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Synapses, Microglia, and Lipids in Alzheimer's Disease

FRONTIERS IN NEUROSCIENCE (2022)

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Review Clinical Neurology

Alzheimer's Disease Genetics: A Dampened Microglial Response?

Zena K. Chatila et al.

Summary: Alzheimer's disease is an age-related neurodegenerative condition, and microglia cells have been found to play a central role in its pathogenesis. Genetic studies have identified dysfunctional microglial pathways associated with genetic risk factors for AD. These findings provide potential therapeutic targets for intervention.

NEUROSCIENTIST (2023)

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Article Clinical Neurology

Diverse human astrocyte and microglial transcriptional responses to Alzheimer's pathology

Amy M. Smith et al.

Summary: The study reveals significant differences in gene expression in astrocytes and microglia in the brains of AD patients, correlated with amyloid-beta or pTau expression. There are distinct gene expression patterns in the two cell types and pathologies, but common gene sets exist in each cell type. Additionally, different sub-clusters are found in astrocytes and microglia, characterized by transcriptional signatures related to either homeostatic functions or disease pathology.

ACTA NEUROPATHOLOGICA (2022)

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Article Neurosciences

C1q and SRPX2 regulate microglia mediated synapse elimination during early development in the visual thalamus but not the visual cortex

Qifei Cong et al.

Summary: The study reveals that the classical complement pathway regulates microglia-mediated synapse elimination in the visual thalamus but does not affect the primary visual cortex during early development of the central nervous system.

GLIA (2022)

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Article Neurosciences

Microglia-specific ApoE knock-out does not alter Alzheimer's disease plaque pathogenesis or gene expression

Caden M. Henningfield et al.

Summary: Previous studies indicate that microglial-expressed ApoE may not be necessary for plaque formation in Alzheimer's disease. However, it may play a role in plaque homeostasis in disease and synaptic maintenance under normal conditions.

GLIA (2022)

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Article Neurosciences

Microglia contribute to the propagation of Aβ into unaffected brain tissue

Paolo d'Errico et al.

Summary: This study demonstrates that Aβ can enter and deposit within wild-type grafts via microglia, identifying microglia as carriers of Aβ deposition into previously unaffected brain tissue, thus supporting a previously unexplored mechanism of Aβ propagation.

NATURE NEUROSCIENCE (2022)

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Review Cell Biology

Pathological mechanisms and therapeutic strategies for Alzheimer's disease

Yaojun Ju et al.

Summary: Alzheimer's disease is a complex neurodegenerative disease characterized by synaptic dysfunctions and neurotransmitter deficiencies. The pathological features of Alzheimer's disease include changes in β-amyloid and tau proteins. Aging and other factors are also risk factors for the disease. Therefore, developing treatment strategies that target different pathological factors is crucial.

NEURAL REGENERATION RESEARCH (2022)

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Review Cell Biology

Role of Microglia in Regulating Cholesterol and Tau Pathology in Alzheimer's Disease

Shwetha Nanjundaiah et al.

Summary: Cholesterol, a crucial component of the cell membrane, plays a significant role in the brain by influencing synaptic transmission, neuronal signaling, and neurodegenerative diseases. Dysregulation of cholesterol trafficking is linked to increased production of hyperphosphorylated Tau and Amyloid-beta protein, leading to Alzheimer's disease. Understanding the regulation of cholesterol metabolism and Tau phosphorylation is essential for managing the pathogenesis of Alzheimer's disease.

CELLULAR AND MOLECULAR NEUROBIOLOGY (2021)

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Article Clinical Neurology

Hypothesis: Tau pathology is an initiating factor in sporadic Alzheimer's disease

Amy F. T. Arnsten et al.

Summary: The etiology of common, sporadic Alzheimer's disease is unknown. The hypothesis proposed here suggests that tau pathology within specific projection neurons in susceptible microenvironments may initiate sAD, supported by data showing tau pathology appearing a decade before A beta plaques and targeting glutamate projection neurons.

ALZHEIMERS & DEMENTIA (2021)

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Article Biochemistry & Molecular Biology

Cholesterol in Membranes Facilitates Aggregation of Amyloid β Protein at Physiologically Relevant Concentrations

Siddhartha Banerjee et al.

Summary: The presence of cholesterol in lipid bilayers significantly enhances the aggregation process of Aβ42 at low concentrations, indicating that the lipid composition plays a crucial role in controlling the self-assembly of Aβ oligomers in cellular membranes.

