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Bateman, R. J.

Publications and source records attributed to Bateman, R. J..

12 recordsLinked to original sources

Distribution of big tau isoforms in the human central and peripheral nervous system

ObjectiveTau is widely studied in the field of neurodegenerative disease research, yet most work has focused on canonical brain tau isoforms. A longer isoform, "big tau," produced by inclusion of exon 4a, is expressed in the peripheral nervous system (PNS) and select central nervous system (CNS) regions. We sought to characterize big tau molecular composition, anatomical distribution, and relevance to neurodegenerative disease. MethodsMass spectrometry was used to sequence big tau and map its distribution across the human nervous system. Postmortem samples included brain tissue from Alzheimers disease (AD), amyotrophic lateral sclerosis (ALS), and controls; spinal cord from ALS and controls; and peripheral nerves. Big and canonical ("small") tau isoforms were also quantified in cerebrospinal fluid (CSF) from young controls and participants stratified by amyloid status and cognitive impairment. ResultsHuman big tau results from insertion of either 355 or 251 amino acids encoded by exon 4a-long and exon 4a-short, respectively. Alternative splicing of exons 2, 3, and 10 generates multiple big tau isoforms. Total tau levels were [~]1000-fold higher in brain than in the PNS; however, the relative abundance of big tau increased from the CNS to the PNS, comprising 50 % of the total tau in the periphery and exhibiting considerable regional heterogeneity in the brain ([~] 1 % of total tau). In CSF, big tau levels were unchanged by amyloid abnormalities or cognitive impairment, whereas canonical tau increased with AD-related pathology. InterpretationBig tau represents a distinct tau population enriched in the PNS and largely uncoupled from disease-associated changes in brain-derived tau, suggesting that distinguishing big tau from canonical tau may improve interpretation of tau biomarkers and help differentiate CNS neurodegeneration from peripheral nerve pathology.

neuroscience↗

Post-translational modifications distinguish amyloid-β isoform patterns extracted from vascular deposits and parenchymal plaques

Deposition of amyloid-{beta} (A{beta}) aggregates is a core pathological hallmark of both cerebral amyloid angiopathy (CAA) and extracellular parenchymal plaques in Alzheimers disease (AD). While both disease processes share progressive, decades-long deposition of fibrillar A{beta} peptide, they differ in isoform composition. We hypothesized that post-translational modifications (PTMs) on A{beta} would also differ between CAA and parenchymal plaques. Using Lys-N enzymatic digestion followed by quantitative mass spectrometry, we profiled A{beta} isoforms and N-terminus PTMs (aspartic acid isomerization and pyroglutamate formation) across CAA severity and compared them to parenchymal plaque A{beta} in AD. Moderate to severe CAA primarily featured intact N-terminus (A{beta}1-x) ([~]95%) with minimal N-truncated species (A{beta}2-x, A{beta}3pGlu-x, A{beta}4-x), whereas parenchymal plaques displayed diverse N-terminus truncations and PTMs. Increasing CAA severity correlated with a shift from longer, hydrophobic C-terminal isoforms (A{beta}41, A{beta}42, A{beta}43) to shorter, less hydrophobic C-terminal isoforms (A{beta}37, A{beta}38, A{beta}39, A{beta}40). Importantly, moderate and severe CAA displayed minimal isomerization of Asp-1 and Asp-7 residues, which correlated significantly (r > 0.9) with shorter C-terminal isoforms (A{beta}37, A{beta}38, A{beta}39, A{beta}40). These patterns suggest distinct A{beta} aggregation mechanisms in CAA versus parenchymal plaques. We propose that the intact N-terminus found in CAA with limited Asp isomerization is due to its inclusion within the protofibril structure (less disordered and inaccessible to PTMs), unlike the parenchymal plaques, where the N-terminus is more disordered and accessible to PTMs. These biochemical differences may reflect distinct protofibril architectures with potential implications for biomarker development for early CAA detection and therapeutic targeting of vascular and parenchymal A{beta}.

neuroscience↗

Increasing hub disruption parallels dementia severity in autosomal dominant Alzheimer disease

