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Heymann, T.

Publications and source records attributed to Heymann, T..

13 recordsLinked to original sources

Aggregate Deep Visual Proteomics reveals selective organization of α-synuclein inclusions

-Synuclein inclusions, the lesions typical of Parkinson's disease, have been interpreted as protective deposits, toxic species or failed degradation products, each predicting a different composition and correlating that enrichment with neuron dysfunction and eventual degeneration. Distinguishing them requires measuring what an inclusion concentrates relative to the cell that built it. Here we developed Aggregate Deep Visual Proteomics, which uses ultrasensitive mass spectrometry to profile laser-microdissected inclusions against the remainder of the same cell or a matched host. In HEK293 cells, iPSC-derived dopaminergic neurons and post-mortem patient brain, each inclusion concentrated a selective subset of its cell's proteome, independent of abundance and dominated by membrane, in neurons largely presynaptic. Inclusions took up whole assemblies, with subunits moving together in 421 of 438 complexes, and the V-ATPase alone was enriched in all three systems. Degradation cargo stayed with the receptors that route it, consistent with sequestration and failed degradation acting together. Neuritic and somatic inclusions differed, the former rich in UBQLN2 and the latter in intermediate filaments. In the cell line, phosphorylated -synuclein was tenfold higher in the inclusion than in the rest of the cell, with about one third of the rise already present before an inclusion was visible. Measured against its host, the composition of an inclusion becomes a readout of how it formed and a source of candidate markers and therapeutic targets.

biochemistry↗

The diverse functions of viral microproteins

A large fraction of the uncharacterized proteome consists of microproteins. Viruses, rich in microproteins with potent activities, provide a unique system for exploring their functions and evolution. Here, we systematically annotate viral microproteins through a phenotype-first approach: construction of a >50,000-element small ORF library spanning the microprotein-coding potential of human-infecting viruses, followed by broad screens that enrich candidates for high-resolution profiling by Perturb-seq, mass spectrometry, AI-guided structure prediction, and mechanistic studies. This atlas identified >2,000 active microproteins that modulate host pathways through diverse mechanisms, including molecular mimicry, hijacking of key regulators, and altering subcellular localization. We further show the oncogenic potential of BNLF2b, an uncharacterized Epstein-Barr virus microprotein linked to nasopharyngeal carcinoma. Three principles emerge: viral microproteins are diverse and often multifunctional, show widespread convergence toward shared functions, and serve as reservoirs of evolutionary innovation. These findings elucidate how viral microproteins occupy a large functional landscape, establish them as versatile tools for host manipulation, and provide a framework for functional annotation of uncharacterized proteins, contributing toward predictive systems virology.

systems biology↗

Deep Visual Proteomics links vascular smooth muscle cell phenotypes to atherosclerotic plaque stability

Vascular smooth muscle cells (VSMCs) drive atherosclerosis through phenotypic switching, yet their spatial organization and protein signatures within plaques remain poorly characterized. Here, we applied Deep Visual Proteomics (DVP) to dissect more than 500 VSMC neighborhoods across 24 human carotid plaques and profile VSMC plasticity in disease. To functionally interpret these tissue proteomes, we built a reference atlas of primary VSMCs driven toward five phenotypes by TGF-{beta}, PDGF-BB, osteogenic stimuli, IL-1{beta}, or cholesterol, quantifying over 10,000 proteins. We integrated tissue and reference proteomes with a deep-learning framework that assigns functional phenotypes to each neighborhood. This revealed spatially distinct phenotype distributions and a shift toward dedifferentiated states in unstable plaques. Knockdown of four candidates (TNC, TNFAIP2, AEBP1, PLK1) validated operational roles during phenotypic switching. Our approach functionally annotates spatial proteomes and links VSMC plasticity to plaque instability in carotid artery disease.

systems biology↗

In situ polymerized monolith tips for reproducible, format-flexible proteomic sample preparation applied to biofluids

