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Scanavachi, G.

Publications and source records attributed to Scanavachi, G..

9 recordsLinked to original sources

Naked antisense oligonucleotides remain endolysosomally sequestered despite induced membrane damage

Antisense oligonucleotides (ASOs) enter cells efficiently, but the compartment from which productive escape occurs remains uncertain. We used live-cell microscopy, ratiometric pH measurements and 3D focused ion beam scanning electron microscopy (FIB-SEM) in U2OS cells to track a Malat1-targeting ASO from uptake to delivery. The ASO entered by endocytosis and accumulated in late endosomes, endolysosomes and lysosomes, where it induced luminal neutralization without galectin-3 recruitment or limiting-membrane rupture. Under conditions that reduced Malat1-RNA by >90%, quantitative imaging showed that less than 4% of internalized ASOs reached the nucleus. L-leucyl-L-leucine methyl ester (LLOMe)-induced membrane damage released co-internalized dextran but not ASOs, showing that ASOs remain sequestered even in damaged late endocytic compartments. In apilimod-expanded organelles, ASOs concentrated at limiting membranes and intraluminal foci with constrained motion, consistent with association with membrane and luminal structures. Although G3BP1/2 has been proposed to plug damaged endocytic membranes, we detected no recruitment of G3BP1 to endosomes or lysosomes; loss of G3BP1 and G3BP2 increased functional delivery modestly. We therefore propose that productive escape occurs earlier in endocytosis, most likely in early or recycling endosomes, where ASOs would still be unbound within the lumen and where membrane fusion and fission could generate perforations permitting release.

cell biology↗

SpatialDINO: A Self-Supervised 3D Vision Transformer that enables Segmentation and Tracking in Crowded Cellular Environments

Quantitative, time-resolved 3D fluorescence microscopy can reveal complex cellular dynamics in living cells and tissues. Broader use remains limited by the difficulty of identifying, segmenting, and tracking objects of different size and shape in crowded intracellular environments in low-contrast, anisotropic, monochromatic image volumes. Objects overlap, deform, appear and disappear, and span wide ranges of size and intensity. Classical segmentation pipelines typically require high signal-to-noise data and rely on intensity heuristics with hand-tuned postprocessing that generalize poorly. Supervised deep learning methods require extensive voxel-level annotations that are costly, inconsistent across phenotypes, and rapidly become obsolete as imaging conditions change. We introduce SpatialDINO, a fully automated self-supervised method that trains a native 3D vision transformer, based on a modified version of DINOv2 (1). SpatialDINO yields robust semantic feature maps from single channels of multi-channel microscopy that, irrespective of object shape, support object detection and segmentation directly from naive 3D images across z-spacings and numbers of planes and different imaging modalities, without retraining or voxel annotations. We trained SpatialDINO on a small set of confocal volumes acquired by live-cell fluorescent 3D lattice light-sheet microscopy, spanning targets of different size and shape located in crowded cellular environments, from diffraction-limited clathrin coated pits and clathrin coated vesicles to bigger structures including endosomes and lysosomes, and endosomes and lysosomes pharmacologically enlarged to highlight endosomal membrane profiles. Post-processing of the features generated by SpatialDINO allows detection and unique object identification of these objects in naive 3D images. It also enables detection of significantly different previously unseen object classes, such as cellular plasma membranes and nuclei and even tumors in MRI scans. Finally, we illustrate its value by tracking endosomes in 3D time series, combining SpatialDINO-derived feature similarity with spatial proximity to improve association through occlusion, abrupt appearance changes, and dense packing, all conditions that have been challenging for existing methods. SpatialDINO therefore lowers a major barrier to quantitative analysis of heterogeneous, monochromatic objects in crowded 3D cellular environments. SUMMARYLavaee et al. have developed SpatialDINO to surmount the difficulties presented by attempting to identify, segment, and track objects in crowded volumes. SpatialDINO is a self-supervised, native 3D vision transformer trained directly on unlabeled fluorescence volumes acquired by live-cell 3D lattice light-sheet microscopy. By learning dense volumetric representations without voxel-level supervision, SpatialDINO generates features that enable fully automated detection, segmentation, and tracking of subcellular structures across a wide range of sizes and morphologies in crowded, anisotropic 3D/4D datasets acquired with different microscopy modalities. The approach generalizes across targets and imaging conditions without further training, reducing dependence on manual annotation while maintaining performance in complex cellular environments. SIGNIFICANCESpatialDINO brings a self-supervised foundation model for analyzing 3D fluorescence microscopy images by adapting DINOv2-style joint-embedding training to learn dense volumetric features directly from unlabeled 3D datasets. By exploiting true 3D context rather than slice-wise "2.5D" aggregation, it enables automated detection and segmentation in crowded, anisotropic, low-contrast volume and enables tracking in 4D time-lapse data. SpatialDINO generalizes across targets and imaging conditions without voxel-level annotation or retraining.