Hub regions in the brain, recognized for their roles in ensuring efficient information transfer, are vulnerable to pathological alterations in neurodegenerative conditions, including Alzheimer Disease (AD). Given their essential role in neural communication, disruptions to these hubs have profound implications for overall brain network integrity and functionality. Hub disruption, or targeted impairment of functional connectivity at the hubs, is recognized in AD patients. Computational models paired with evidence from animal experiments hint at a mechanistic explanation, suggesting that these hubs may be preferentially targeted in neurodegeneration, due to their high neuronal activity levels--a phenomenon termed "activity-dependent degeneration". Yet, two critical issues were unresolved. First, past research hasnt definitively shown whether hub regions face a higher likelihood of impairment (targeted attack) compared to other regions or if impairment likelihood is uniformly distributed (random attack). Second, human studies offering support for activity-dependent explanations remain scarce. We applied a refined hub disruption index to determine the presence of targeted attacks in AD. Furthermore, we explored potential evidence for activity-dependent degeneration by evaluating if hub vulnerability is better explained by global connectivity or connectivity variations across functional systems, as well as comparing its timing relative to amyloid beta deposition in the brain. Our unique cohort of participants with autosomal dominant Alzheimer Disease (ADAD) allowed us to probe into the preclinical stages of AD to determine the hub disruption timeline in relation to expected symptom emergence. Our findings reveal a hub disruption pattern in ADAD aligned with targeted attacks, detectable even in pre-clinical stages. Notably, the disruptions severity amplified alongside symptomatic progression. Moreover, since excessive local neuronal activity has been shown to increase amyloid deposition and high connectivity regions show high level of neuronal activity, our observation that hub disruption was primarily tied to regional differences in global connectivity and sequentially followed changes observed in A{beta} PET cortical markers is consistent with the activity-dependent degeneration model. Intriguingly, these disruptions were discernible 8 years before the expected age of symptom onset. Taken together, our findings not only align with the targeted attack on hubs model but also suggest that activity-dependent degeneration might be the cause of hub vulnerability. This deepened understanding could be instrumental in refining diagnostic techniques and developing targeted therapeutic strategies for AD in the future.

neuroscience↗

Endogenous recapitulation of Alzheimers disease neuropathology through human 3D direct neuronal reprogramming

Alzheimers disease (AD) is a neurodegenerative disorder that primarily affects elderly individuals, and is characterized by hallmark neuronal pathologies including extracellular amyloid-{beta} (A{beta}) plaque deposition, intracellular tau tangles, and neuronal death. However, recapitulating these age-associated neuronal pathologies in patient-derived neurons has remained a significant challenge, especially for late-onset AD (LOAD), the most common form of the disorder. Here, we applied the high efficiency microRNA-mediated direct neuronal reprogramming of fibroblasts from AD patients to generate cortical neurons in three-dimensional (3D) Matrigel and self-assembled neuronal spheroids. Our findings indicate that neurons and spheroids reprogrammed from both autosomal dominant AD (ADAD) and LOAD patients exhibited AD-like phenotypes linked to neurons, including extracellular A{beta} deposition, dystrophic neurites with hyperphosphorylated, K63-ubiquitin-positive, seed-competent tau, and spontaneous neuronal death in culture. Moreover, treatment with {beta}- or {gamma}-secretase inhibitors in LOAD patient-derived neurons and spheroids before A{beta} deposit formation significantly lowered A{beta} deposition, as well as tauopathy and neurodegeneration. However, the same treatment after the cells already formed A{beta} deposits only had a mild effect. Additionally, inhibiting the synthesis of age-associated retrotransposable elements (RTEs) by treating LOAD neurons and spheroids with the reverse transcriptase inhibitor, lamivudine, alleviated AD neuropathology. Overall, our results demonstrate that direct neuronal reprogramming of AD patient fibroblasts in a 3D environment can capture age-related neuropathology and reflect the interplay between A{beta} accumulation, tau dysregulation, and neuronal death. Moreover, miRNA-based 3D neuronal conversion provides a human-relevant AD model that can be used to identify compounds that can potentially ameliorate AD-associated pathologies and neurodegeneration.

neuroscience↗

Apolipoprotein E O-glycosylation is associated with amyloid plaques and APOE genotype.

Although the APOE {varepsilon}4 allele is the strongest genetic risk factor for sporadic Alzheimers disease (AD), the relationship between apolipoprotein (apoE) and AD pathophysiology is not yet fully understood. Relatively little is known about the apoE protein species, including post-translational modifications, that exist in the human periphery and CNS. To better understand these apoE species, we developed a LC-MS/MS assay that simultaneously quantifies both unmodified and O-glycosylated apoE peptides. The study cohort included 47 older individuals (age 75.6 {+/-} 5.7 years [mean {+/-} standard deviation]), including 23 individuals (49%) with cognitive impairment. Paired plasma and cerebrospinal fluid samples underwent analysis. We quantified O-glycosylation of two apoE protein residues - one in the hinge region and one in the C-terminal region - and found that glycosylation occupancy of the hinge region in the plasma was significantly correlated with plasma total apoE levels, APOE genotype and amyloid status as determined by CSF A{beta}42/A{beta}40. A model with plasma glycosylation occupancy, plasma total apoE concentration, and APOE genotype distinguished amyloid status with an AUROC of 0.89. These results suggest that plasma apoE glycosylation levels could be a marker of brain amyloidosis, and that apoE glycosylation may play a role in the pathophysiology of AD. HighlightsO_LISimultaneous quantification of unmodified and O-glycosylated apoE via LC-MS/MS. C_LIO_LITotal plasma apoE varies by APOE genotype in an isoform, dose-dependent fashion. C_LIO_LICNS-derived apoE is more extensively O-glycosylated than peripherally derived apoE. C_LIO_LIHinge region glycosylation occupancy of plasma apoE is associated with amyloidosis. C_LI

biochemistry↗

Systematic characterization of brain cellular crosstalk signaling networks in Alzheimer's disease reveals a novel role for SEMA6D in TREM2-dependent microglial activation

