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Kelly, J. W.

Publications and source records attributed to Kelly, J. W..

At least 19 recordsLinked to original sources

Rank Normalization Enables Cross Pathway Comparison in Degradation Resolved Proteome Turnover Analysis

Protein homeostasis, or proteostasis, is essential for cellular health, and its disruption contributes to cancer, aging, and neurodegenerative disease. Proteostasis is maintained largely by two intracellular degradation systems: the ubiquitin proteasome system (UPS) and the autophagy lysosomal pathway (ALP). Here, we combine pulse stable isotope labeling by amino acids in cell culture (pSILAC) with selective inhibition of the UPS or ALP to quantify pathway-dependent protein turnover and identify substrates that are preferentially cleared through each route. Direct comparison of these perturbations is complicated by their markedly different response distributions. To address the mismatch in dynamic range, we developed a normalization strategy based on within-condition ranks. Protein stabilization values are converted to percentile scores before comparison across pathways, placing both perturbations on a common relative response scale. Across two independent pSILAC experiments, 5,518 proteins were quantified in at least one condition, and 3,814 yielded high confidence half-life measurements in control, proteasome-inhibited, and lysosome-inhibited conditions. Rank normalization resolved pathway sensitivities that were obscured by direct comparison of absolute half-life changes. Importantly, the method reports relative pathway preference rather than absolute pathway contribution, exchanging effect size magnitude for comparability across perturbations with unequal response distributions. Integration with a curated proteostasis network annotation revealed coherent pathway preferences, including coordinated stabilization of proteasome core and regulatory subunits following lysosomal inhibition. This finding provides proteome-wide quantitative evidence for proteaphagy that complements previous targeted observations. Together, these results establish rank normalization as a practical strategy for comparing degradation resolved proteome turnover across perturbations with different dynamic ranges.

molecular biology↗

The Microglial Protein sTREM2 Inhibits the Bacterial Functional Amyloid CsgA and Suppresses Amyloid-Dependent Biofilm Formation

Protein misfolding and aggregation, including amyloid fibril formation, underlie a large class of human diseases including prominent neurological disorders such as Alzheimers and Parkinsons disease. A small number of human proteins have been identified that inhibit amyloidogenesis. One such protein is sTREM2, a soluble receptor liberated from microglia, the resident macrophages of the central nervous system. The extracellular domain of TREM2 is shed upon proteolytic cleavage to create sTREM2, which has previously been shown to inhibit amyloid-{beta} aggregation in vitro. TREM2 is also expressed by intestinal macrophages, which are known to directly bind the bacterial amyloid curli and mount cytokine responses upon exposure. Here we show that sTREM2 is a sub-stoichiometric inhibitor of CsgA amyloidogenesis, CsgA being the major protein component of curli that drives biofilm formation in uropathogenic Escherichia coli and many other proteobacteria. In vitro, sTREM2 potently and sub-stoichiometrically inhibited CsgA amyloidogenesis in a dose-dependent manner. Kinetic modeling indicated that sTREM2 slowed primary and secondary nucleation, rather than altering fiber elongation. When added exogenously to bacterial growth medium, sTREM2 significantly suppressed curli-dependent pellicle biofilm formation without affecting bacterial growth. These findings establish sTREM2 as a member of the small group of human proteins capable of inhibiting bacterial functional amyloidogenesis, suggesting that gut-resident TREM2-expressing macrophages, which are already known to interact with curli, may employ sTREM2 as a physiologically relevant defense against bacterial amyloid formation.

biochemistry↗

Siphoviridae phage tails co-enrich with ex vivo amyloids

Amyloid fibrils extracted from patient tissue are enriched by physicochemical fractionation methods and enzymatic tissue digestion with collagenase, resulting in a mixture of sedimented complexes. Reprocessing of an ex vivo lysozyme amyloid dataset revealed non-amyloid tubular assemblies, which we reconstructed to 3.5 angstrom. Sequence-agnostic model building with CryoAtom and fold search with FoldSeek identified a phage tail tube fold. Testing the crude Clostridium histolyticum collagenase used for tissue digestion, negative-stain TEM and LC-MS/MS showed proteins of an F-type tailocin, allowing us to assign the helical reconstruction to a major tail tube protein (TTP) of C. histolyticum. We also observed tailocin contamination in cardiac light-chain amyloid extracts, following the same collagenase treatment. Overall, we identify tailocins as recurrent reagent-borne contaminants in collagenase-treated ex vivo amyloid preparations and propose strategies to detect and avoid such artefacts in single-particle cryo-EM by optimizing the experimental design and data annotation towards a database of common contaminants.