cell biology↗

How endosomal PIKfyve inhibition prevents viral membrane fusion and entry

Enveloped viruses enter cells by membrane fusion. The viral membrane fuses with a host membrane, either at the cell surface or within endocytic compartments. For endocytic entry, fusion is typically triggered by low pH and often requires proteolytic priming by compartment-specific host proteases, which together define the site and mechanism of fusion and shape viral tropism. Inhibition of the lipid kinase PIKfyve, which generates PI(5)P and PI(3,5)P2 in late endosomes and lysosomes, swells those compartments and blocks infection by a subset of enveloped viruses, including Ebola virus, Marburg virus, coronaviruses (SARS-CoV-2), and VSV chimeras bearing Ebola, SARS-CoV-2, or Lassa glycoproteins, while showing minor effects on H1N1 influenza and no effect on VSV or VSV-rabies chimeras. In the work reported here, we have determined the basis for selectivity. We show that swelling of late endosomes/lysosomes, independent of changes in lipid composition or altered virion trafficking, is sufficient to block virus-endosome fusion and genome release, even when endosomal acidity is preserved. Acute PIKfyve inhibition with apilimod or brief hypotonic treatment produced endosomal swelling and impaired infection by interrupting a late endosomal entry step. Live-cell 3D lattice light-sheet fluorescence microscopy imaging tracked fluorescent virions accumulating and arresting in late endosomes prior to fusion, and single-cell, single-round assays confirmed loss of infectivity. These data support a simple biophysical mechanism: endo-lysosomal swelling, likely increasing endosomal membrane tension, creates an energy barrier to fusion and genome release. Inducing such swelling may offer a general strategy to inhibit viruses that depend on late endosomal entry. SIGNIFICANCE STATEMENTWhy does inhibiting the endosomal lipid kinase PIKfyve, which generates PI(5)P and PI(3,5)P2, block entry of some enveloped viruses but spare VSV-G? Using single-round infectivity and live-cell 3D imaging, we show that acute PIKfyve inhibition traps incoming VSV chimeras bearing SARS-CoV-2 spike or Ebola GP in swollen late endosomes/lysosomes before fusion and genome release. Hypotonic swelling phenocopies the block, and removing glutamine prevents apilimod-induced swelling and largely restores infection, arguing that swelling--not altered phosphoinositides--restricts entry. We propose a physical mechanism: increased endosomal membrane tension raises the energetic barrier for fusion-pore formation and genome release. Modulating endolysosomal volume may therefore inhibit viruses that rely on late endosomal entry.

cell biology↗

Tau seeding in neurons enabled by transient endolysosomal perforations are confined within endolysosomes