Cellular crosstalk, mediated by membrane receptors and their ligands, is crucial for brain homeostasis and can contribute to neurodegenerative diseases such as Alzheimers disease (AD). To discover crosstalk dysregulations in AD, we reconstructed crosstalk networks from single-nucleus transcriptional profiles from 67 clinically and neuropathologically well-characterized controls and AD brain donors. We predicted a significant role for TREM2 and additional AD risk genes mediating neuron-microglia crosstalk in AD. The gene sub-network mediating SEMA6D-TREM2 crosstalk is activated near A{beta} plaques and SEMA6D-expressing cells and is disrupted in late AD stages. Using CRISPR-modified human induced pluripotent stem cell-derived microglia, we demonstrated that SEMA6D induces microglial activation in a TREM2-dependent manner. In summary, we demonstrate that characterizing cellular crosstalk networks can yield novel insights into AD biology. One Sentence SummaryWe investigate cell-to-cell communication in Alzheimers disease to characterize disease biology and suggest new avenues for therapeutic intervention.

neuroscience↗

Spontaneous Isomerization of Asp387 in Tau is Diagnostic for Alzheimer's Disease: An Endogenous Indicator of Reduced Autophagic Flux

Amino acid isomerization is a spontaneous chemical modification potentially related to the underlying causes of Alzheimers disease (AD). We demonstrate that data-independent acquisition mass spectrometry can be used to characterize isomerization in complex protein mixtures. Examination of a large cohort of brain tissue samples revealed a striking relationship between isomerization of tau and AD status. Surprisingly, isomerization was found to be more abundant in both autosomal dominant and sporadic AD samples relative to controls. We hypothesize that lower autophagic flux in AD brains accounts for these results. Additional data, including quantitative analysis of proteins related to autophagy, strongly support this hypothesis. For example, isomerization of tau is positively correlated with levels of p62, a recognized indicator of autophagic inhibition. In sum, the data suggest strong ties between isomerization and autophagic flux, which may therefore represent a promising target for future investigations into the therapy and prevention of AD.

neuroscience↗

Functional brain age prediction suggests accelerated aging in preclinical familial Alzheimer's disease, irrespective of fibrillar amyloid-beta pathology

We aimed at developing a model able to predict brain aging from resting state functional connectivity (rs-fMRI) and assessing whether genetic risk/determinants of Alzheimers disease (AD) and amyloid (A{beta}) pathology contributes to accelerated brain aging. Using data collected in 1340 cognitively unimpaired participants from 18 to 94 years old selected across multi-site cohorts, we showed that chronological age can be predicted across the whole lifespan from topological properties of graphs constructed from rs-fMRI. We subsequently used the difference between the model-predicted age and the chronological age in pre-symptomatic autosomal dominant AD (ADAD) mutation carriers and asymptomatic individuals at risk of sporadic AD and assessed the influence of genetics and A{beta} pathology on brain age. Applying our predictive model in the context of preclinical AD revealed that the pre-symptomatic phase of ADAD is characterized by accelerated functional brain aging. This phenomenon is independent from, and might precede, detectable fibrillar A{beta} deposition.

neuroscience↗

Genetic variants associated with Alzheimer's disease confer different cerebral cortex cell-type population structure

Alzheimers disease (AD) is characterized by neuronal loss and astrocytosis in the cerebral cortex. However, the effects of brain cellular composition are often ignored in high-throughput molecular studies. We developed and optimized a cell-type specific expression reference panel and employed digital deconvolution methods to determine brain cellular distribution in three independent transcriptomic studies. We found that neuronal and astrocyte proportions differ between healthy and diseased brains and also among AD cases that carry specific genetic risk variants. Brain carriers of pathogenic mutations in APP, PSEN1 or PSEN2 presented lower neurons and higher astrocytes proportions compared to sporadic AD. Similarly, the APOE {varepsilon}4 allele also showed decreased neurons and increased astrocytes compared to AD non-carriers. On the contrary, carriers of variants in TREM2 risk showed a lower degree of neuronal loss than matched AD cases in multiple independent studies. These findings suggest that genetic risk factors associated with AD etiology have a specific imprinting in the cellular composition of AD brains. Our digital deconvolution reference panel provides an enhanced understanding of the fundamental molecular mechanisms underlying neurodegeneration, enabling the analysis of large bulk RNA-seq studies for cell composition, and suggests that correcting for the cellular structure when performing transcriptomic analysis will lead to novel insights of AD.