biophysics↗

Molecular and Structural Characterization Reveals Divergent Extracellular Vesicle Profiles Between Wild Type and Alzheimer's Disease Cerebrocortical Organoids

Alzheimers disease (AD) is a neurodegenerative disorder affecting millions of patients globally. Despite significant efforts from researchers in recent decades, there are still many unanswered questions about AD pathogenesis. AD patient brains manifest changes in extracellular vesicles (EVs) secreted from diseased neurons, and the effect of this phenomenon remains poorly understood. EVs contain a variety of biomolecules and play a critical role in cell-to-cell communication in all eukaryotic organisms. Here, we report a thorough characterization of small EVs purified from cultures of human cerebrocortical organoids. These organoids are differentiated from human patient-derived stem cells that bear a familial AD mutation in the presenilin 1 (PSEN1) gene, or from an isogenic wildtype (WT) control. The organoid conditioned media was aspirated from cultures and processed for EV enrichment using a non-invasive technique that requires no cellular disruption. EVs purified from AD organoid conditioned media have a wider size distribution and show differential expression of tetraspanins CD63, CD9, and CD81 when compared to WT organoid-derived EVs. AD organoid-derived EVs can have single, double, and even triple membranes and display luminal fibrillar material. A deep proteomic profiling of the EVs reveals several statistically significant differences, including evidence for modifications in secretory autophagy. EV isolates from both WT and AD organoids show strong binding to amyloid detecting dyes, both in bulk fluorescence and fluorescence microscopy assays. After a 1-week co-culture of AD organoids with WT organoids, there is evidence of endosomal membrane transfer between the isogenic cultures with an increase in amyloid-{beta} peptides in the WT organoids. These observations support the notion that non-cell-autonomous spread of amyloid-containing EVs in human AD brains can be modeled in a cerebral organoid system.

neuroscience↗

Impaired lipoprotein secretion by APOE4 leads to lysosomal and mitochondrial dysfunction in human microglia

While Apolipoprotein E4 (APOE4) is the greatest known genetic risk factor for late-onset Alzheimers disease, its mechanistic role in the brain-resident macrophage, microglia, remains elusive. Microglia are important in the clearance of pathology in disease, heavily relying on lysosome functionality; therefore, we sought to understand the impact of APOE4 on microglial function. APOE44 microglia have been shown to have lipid accumulation, yet the mechanisms leading to this accumulation are unknown. Using induced pluripotent stem cell-derived microglia, we found that the APOE4 haplotype resulted in transcriptional state shifts in microglia, suppressing activated-response microglia (ARMs) and promoting a G2 senescent-like state. We found that APOE44 microglia accumulate cholesterol esters and provide less lipid support to fibroblast-induced neurons, decreasing their synaptic connections. APOE44 microglia secrete significantly less lipoproteins, leading to the accumulation of lipoproteins within the cells including the lysosomes. APOE44 microglia exhibit impaired lysosomal acidification and degradation capacity. Further, our results elucidated that APOE44 microglia are proinflammatory and shift away from fatty acid oxidation towards glycolysis, due to dysfunctional mitochondria. Taken together, our findings indicate that a loss-of-function in lipoprotein secretion drives intracellular lipid accumulation, including within lysosomes, ultimately disrupting the lysosome-endoplasmic reticulum-mitochondrial axis. This drives a proinflammatory and metabolically compromised microglial phenotype with impaired neuro-supportive functions. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=138 SRC="FIGDIR/small/724612v1_ufig1.gif" ALT="Figure 1"> View larger version (44K): org.highwire.dtl.DTLVardef@18d6a2org.highwire.dtl.DTLVardef@b3644dorg.highwire.dtl.DTLVardef@17e3716org.highwire.dtl.DTLVardef@1529caf_HPS_FORMAT_FIGEXP M_FIG C_FIG