Sample preparation increasingly sets the throughput and reproducibility of mass spectrometry (MS)-based proteomics. StageTips (stop-and-go extraction tips) and variants thereof have long been common implements to purify samples, and we recently extended the concept to solid-phase extraction capture (SPEC) tips, in which the entire digestion takes place in sub-microliter volumes. Here we replace the hand-packed bed with a strong anion-exchange (SAX) monolith photopolymerized directly inside the pipette tip from a defined recipe (pSPEC). A liquid-handling robot casts 384 tunable tips in minutes, at low cost and in any format, adding negligibly to the workflows variance. Across biofluids, pSPEC added [~]20% more identifications than in-solution plasma and reached 3,500 protein groups from a single injection of healthy urine and 4,800 from saliva at 100 samples per day, depths usually requiring depletion or fractionation. The same light-cast chemistry should extend to single cells, affinity capture, and population-scale studies.

biochemistry↗

HIP-MS: An ultra-high-throughput, sensitive, and versatile affinity enrichment platform for static and dynamic interactome profiling

Although protein-protein interactions govern virtually all cellular processes, systematic interactome mapping by affinity enrichment mass spectrometry (AE-MS) is constrained by manual sample preparation and lengthy liquid chromatography (LC)-MS/MS acquisition. Here we present High-throughput Interactome Profiling by MS (HIP-MS), an automated, end-to-end pipeline that overcomes these limitations. It leverages the compact, high-affinity ALFA tag for on-plate nanobody capture in 384-well format, combined with on-plate tryptic digestion. It can process almost 10,000 samples per week from protein expression up to MS measurement and can be combined with ultra-fast gradient LC-MS acquisition of 500 samples per day. HIP-MS remains sensitive down to low-microgram lysate inputs, a 4,000-fold reduction compared to recent large-scale screens. Our pipeline recovers complexes from diverse cellular compartments and resolves endogenous membrane receptor signaling. HIP-MS establishes a scalable foundation for systematic interrogation of protein interactions across conditions, perturbations, and time, and for the generation of large-scale datasets for computational modeling.

systems biology↗

A cell type-resolved proteomic atlas of the human body

Proteins define what cells do, yet their systematic quantification across human cell types has remained out of reach. Using Deep Visual Proteomics on tissue from a healthy female donor, we built an atlas of 27 cell types across 14 tissues, quantifying two-thirds of all human protein-coding genes, with up to 8,500 per population. The proteome partitions bimodally into a universal core and highly specialized programs. Integration into the Human Protein Atlas Single Cell Resource enabled comparison of RNA and protein abundance at cell type resolution, revealing that concordance depends on pathway rather than cellular identity. This resolution uncovered cancer-testis antigens in oocytes invisible to bulk profiling. Our openly accessible resource provides a foundation for cell type-resolved proteomics in health and disease.

biochemistry↗

Scanning DIA on the ZenoTOF 8600 system enables ultra-sensitive and quantitative proteomics from single cells to post-translational modifications in a compact platform

Mass spectrometry-based proteomics increasingly demands platforms that combine quantitative rigor with the discovery capabilities of accurate mass systems. Here we present the ZenoTOF 8600 system, a compact mass spectrometry system that integrates enhanced ion capture and transmission optics with an optical detection system, Zeno trap-enhanced MS/MS, electron-activated dissociation, and scanning quadrupole data-independent acquisition (ZT Scan DIA). We show that ZT Scan DIA outperforms conventional variable-window DIA (Zeno SWATH DIA) in both identifications and quantitative reproducibility, and demonstrate the platforms versatility across proteomics applications: thousands of protein groups from bulk samples at up to 500 samples per day, single-cell proteomics yielding up to 4,700 proteins, accurate ratio recovery in mixed-species quantitative benchmarks, low-attomole targeted quantitation, and detection of disease-relevant phosphorylation in a Parkinsons disease cellular model using complementary CID and EAD fragmentation. The instruments compact footprint makes it attractive for settings where both analytical breadth and operational robustness are required.

biophysics↗

A Solid-Phase Extraction Capture (SPEC) workflow in nanoliter volumes for fast, robust and ultrasensitive proteomics