Pathogenic tau assemblies propagate by templated seeding. For endocytosed fibrils to initiate aggregation of endogenous tau, a breach must occur in the limiting membrane of an endosome or lysosome. To study the route by which internalized tau seeds access cytosolic monomers and to identify the site of aggregate growth, we imaged live human iPSC-derived neurons (iNs) expressing tau P301L-eGFP after exposure to recombinant tau pre-formed fibrils (PFFs) or Alzheimers disease (AD) brain-derived oligomers or fibrils. We detected seeded tau P301L- eGFP aggregation within late endosomes/lysosomes of iNs but not in undifferentiated iPSCs. Colocalization with a Dextran pH biosensor showed that the aggregates remained within the lumen of an intact, low-pH compartment. Reporters of endolysosomal injury and repair (endolysosomal recruitment cytosolic galectin-3 and the ESCRT-III component IST1) did not change during seeding. Volume focused-ion-beam scanning electron microscopy showed fibrillar material exclusively inside membrane-bounded endolysosomes, with no membrane discontinuities in the fibril-containing compartments and with no evidence of cytosolic aggregates. Because tau and -synuclein can cross-seed, we adapted a HaloTag pulse-chase assay to test for the persistence of trans-membrane access. AD fiber-containing endolysosomes progressively recruited cytosolic -synuclein-Halo over days, with heterogeneous incorporation histories consistent with recurrent, self-limited access events rather than persistent rupture or terminal sealing. Pharmacologic inhibition of the endolysosomal lipid kinase PIKfyve with apilimod suppressed seeded tau aggregation and prevented neuronal toxicity. These data indicate that templated conversion proceeds within acidic, membrane-intact endolysosomes; tau seeding in neurons is enabled by transient, self-limited endolysosomal perforations yet remains confined to the endolysosomal lumen, and it requires PIKfyve- dependent PI(3,5)P2.

neuroscience↗

Constitutive Endolysosomal Perforation in Neurons allows Induction of alpha-Synuclein Aggregation by Internalized Pre-Formed Fibrils

The endocytic pathway is both an essential route of molecular uptake in cells and a potential entry point for pathology-inducing cargo. The cell-to-cell spread of cytotoxic aggregates, such as those of -synuclein (-syn) in Parkinsons Disease (PD), exemplifies this duality. Here we used a human iPSC-derived induced neuronal model (iNs) prone to death mediated by aggregation in late endosomes and lysosomes of endogenous -syn, seeded by internalized pre-formed fibrils of -syn (PFFs). This PFF-mediated death was not observed with parental iPSCs or other non-neuronal cells. Using live-cell optical microscopy to visualize the read out of biosensors reporting endo-lysosome wounding, we discovered that up to about 10% of late endosomes and lysosomes in iNs exhibited spontaneous constitutive perforations, regardless of the presence of internalized PFFs. This wounding, absent in parental iPSCs and non-neuronal cells, corresponded to partial damage by nanopores in the limiting membranes of a subset of endolysosomes directly observed by volumetric focused ion beam scanning electron microscopy (FIB-SEM) in iNs and in CA1 pyramidal neurons from mouse brain, and not found in iPSCs or in other non-neuronal cells in culture or in mouse liver and skin. We suggest that the compromised limiting membranes in iNs and neurons in general are the primary conduit for cytosolic -syn to access PFFs entrapped within endo-lysosomal lumens, initiating PFF-mediated -syn aggregation. Significantly, eradicating the intrinsic endolysosomal perforations in iNs by inhibiting the endosomal Phosphatidylinositol-3-Phosphate/Phosphatidylinositol 5-Kinase (PIKfyve kinase) using Apilimod or Vacuolin-1 markedly reduced PFF-induced -syn aggregation, despite PFFs continuing to enter the endolysosomal compartment. Crucially, this intervention also diminished iN death associated with PFF incubation. Our results reveal the surprising presence of intrinsically perforated endo-lysosomes in neurons, underscoring their crucial early involvement in the genesis of toxic -syn aggregates induced by internalized PFFs. This discovery offers a basis for employing PIKfyve kinase inhibition as a potential therapeutic strategy to counteract synucleinopathies.

cell biology↗

Deep learning assisted single particle tracking for automated correlation between diffusion and function