neuroscience↗

Survey of the human proteostasis network: the ubiquitin-proteasome system

Modification by ubiquitination governs the half-lives of thousands of proteins that are fated for elimination by either the proteasome or autophagy pathways, depending on the intricate architectures of ubiquitin modification. This system mediates quality control for individual proteins, protein complexes, and organelles, as well as myriad purely regulatory functions. Here we provide a comprehensive survey of the ubiquitin-proteasome system (UPS), the scope of which is at present poorly defined. The UPS, with the inclusion of pathways involving ubiquitin-like modifiers, comprises in our estimate over 1430 distinct proteins in humans, a vast set of activities whose collective impact on the biology of the cell is pervasive. The UPS is an integral component of the proteostasis network (PN), the remainder of which we have also surveyed in recent studies. With the addition of molecular chaperones, proteins from autophagy-lysosome pathway, and related activities, the PN includes in total over 3150 components by our estimates. Comprehensive and systematic definition of these pathways should support a range of ongoing investigations in the areas of genomics, proteomics, biochemistry, cell biology, and disease research.

bioinformatics↗

3D Visualization and Proteomic Analysis of Human Cardiac Transthyretin Amyloidosis Tissue Reveals Microangiopathy and Capillary Occlusion

AO_SCPLOWBSTRACTC_SCPLOWO_ST_ABSBackgroundC_ST_ABSTransthyretin amyloidosis (ATTR) is a progressive, degenerative disease affecting the heart and other organ systems, as well as the peripheral, autonomic, and central nervous systems. Although pharmacological and genetic evidence establishes aggregation as a driver of ATTR pathology, the mechanism by which aggregation compromises post-mitotic tissue function is poorly understood. We utilized bottom-up proteomics on wild-type (WT) human cardiac (WT/WT genotype) and V122I human cardiac (V122I/WT genotype) tissue, combined with tissue clearing technology to create an optically transparent tissue architecture to visualize three-dimensional relationships, to better understand TTR cardiomyopathy (CM). MethodsFlash-frozen 0.5 mm cardiac tissue slices from human subjects with end-stage WT-TTR CM, end-stage V122I CM, and slices from an age-matched human control were used for these experiments. Fibril extraction from diseased tissue followed published protocols. Strong denaturant-mediated proteome tissue extraction on samples from each subject facilitated bottom-up proteomics by using liquid chromatography (LC)-mass spectrometry (MS)/MS. Tissue clearing was performed on 0.5 mm cardiac slices utilizing a lauryl sulfate-based lipid removal strategy. Slices were stained using indirect immunofluorescence with antibodies to protein targets identified by proteomics. We used an antibody to non-native TTR and AmyTracker 480 (an oligothiophene dye that binds to amyloid fibrils) to image TTR deposits. ATTR fibrils were characterized structurally using cryogenic electron microscopy (cryo-EM) followed by helical reconstruction. ResultsProteomic cardiac analysis afforded high spectral counts for transthyretin (TTR) and proteins typically associated with amyloid fibrils, e.g. serum amyloid P (APCS). Fibril and cardiac homogenate proteomics revealed high levels of angiogenic and hemostatic proteins, including those composing the complement and coagulation cascades. 3D imaging revealed loss of normal microvascular architecture in CM samples with regions of hyper- and hypovascularization. Microvascular obstruction by capillary thrombosis was also observed in CM. ATTR fibrils adopted the common spearhead fold and were decorated with collagen VI (COLVI), an extracellular matrix component. ConclusionsWe hypothesize that ATTR CM is a microangiopathy driven by capillary bed thrombo-inflammation and dysregulated angiogenic revascularization. Phenotypic convergence of WT ATTR CM and V122I ATTR CM was observed via proteomics, 3D imaging, and ex vivo fibril characterization by cryo-EM. We provide evidence of capillary thrombosis in ex vivo ATTR CM tissue. Vasodilation and increased capillary permeability expose components of the vascular basement membrane (VBM) to misfolded TTR. These components are known to promote TTR aggregation and stabilize amyloid fibrils in the extracellular space. Congestion of the VBM prevents appropriate revascularization, reducing cardiac exertional capacity over time, leading to heart failure. Our ATTR CM heart tissue proteomics data shows significant overlap with the proteomic profiles of human AD brain tissues, revealing key amyloid, coagulation, complement, and angiogenesis proteins being changed in amyloidoses.

pathology↗

Ketone body beta-hydroxybutyrate restores neuronal Tau proteostasis via ketolysis-independent mechanism