Sample preparation remains a critical bottleneck in mass spectrometry (MS)-based proteomics, particularly for limited sample amounts where surface adsorption and dilution cause substantial losses. Here, we present Solid-Phase Extraction Capture (SPEC), a workflow that confines protein processing to nanoliter volumes within ion-exchange or C18 matrix inside a pipette tip. This achieves near-complete proteolysis within 5 minutes instead of hours and maintains full compatibility with strong detergents without cleanup steps, enabling effective lysis of challenging samples. From 200 ng FFPE tissue, SPEC achieves proteome depth and reproducibility exceeding conventional bulk protocols using 100 {micro}g, critical when sample is irreplaceable. The modular two-tip configuration enables on-tip chemical modifications for mTRAQ labeling and fractionation, while integration with enrichment workflows yields 2-fold improved glycopeptide identifications from plasma and 3-fold enhanced ubiquitin remnant identification at low amounts. SPEC enables nanoPhos for cell-type resolved tissue phosphoproteomics and provides a universal platform for proteomics sample preparation.

systems biology↗

nanoPhos enables ultra-sensitive and cell-type resolved spatialphosphoproteomics

Mass spectrometry (MS)-based phosphoproteomics has transformed our understanding of cell signaling, yet current workflows face limitations in sensitivity and spatial resolution at sub-microgram inputs. Here, we present nanoPhos, a robust method that extends phosphoproteomics to nanogram scale, making it compatible with cell-type-resolved spatial analysis. It employs loss-less solid phase extraction capture (SPEC) for sample preparation, followed by automated phosphopeptide enrichment using Fe(III)-NTA cartridges. nanoPhos identifies over 57,000 unique phosphorylation sites from 1 {micro}g cell lysate and over 4,000 from only 10 ng, a hundred-fold improvement from recent protocols. Combined with Deep Visual Proteomics (DVP), it enables region- and cell-type resolved phosphoproteomics of mouse brain tissue with spatial fidelity and a depth of 13,000 phosphosites from only 1000 cell shapes. This establishes nanoPhos as a versatile and ultra-sensitive platform that extends DVP to post-translational modifications and opens up for cell-type-specific signaling analysis in intact tissue.

systems biology↗

DCHS1 Modulates Forebrain Proportions in Modern Humans via a Glycosylation Change

Comparative anatomical studies of primates and extinct hominins, including Neanderthals, show that the modern human brain is characterised by a disproportionately enlarged neocortex relative to the striatum. To explore the molecular basis of this difference, we screened for missense mutations that are unique to modern humans and occur at high frequency and that alter post-translational sites. One such mutation was identified in DCHS1, a protocadherin family gene, and it was found to disrupt an N-glycosylation site in modern humans. Using CRISPR/Cas9-editing we introduced into human-induced pluripotent stem cells (hiPSCs) this ancestral DCHS1 variant present in Neanderthals and other primates, representing the ancestral state before the modern human-specific substitution. Leveraging hiPSCs-derived neural organoids, we observed an expansion of striatal progenitors at the expense of the neocortex, mirroring the anatomical distribution seen in non-human primates. We further identify the ephrin receptor EPHA4 as a binding partner of DCHS1 and show that modern human-specific alterations in DCHS1 modulate EPHA4-ephrin signalling, contributing to a gradual shift in the neocortex-to-striatum ratio - a hallmark of brain organisation in our species.

neuroscience↗

Acute and early stress axis modulation in joint disease permanently reduces pain and emotional comorbidities