ACS CHEMICAL NEUROSCIENCE (2021)

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Article Clinical Neurology

Reactive or transgenic increase in microglial TYROBP reveals a TREM2-independent TYROBP-APOE link in wild-type and Alzheimer's-related mice

Mickael Audrain et al.

Summary: The research shows that TYROBP-APOE signaling does not require TREM2 and may be an initiating step in establishing the disease-associated microglia (DAM) phenotype.

ALZHEIMERS & DEMENTIA (2021)

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Review Pharmacology & Pharmacy

Roles of microglia in Alzheimer's disease and impact of new findings on microglial heterogeneity as a target for therapeutic intervention

Kazuyuki Takata et al.

Summary: Microglia are specialized macrophages in the central nervous system that play key roles in brain immunity, development, and homeostasis. Recent advances in single-cell and single-nucleus transcriptomic technologies have revealed the heterogeneity of microglia and their involvement in brain pathologies, including Alzheimer's disease. Understanding microglial biology at the single-cell level may lead to new therapeutic targets for treating neuroinflammatory conditions like AD.

BIOCHEMICAL PHARMACOLOGY (2021)

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Review Biochemistry & Molecular Biology

Changing Functional Signatures of Microglia along the Axis of Brain Aging

Bianca Brawek et al.

Summary: Microglia, the innate immune cells of the brain, exhibit unique morphology and physiology, adapting well to their microenvironment and becoming legitimate members of the cellular brain architecture. As the brain ages, changes in the microglial microenvironment impact their functional properties, triggering further rounds of adaptation. This review discusses recent data showing how microglial functional properties adapt to age-related changes in brain parenchyma in a sex-specific manner, with a focus on early changes occurring at middle age and strategies counteracting their aging.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Biochemistry & Molecular Biology

Microglial circadian clock regulation of microglial structural complexity, dendritic spine density and inflammatory response

Hiroshi Nakanishi et al.

Summary: Microglia in the cortex exhibit different shapes and functions during wakefulness and sleep, with their molecular circadian clock playing a key role in regulating these processes. Disruption of the microglial clock system could lead to sleep disturbances, impaired social interaction, and cognitive impairment, potentially contributing to the pathogenesis of neurodegenerative disorders such as Alzheimer's disease. Understanding and targeting the microglial circadian molecular clock may offer insights for developing novel pharmacological interventions for neuropsychiatric and neurodegenerative disorders.

NEUROCHEMISTRY INTERNATIONAL (2021)

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Article Multidisciplinary Sciences

Molecular subtyping of Alzheimer's disease using RNA sequencing data reveals novel mechanisms and targets

Ryan A. Neff et al.

Summary: This study identified three major molecular subtypes of Alzheimer's disease (AD) and specific driver genes through analyzing transcriptomes from multiple brain regions. The research also demonstrated that existing AD mouse models reflect some degree of subtype heterogeneity, possibly explaining the lack of alignment between successful drugs in specific mouse models and generalized human trials across all AD subtypes. Subtyping patients with AD is considered a critical step towards precision medicine for this devastating disease.

SCIENCE ADVANCES (2021)

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Article Clinical Neurology

Distinct amyloid-β and tau-associated microglia profiles in Alzheimer's disease

Emma Gerrits et al.

Summary: This study conducted single-nuclei RNA sequencing on Alzheimer's disease (AD)-related human microglia, revealing two distinct expression profiles associated with pathology. These findings shed light on the role of microglia in AD and offer new targets for microglia-specific therapeutic strategies.

ACTA NEUROPATHOLOGICA (2021)

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Article Clinical Neurology

Concomitant neurodegenerative pathologies contribute to the transition from mild cognitive impairment to dementia

Kirsty E. McAleese et al.

Summary: The aged brain often exhibits multiple pathologies, rather than a single pathology, and the presence of multiple pathologies can significantly worsen cognitive decline, increasing the risk of transitioning from mild cognitive impairment to dementia.

ALZHEIMERS & DEMENTIA (2021)

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Article Multidisciplinary Sciences

Neurotoxic reactive astrocytes induce cell death via saturated lipids

Kevin A. Guttenplan et al.

Summary: Astrocytes respond to diseases and injuries in the central nervous system by releasing long-chain saturated fatty acids contained in lipoparticles, leading to the death of neurons and mature oligodendrocytes. The elimination of saturated lipids produced by astrocytes can mitigate astrocyte-induced toxicity, suggesting a mechanism by which astrocytes kill cells in the central nervous system.

NATURE (2021)

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Review Biochemistry & Molecular Biology

Targeting Microglia-Synapse Interactions in Alzheimer's Disease

Gaia Piccioni et al.