Metabolic interventions that induce ketosis, including ketogenic diets, caloric restriction, intermittent fasting, and exercise, show promise in the treatment of Alzheimers disease (AD) and related tauopathies. {beta}-hydroxybutyrate ({beta}HB), the primary ketone body produced during ketosis, reproduces key features of these metabolic interventions, but the molecular mechanism underlying its neuroprotective properties is not fully understood. Here, we demonstrate that a {beta}HB precursor diet is sufficient to ameliorate Tau pathophysiology in a tauopathy mouse model. Furthermore, across in vitro, ex vivo, and in vivo models, we find that {beta}HB enhances neuronal Tau proteostasis and reduces Tau aggregation and secretion. Importantly, these effects are independent of {beta}HBs oxidation for ATP production, as its ketolysis-resistant enantiomer reproduces these benefits, indicating that ketolysis is dispensable for these effects. Overall, these data position {beta}HB as a novel therapeutic avenue for AD and tauopathy and elucidate a novel mechanism of action of metabolic interventions in neurodegenerative disease.

neuroscience↗

A HaloTag-4R-Tau Pulse-Chase Sensor Reveals Neddylation Inhibition Promotes Degradation of Tau in iNeurons

Tau accumulation is a central driver of neurodegenerative diseases, yet strategies to promote its clearance remain limited. We developed a HaloTag-4R-Tau sensor in human iPSC-derived neurons (iNeurons) that enables sensitive monitoring the kinetics of both lysosomal partitioning and overall cellular turnover of tau. Using this sensor, we screened a small collection of small-molecule modulators of proteostasis network function and identified Neddylation inhibition by Pevonedistat as a robust promoter of soluble tau degradation. Mechanistic analysis including proteomic profiling revealed that Neddylation inhibition hastens HaloTag-Tau clearance via compensatory activation of a proteasome-dependent pathway(s) as well as the autophagy-lysosome pathway. Our findings establish a powerful tool for probing tau homeostasis and highlight Neddylation inhibition as a potential therapeutic approach for enhancing both proteasome and lysosome-mediated tau clearance in tauopathies.

neuroscience↗

Small molecule stabilization of diverse amyloidogenic immunoglobulin light chains revealed by hydrogen-deuterium exchange mass spectrometry

Immunoglobulin light chains, a component of antibodies, can misfold and aggregate to cause systemic AL amyloidosis. Aggregation, including amyloid fibril formation, requires unfolding of the full-length light chain from its native state, and in most cases aberrant proteolysis. Small molecules that bind to the native state of light chains to stabilize them against conformational excursions and proteolysis are under development as drug candidates for AL amyloidosis. Since each patient has a unique light chain sequence, a challenge for candidate stabilizer drugs is to bind multiple light chains and suppress their dynamics. Here, we used hydrogen-deuterium exchange measured by mass spectrometry to characterize the binding of six small molecule stabilizers to eleven different {lambda} light chain proteins. Despite structural and dynamic differences among the light chains, the binding of the most efficacious stabilizer molecule led to increased protection from hydrogen exchange, consistent with reduced local and global unfolding. Protection upon binding was most prominent in residues within complementarity determining region 3 and framework region 4 of the light chain variable domains, which undergo major conformational changes enabling amyloid formation. Stabilizer binding also reduced the rate at which all light chains were cleaved by protease. These data show that these stabilizers suppress the range of conformational dynamics associated with light chain aggregation, supporting their therapeutic potential. HighlightsO_LISmall-molecule kinetic stabilizers suppress conformational dynamics and aberrant proteolysis of diverse amyloidogenic full-length {lambda} light chains. C_LIO_LIHDX-MS indicates conserved protection in regions forming the interface between the two variable domains of the light chain dimer, corresponding to residues that form the core of patient-derived amyloid fibrils. C_LIO_LIPLIMSTEX binding titrations show coupled binding, dimerization and stabilization at sub-micromolar kinetic stabilizer concentrations. C_LIO_LISmall molecule kinetic stabilization across different {lambda} sequences supports kinetic stabilizers as a promising therapeutic strategy for AL amyloidosis. C_LI

biophysics↗

Cathepsin C-Catalyzed Ligation Generates Intralysosomal Amyloid Fibrils from Dipeptide Esters

