previously inaccessible large scale dynamics at high resolution from massive datasets. The SPtsAnalysis algorithm is available as an ImageJ plugin that can be applied by users to large datasets of overlapping trajectories and offer a standard of SPTs metrics.

cell biology↗

Reconstructing wells from high density regions extracted from super-resolution single particle trajectories

Large amount of super-resolution single particle trajectories has revealed that the cellular environment is enriched in heterogenous regions of high density, which remain unexplained. The biophysical properties of these regions are characterized by a drift and their extension (a basin of attraction) that can be estimated from an ensemble of trajectories. We develop here two statistical methods to recover the dynamics and local potential wells (field of force and boundary) using as a model a truncated Ornstein-Ulhenbeck process. The first method uses the empirical distribution of points, which differs inside and outside the potential well, while the second focuses on recovering the drift field. Finally, we apply these two methods to voltage-gated calcium channels and phospholipids moving on the surface of neuronal cells and recover the energy and size of these high-density regions with nanometer precision.

biophysics↗

Neuronal receptors display cytoskeleton-independent directed motion on the plasma membrane

Directed transport of transmembrane proteins is generally believed to occur via intracellular transport vesicles. However, using single particle tracking in rat hippocampal neurons with a pH-sensitive quantum dot probe which specifically reports surface movement of receptors, we have identified a subpopulation of neuronal EphB2 receptors that exhibit directed motion between synapses within the plasma membrane itself. This receptor movement occurs independently of the cytoskeleton but is dependent on cholesterol and is regulated by neuronal activity.

cell biology↗