Sub-cellular diffusion in living systems reflects cellular processes and interactions. Recent advances in optical microscopy allow the tracking of this nanoscale diffusion of individual objects with an unprecedented level of precision. However, the agnostic and automated extraction of functional information from the diffusion of molecules and organelles within the sub-cellular environment, is labor-intensive and poses a significant challenge. Here we introduce DeepSPT, a deep learning framework to interpret the diffusional 2D or 3D temporal behavior of objects in a rapid and efficient manner, agnostically. Demonstrating its versatility, we have applied DeepSPT to automated mapping of the early events of viral infections, identifying distinct types of endosomal organelles, and clathrin-coated pits and vesicles with up to 95% accuracy and within seconds instead of weeks. The fact that DeepSPT effectively extracts biological information from diffusion alone indicates that besides structure, motion encodes function at the molecular and subcellular level.

biophysics↗

Temporal Dynamics and Stoichiometry in Notch Signaling - from Notch Synaptic Complex Formation to NICD Nuclear Entry

Mammalian Notch signaling occurs when binding of Delta or Jagged to Notch stimulates proteolytic release of the Notch intracellular domain (NICD), which enters the nucleus to regulate target gene expression. To determine the temporal dynamics of events associated with Notch signaling under native conditions, we fluorescently tagged Notch and Delta at their endogenous genomic loci and visualized them upon pairing of receiver (Notch) and sender (Delta) cells as a function of time after cell contact. At contact sites, Notch and Delta immediately accumulated at 1:1 stoichiometry in synapses, which resolved by 15-20 min after contact. Synapse formation preceded entrance of the Notch extracellular domain into the sender cell and accumulation of NICD in the nucleus of the receiver cell, which approached a maximum after [~]45 min and was prevented by chemical and genetic inhibitors of signaling. These findings directly link Notch-Delta synapse dynamics to NICD production with unprecedented spatiotemporal precision.

cell biology↗

A Spatiotemporal Notch Interaction Map from Membrane to Nucleus

Notch signaling relies on ligand-induced proteolysis to liberate a nuclear effector that drives cell fate decisions. The location and timing of individual steps required for proteolysis and movement of Notch from membrane to nucleus, however, remain unclear. Here, we use proximity labeling with quantitative multiplexed mass spectrometry to monitor the microenvironment of endogenous Notch2 after ligand stimulation in the presence of a gamma secretase inhibitor and then as a function of time after inhibitor removal. Our studies show that gamma secretase cleavage of Notch2 occurs in an intracellular compartment and that formation of nuclear complexes and recruitment of chromatin-modifying enzymes occurs within 45 minutes of inhibitor washout. This work provides a spatiotemporal map of unprecedented detail tracking the itinerary of Notch from membrane to nucleus after activation and identifies molecular events in signal transmission that are potential targets for modulating Notch signaling activity.

molecular biology↗

Tracking infectious entry routes of SARS-CoV-2

SARS-CoV-2 cell entry starts with membrane attachment and ends with spike-protein (S) catalyzed membrane fusion depending on two cleavage steps, one usually by furin in producing cells and the second by TMPRSS2 on target cells. Endosomal cathepsins can carry out both. Using real-time 3D single virion tracking, we show fusion and genome penetration requires virion exposure to an acidic milieu of pH 6.2-6.8, even when furin and TMPRSS2 cleavages have occurred. We detect the sequential steps of S1-fragment dissociation, fusion, and content release from the cell surface in TMPRRS2 overexpressing cells only when exposed to acidic pH. We define a key role of an acidic environment for successful infection, found in endosomal compartments and at the surface of TMPRSS2 expressing cells in the acidic milieu of the nasal cavity. Significance StatementInfection by SARS-CoV-2 depends upon the S large spike protein decorating the virions and is responsible for receptor engagement and subsequent fusion of viral and cellular membranes allowing release of virion contents into the cell. Using new single particle imaging tools, to visualize and track the successive steps from virion attachment to fusion, combined with chemical and genetic perturbations of the cells, we provide the first direct evidence for the cellular uptake routes of productive infection in multiple cell types and their dependence on proteolysis of S by cell surface or endosomal proteases. We show that fusion and content release always require the acidic environment from endosomes, preceded by liberation of the S1 fragment which depends on ACE2 receptor engagement. One sentence summaryDetailed molecular snapshots of the productive infectious entry pathway of SARS-CoV-2 into cells

microbiology↗