The lysosome is a major catabolic organelle responsible for the breakdown of both intra- and extracellular substrates1,2. Lysosomal membrane damage mediated by pathologic amyloid fibrils is an area of recent focus3-6. The dipeptide ester LLOMe is typically employed to model lysosomal membrane damage7-11; however its mechanism of membranolysis was previously incompletely understood. Here, in vitro and cell-based analyses, and cryo-electron microscopy and tomography studies reveal LLOMe-derived oligopeptides generated by the lysosomal protease Cathepsin C assemble into cross-{beta}-sheet amyloid fibrils within the lysosome. Additionally, we report lysosome membrane damage triggers the broadly nonspecific dipeptidyl ligase activity of Cathepsin C, facilitating the tagging of proximal proteins within the damaged lysosome lumen with a click chemistry handle: to our knowledge, the first reported localized proximity labeling approach exploiting a fully endogenous, non-engineered enzyme. While Cathepsin C ligase activity has been demonstrated in vitro12,13, our observations of dipeptidyl ligation onto proximal proteins in cells suggests an unexplored role of Cathepsin C in lysosomal biology and broadly exemplifies how other endogenous enzymes might be similarly exploited for proximity labeling. Altogether our results unveil two mechanisms by which dipeptide esters perturb lysosomal homeostasis and provide a roadmap for their utilization toward targeted studies of the lysosome.

biochemistry↗

Helical Reconstruction of Amyloids in cryoSPARC

Amyloid-mediated proteotoxicity underlies more than 50 human diseases. Cryo-electron microscopy (cryo-EM) analyses have yielded hundreds of in vitro and patient-derived amyloid structures, establishing direct links between filament morphologies and specific pathological conditions. Despite the growing popularity of the processing software cryoSPARC for single-particle analyses, RELION remains the dominant software platform for performing helical reconstruction of amyloid structures, highlighting an area for further development. Here, we present comprehensive processing guidelines for helical reconstruction of helical amyloids using cryoSPARC. Through systematic re-processing and validation of publicly deposited datasets, we demonstrate current capabilities and identify key limitations, emphasizing the need for amyloid-specific parameter optimization within cryoSPARC workflows. Our findings showcase a potential for developing unsupervised processing workflows to meet the demanding throughput requirements of time-resolved in vitro studies and largescale compound screening initiatives, thereby accelerating therapeutic drug development. Ultimately, our goal is to shift the focus of amyloid cryo-EM from computationally intensive processing challenges toward addressing fundamental biological questions that enhance our capacity for treatment discovery. O_FIG O_LINKSMALLFIG WIDTH=110 HEIGHT=200 SRC="FIGDIR/small/680389v2_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@1f2e9fcorg.highwire.dtl.DTLVardef@dfb6f5org.highwire.dtl.DTLVardef@164a2c3org.highwire.dtl.DTLVardef@1f9c570_HPS_FORMAT_FIGEXP M_FIG C_FIG

bioinformatics↗

Autophagy activators normalize aberrant Tau proteostasis and rescue synapses in human familial Alzheimer's disease iPSC-derived cortical organoids

Alzheimers disease (AD) is the most common form of dementia worldwide. Despite extensive progress, the cellular and molecular mechanisms of AD remain incompletely understood, partially due to inadequate disease models. To illuminate the earliest changes in hereditary (familial) Alzheimers disease, we developed an isogenic AD cerebrocortical organoid (CO) model. Our refined methodology produces COs containing excitatory and inhibitory neurons alongside glial cells, utilizing established isogenic wild-type and diseased human induced pluripotent stem cells (hiPSCs) carrying heterozygous familial AD mutations, namely PSEN1{Delta}E9/WT, PSEN1M146V/WT, or APPswe/WT. Our CO model reveals time-progressive accumulation of amyloid beta (A{beta}) species, loss of monomeric Tau, and accumulation of aggregated high-molecular-weight (HMW) phospho(p)-Tau species. This is accompanied by neuronal hyperexcitability, as observed in early human AD cases on electroencephalography (EEG), and synapse loss. Single-cell RNA-sequencing analyses reveal significant differences in molecular abnormalities in excitatory vs. inhibitory neurons, helping explain AD clinical phenotypes. Finally, we show that chronic dosing with autophagy activators, including a novel CNS-penetrant mTOR inhibitor-independent drug candidate, normalizes pathologic accumulation of A{beta} and HMW p-Tau, normalizes hyperexcitability, and rescues synaptic loss in COs. Collectively, our results demonstrate these COs are a useful human AD model suitable for assessing early features of familial AD etiology and for testing drug candidates that ameliorate or prevent molecular AD phenotypes. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/661453v2_ufig1.gif" ALT="Figure 1"> View larger version (58K): org.highwire.dtl.DTLVardef@12ac9c6org.highwire.dtl.DTLVardef@24eceaorg.highwire.dtl.DTLVardef@3e3238org.highwire.dtl.DTLVardef@1530d1e_HPS_FORMAT_FIGEXP M_FIG C_FIG