genetics↗

Data-driven models of dominantly-inherited Alzheimer’s disease progression

Dominantly-inherited Alzheimers disease is widely hoped to hold the key to developing interventions for sporadic late onset Alzheimers disease. We use emerging techniques in generative data-driven disease-progression modelling to characterise dominantly-inherited Alzheimers disease progression with unprecedented resolution, and without relying upon familial estimates of years until symptom onset (EYO). We retrospectively analysed biomarker data from the sixth data freeze of the Dominantly Inherited Alzheimer Network observational study, including measures of amyloid proteins and neurofibrillary tangles in the brain, regional brain volumes and cortical thicknesses, brain glucose hypometabolism, and cognitive performance from the Mini-Mental State Examination (all adjusted for age, years of education, sex, and head size, as appropriate). Data included 338 participants with known mutation status (211 mutation carriers: 163 PSEN1; 17 PSEN2; and 31 APP) and a baseline visit (age 19-66; up to four visits each, 1{middle dot}1 {+/-} 1{middle dot}9 years in duration; spanning 30 years before, to 21 years after, parental age of symptom onset). We used an event-based model to estimate sequences of biomarker changes from baseline data across disease subtypes (mutation groups), and a differential-equation model to estimate biomarker trajectories from longitudinal data (up to 66 mutation carriers, all subtypes combined). The two models concur that biomarker abnormality proceeds as follows: amyloid deposition in cortical then sub-cortical regions (approximately 24{+/-}11 years before onset); CSF p-tau (17{+/-}8 years), tau and A{beta}42 changes; neurodegeneration first in the putamen and nucleus accumbens (up to 6 {+/-} 2 years); then cognitive decline (7 {+/-} 6 years), cerebral hypometabolism (4 {+/-} 4 years), and further regional neurodegeneration. Our models predicted symptom onset more accurately than EYO: root-mean-squared error of 1{middle dot}35 years versus 5{middle dot}54 years. The models reveal hidden detail on dominantly-inherited Alzheimers disease progression, as well as providing data-driven systems for fine-grained patient staging and prediction of symptom onset with great potential utility in clinical trials.

neuroscience↗

Tau hyperphosphorylation on T217 in cerebrospinal fluid is specifically associated to amyloid-β pathology

IntroductionModification of CSF tau phosphorylation in AD remains controversial since total-tau and phospho-tau levels measured by immunoassays are highly correlated.\n\nMethodsStoichiometry of phosphorylation of CSF tau was monitored on five sites by mass spectrometry. We compared 50 participants with AD at mild to moderate stages, others tauopathies and controls then confirmed our results in a cohort of 86 participants cognitively normal or with mild cognitive impairment and stratified according to amyloid-{beta} status.\n\nResultsChanges in tau phosphorylation rates were observed in AD participants but not in other tauopathies. T181 appeared slightly hyperphosphorylated in AD. In comparison, T217 phosphorylation, was considerably modified. We demonstrated T217 hyperphosphorylation occurred systematically in amyloid positive participants even at preclinical stage (AUC 0.999). T217 phosphorylation change specificity overpasses other phosphorylated tau sites investigated in this study, but also CSF total-tau and p-tau levels.\n\nDiscussionCSF T217 hyperphosphorylation defines a specific tauopathy status concomitant with {beta}-amyloidosis.

neuroscience↗

Polygenic Risk Score of Sporadic Late Onset Alzheimer Disease Reveals a Shared Architecture with the Familial and Early Onset Forms

ObjectiveTo determine whether the genetic architecture of sporadic late-onset Alzheimers Disease (sLOAD) has an effect on familial late-onset AD (fLOAD), sporadic early-onset (sEOAD) and autosomal dominant early-onset (eADAD).\n\nMethodsPolygenic risk scores (PRS) were constructed using previously identified 21 genome-wide significant loci for LOAD risk.\n\nResultsWe found that there is an overlap in the genetic architecture among sEOAD, fLOAD, and sLOAD. sEOAD showed the highest odds for the PRS (OR=2.27; p=1.29x10-7), followed by fLOAD (OR=1.75; p=1.12x10-7) and sLOAD (OR=1.40; p=1.21x10-3). PRS is associated with cerebrospinal fluid ptau181-A{beta}42 on eADAD.\n\nConclusionOur analysis confirms that the genetic factors identified for sLOAD also modulate risk in fLOAD and sEOAD cohorts. Furthermore, our results suggest that the burden of these risk variants is associated with familial clustering and earlier-onset of AD. Although these variants are not associated with risk in the eADAD, they may be modulating age at onset.

genetics↗