Chronic pain affects 20-30% of the population and imposes a significant socio-economic burden as it is often accompanied by substantial emotional comorbidities such as anxiety and depression. Yet, the mechanisms underlying the interactions between the sensory and emotional aspects of chronic pain remain poorly understood. Here, we investigated the role of FKBP51, a regulator of the stress response, in mediating both sensory and emotional symptoms of chronic pain. Inhibition of FKBP51, via genetic deletion or pharmacological blockade, in persistent joint pain reduced fast-onset sensory, functional and activity-related symptoms, as well as late anxio-depressive comorbidities. FKBP51 inhibition after the establishment of the hypersensitive state provided only temporary symptoms relief, while acute inhibition at disease onset protected from the full development of sensory and anxio-depressive symptoms for up to 6 months. Our results also indicated that early pain symptoms could predict the late sensory and emotional outcomes of chronic pain. RNA sequencing of spinal cord tissue revealed that late FKBP51 inhibition transiently altered nociceptive genes associated with mechanical hypersensitivity. In contrast, early inhibition persistently downregulated the Naaa gene, a key regulator of the transition to chronic pain, and reorganized spinal cilia. Our results indicate that early FKBP51 inhibition after injury can persistently reduce chronic pain and prevent the onset of associated emotional comorbidities by modulating critical spinal neurobiological pathways that play pivotal roles in the transition to chronic pain. Significance statementOur study reveals that early inhibition of FKBP51, a modulator in the stress axis, at the onset of joint damage provides sustained pain relief and significantly delays or prevents emotional comorbidities in a sex-dependent manner. In contrast, FKBP51 inhibition initiated after chronic pain is established results in only temporary symptoms improvement. These findings highlight a critical therapeutic window during which timely intervention can prevent the transition from acute to chronic pain. By establishing a predictive link between early therapeutic response and long-term outcomes, this work has important clinical implications for proactive and personalized chronic pain management.

neuroscience↗

AlphaDIA enables End-to-End Transfer Learning for Feature-Free Proteomics

Mass spectrometry (MS)-based proteomics continues to evolve rapidly, opening more and more application areas. The scale of data generated on novel instrumentation and acquisition strategies pose a challenge to bioinformatic analysis. Search engines need to make optimal use of the data for biological discoveries while remaining statistically rigorous, transparent and performant. Here we present alphaDIA, a modular open-source search framework for data independent acquisition (DIA) proteomics. We developed a feature-free identification algorithm particularly suited for detecting patterns in data produced by sensitive time-of-flight instruments. It naturally adapts to novel, more eTicient scan modes that are not yet accessible to previous algorithms. Rigorous benchmarking demonstrates competitive identification and quantification performance. While supporting empirical spectral libraries, we propose a new search strategy named end-to-end transfer learning using fully predicted libraries. This entails continuously optimizing a deep neural network for predicting machine and experiment specific properties, enabling the generic DIA analysis of any post-translational modification (PTM). AlphaDIA provides a high performance and accessible framework running locally or in the cloud, opening DIA analysis to the community.

bioinformatics↗

Involvement of FKBP5, but not of stress, in alcohol memory reconsolidation

Relapse is a fundamental challenge in drug addiction, often evoked by exposure to drug-associated cues. Upon retrieval, memories become temporarily labile before re-stabilizing in a process termed reconsolidation. Therefore, targeting the reconsolidation process offers a therapeutic approach for relapse prevention via the disruption of the drug-cue memories. We recently demonstrated that retrieval of contextual alcohol memories increased the expression of the mRNA encoding for FK506 binding protein 51 (FKBP51), a regulator of the hypothalamic-pituitary-adrenal (HPA) axis. Here, we explored the role of the HPA axis, and FKBP5/FKBP51 in particular, in the reconsolidation of alcohol memories. We found that the FKBP51 inhibitor SAFit2 given before alcohol-memory retrieval using contextual cues prevented the extinction of alcohol place preference behavior in female mice, suggesting that this protein may play a role in cognitive flexibility in a sex-dependent manner. Conversely, the retrieval of alcohol memories using an odor-taste cue did not affect Fkbp5 expression in rats with a history of chronic alcohol consumption, suggesting that FKBP5 may play a differential role in different alcohol-associated memories. In addition, we provide evidence for HPA axis activation following alcohol memory retrieval, by showing that exposure to an alcohol-associated context led to elevated corticosterone secretion. However, we found that the reconsolidation process was unaffected by HPA axis-related manipulations, namely stress exposure, and administration of corticosterone or the glucocorticoid receptors inhibitor, mifepristone. Our results suggest that although FKBP5 can affect cognitive flexibility, and thereby impact the reconsolidation of alcohol memories, this effect is not likely mediated by HPA axis-related mechanisms.

neuroscience↗