neuroscience↗

Phenylhydrazone-based Endoplasmic Reticulum Proteostasis Regulator Compounds with Enhanced Biological Activity

Pharmacological enhancement of endoplasmic reticulum (ER) proteostasis is an attractive strategy to mitigate pathology linked to etiologically-diverse protein misfolding diseases. However, despite this promise, few compounds have been identified that enhance ER proteostasis through defined mechanisms of action. We previously identified the phenylhydrazone-based compound AA263 as a compound that promotes adaptive ER proteostasis remodeling through mechanisms including preferential activation of the ATF6 signaling arm of the unfolded protein response (UPR). However, the protein target(s) of AA263 and the potential for further development of this class of ER proteostasis regulators had not been previously explored. Here, we employ chemical proteomics to demonstrate that AA263 covalently targets a subset of ER protein disulfide isomerases, revealing a potential molecular mechanism for the activation of ATF6 afforded by this compound. We then use medicinal chemistry to establish next-generation AA263 analogs showing improved potency and efficacy for ATF6 activation, as compared to the parent compound. Finally, we show that treatment with these AA263 analogs enhances secretory pathway proteostasis to correct the pathologic protein misfolding and trafficking of both a destabilized, disease-associated 1-antitrypsin (A1AT) variant and an epilepsy-associated GABAA receptor variant. These results establish AA263 analogs with enhanced potential for correcting imbalanced ER proteostasis associated with etiologically-diverse protein misfolding disorders.

cell biology↗

Activation of XBP1s attenuates disease severity in models of proteotoxic Charcot-Marie-Tooth type 1B

Mutations in myelin protein zero (MPZ) are generally associated with Charcot-Marie-Tooth type 1B (CMT1B) disease, one of the most common forms of demyelinating neuropathy. Pathogenesis of some MPZ mutants, such as S63del and R98C, involves the misfolding and retention of MPZ in the endoplasmic reticulum (ER) of myelinating Schwann cells. To cope with proteotoxic ER-stress, Schwann cells mount an unfolded protein response (UPR) characterized by activation of the PERK, ATF6 and IRE1/XBP1 pathways. Previous results showed that targeting the PERK UPR pathway mitigates neuropathy in mouse models of CMT1B; however, the contributions of other UPR pathways in disease pathogenesis remains poorly understood. Here, we probe the importance of the IRE1/XBP1 signalling during normal myelination and in CMT1B. In response to ER stress, IRE1 is activated to stimulate the non-canonical splicing of Xbp1 mRNA to generate spliced Xbp1 (Xbp1s). This results in the increased expression of the adaptive transcription factor XBP1s, which regulates the expression of genes involved in diverse pathways including ER proteostasis. We generated mouse models where Xbp1 is deleted specifically in Schwann cells, preventing XBP1s activation in these cells. We observed that Xbp1 is dispensable for normal developmental myelination, myelin maintenance and remyelination after injury. However, Xbp1 deletion dramatically worsens the hypomyelination and the electrophysiological and locomotor parameters observed in young and adult CMT1B neuropathic animals. RNAseq analysis suggested that XBP1s exerts its adaptive function in CMT1B mouse models in large part via the induction of ER proteostasis genes. Accordingly, the exacerbation of the neuropathy in Xbp1 deficient mice was accompanied by upregulation of ER-stress pathways and of IRE1-mediated RIDD signaling in Schwann cells, suggesting that the activation of XBP1s via IRE1 plays a critical role in limiting mutant protein toxicity and that this toxicity cannot be compensated by other stress responses. Schwann cell specific overexpression of XBP1s partially re-established Schwann cell proteostasis and attenuated CMT1B severity in both the S63del and R98C mouse models. In addition, the selective, pharmacologic activation of IRE1/XBP1 signaling ameliorated myelination in S63del dorsal root ganglia explants. Collectively, these data show that XBP1 has an essential adaptive role in different models of proteotoxic CMT1B neuropathy and suggest that activation of the IRE1/XBP1 pathway may represent a therapeutic avenue in CMT1B and possibly for other neuropathies characterized by UPR activation.

neuroscience↗

The conformational landscape of human transthyretin revealed by cryo-EM

Transthyretin (TTR) is a natively tetrameric thyroxine transporter found in blood and cerebrospinal fluid whose misfolding and aggregation causes transthyretin amyloidosis. A rational drug design campaign identified the small molecule tafamidis (Vyndaqel/Vyndamax) as an effective stabilizer of the native TTR fold, and this aggregation inhibitor is regulatory agency-approved for the treatment of TTR amyloidosis. Despite 50 years of structural studies on TTR and this triumph of structure-based drug design, there remains a notable dearth of structural information available to understand ligand binding allostery and amyloidogenic TTR unfolding intermediates. We used single-particle cryo-electron microscopy (cryo-EM) to investigate the conformational landscape of this 55 kiloDalton tetramer in the absence and presence of one or two ligands, revealing inherent asymmetries in the tetrameric architecture and previously unobserved conformational states. These findings provide critical mechanistic insights into negatively cooperative ligand binding and the structural pathways responsible for TTR amyloidogenesis. This study underscores the capacity of cryo-EM to provide new insights into protein structures that have been historically considered too small to visualize and to identify pharmacological targets suppressed by the confines of the crystal lattice, opening uncharted territory in structure-based drug design.

molecular biology↗

Aβ Amyloid Scaffolds the Accumulation of Matrisome and Additional Proteins in Alzheimer's Disease

We report a highly significant correlation between human Alzheimers disease (AD) brain proteome changes and those in CRND8 APP695NL/F transgenic mice. Comparing protein changes observed in the CRND8 mice with co-expression networks derived from human Alzheimers disease (AD), reveals both conserved and divergent module changes. Many proteins in the most highly conserved module (M42, matrisome) accumulate in plaques, cerebrovascular amyloid (CAA), dystrophic neuronal processes, or a combination thereof. Overexpression of two M42 proteins, midkine (Mdk) and pleiotrophin (PTN), in CRND8 mice brains leads to increased accumulation of A{beta} in plaques and in blood vessels; further, recombinant MDK and PTN enhance A{beta} aggregation into amyloid structures. Multiple M42 proteins bind to fibrillar A{beta}42 and a non-human amyloid fibril in vitro. Supporting this binding data, MDK and PTN co-accumulate with transthyretin (TTR) amyloid in the heart. Notably, our findings establish that proteomic changes in modules observed in human AD brains define an A{beta} amyloid "responsome" that is well conserved from mouse models to humans. Further, distinct amyloid structures appear to serve as scaffolds, facilitating the co-accumulation of proteins with signaling functions, and this co-accumulation may contribute to downstream pathological sequalae. Overall, this contextualized understanding of proteomic changes and their interplay with amyloid deposition provides valuable insights into the complexity of AD pathogenesis and potential biomarkers and therapeutic targets.

neuroscience↗

Proteostasis and lysosomal quality control deficits in Alzheimer's disease neurons

Aging is the most prominent risk factor for Alzheimers disease (AD). However, the cellular mechanisms linking neuronal proteostasis decline to the characteristic aberrant protein deposits in AD brains remain elusive. Here, we develop transdifferentiated neurons (tNeurons) from human dermal fibroblasts as a neuronal model that retains aging hallmarks and exhibits AD-linked vulnerabilities. Remarkably, AD tNeurons accumulate proteotoxic deposits, including phospho-Tau and A{beta}, resembling those in AD patient and APP mouse brains. Quantitative tNeuron proteomics identify aging and AD-linked deficits in proteostasis and organelle homeostasis, most notably in endosome-lysosomal components. Lysosomal deficits in aged tNeurons, including constitutive lysosomal damage and ESCRT-mediated lysosomal repair defects, are exacerbated in AD tNeurons and linked to inflammatory cytokine secretion and cell death. Supporting lysosomal deficits centrality in AD, compounds ameliorating lysosomal function reduce A{beta} deposits and cytokine secretion. Thus, the tNeuron model system reveals impaired lysosomal homeostasis as an early event of aging and AD.

cell biology↗