Summary: This review focuses on the emerging roles of microglia in the brain, particularly in synaptic plasticity in health and disease. Evidence suggests that maintaining the ramified state of microglia is crucial for normal synaptic plasticity and cognitive function. Inflammatory signals associated with diseases like Alzheimer's can alter the morphology of microglia and lead to synaptic loss and cognitive impairment, highlighting potential targets for disease-modifying therapy.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Ground state depletion microscopy as a tool for studying microglia-synapse interactions

Patrick Jarmo Paasila et al.

Summary: The study successfully applied GSDIM technology to human brain tissue sections as well as samples from mouse and zebrafish larvae, achieving high-resolution molecular imaging and providing clearer insights into the interactions between microglia cells and synapses.

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Distinct microglial profiles associated with amyloid and tau pathology in Alzheimer disease

Sarah Lemprière

Nature Reviews Neurology (2021)

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Trem2 restrains the enhancement of tau accumulation and neurodegeneration by β-amyloid pathology

Seung-Hye Lee et al.

Summary: Loss-of-function TREM2 mutations increase Alzheimer's disease risk. TREM2 deletion has protective functions in beta-amyloid and tau pathologies; in the presence of beta-amyloid pathology, Trem2 deletion exacerbates tau accumulation and spreading, promoting neurodegeneration. TREM2 may slow AD progression and reduce tau-driven neurodegeneration by limiting beta-amyloid's facilitation of pathogenic tau spreading.

NEURON (2021)

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Article Multidisciplinary Sciences

Defining early changes in Alzheimer's disease from RNA sequencing of brain regions differentially affected by pathology

Boris Guennewig et al.

Summary: Tau pathology in Alzheimer's disease follows a predictable pattern corresponding to disease symptoms and severity. Comparing molecular signatures in differentially affected areas may help in modelling disease progression. RNA sequencing in AD brains showed similarities in transcriptomic signatures between mildly and moderately affected regions, with broader abnormalities in the latter due to greater tau load. Both regions exhibited upregulation of immune-related genes, with additional changes in vesicle secretion and neuronal markers in the moderately affected precuneus. Early AD transcriptome is characterized by perturbations in synaptic vesicle secretion and neuroimmune dysfunction.

SCIENTIFIC REPORTS (2021)

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Article Biology

Microglial trogocytosis and the complement system regulate axonal pruning in vivo

Tony K. Y. Lim et al.

Summary: This study directly observed axon trogocytosis by microglia in the developing Xenopus laevis retinotectal circuit, demonstrating the important role of microglia in regulating pruning of retinal ganglion cell axons. It was found that neurons can control this process through expression of complement inhibitory proteins, suggesting that microglia remodel axons via trogocytosis.

ELIFE (2021)

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Article Neurosciences

Plaque associated microglia hyper-secrete extracellular vesicles and accelerate tau propagation in a humanized APP mouse model

Kevin Clayton et al.

Summary: Our findings suggest that MGnD microglia hyper-secrete p-tau(+) EVs while compacting A beta plaques and clearing NP tau, which we propose as a novel mechanistic link between amyloid plaque deposition and exacerbation of tau propagation in App(NL-G-F) mice.

MOLECULAR NEURODEGENERATION (2021)

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Editorial Material Neurosciences

Loss of TREM2 facilitates tau accumulation, spreading, and brain atrophy, but only in the presence of amyloid pathology

Christian Haass

Summary: The study demonstrates that TREM2-dependent microglial functions can prevent the accumulation and spreading of tau protein, but only in the presence of amyloid pathology. This provides further support for the amyloid cascade hypothesis and validates the protective function of microglia.

NEURON (2021)

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Review Geriatrics & Gerontology

Genetic Variability in Molecular Pathways Implicated in Alzheimer's Disease: A Comprehensive Review

David Vogrinc et al.

Summary: Alzheimer's disease is a neurodegenerative disease that affects a significant portion of the elderly population, leading to a major burden on the healthcare system due to rapid aging of the population. Despite the lack of effective drug treatment, genetic studies have identified numerous genes associated with increased risk of AD. This information may help in identifying novel molecular targets for the development of tailored and personalized treatments for Alzheimer's disease.

FRONTIERS IN AGING NEUROSCIENCE (2021)

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Article Biology

Microbiota-derived short chain fatty acids modulate microglia and promote Aβ plaque deposition

Alessio Vittorio Colombo et al.

Summary: Microbiota-derived SCFA play a critical role in promoting A beta deposition in Alzheimer's disease by modulating the microglial phenotype along the gut-brain axis.

ELIFE (2021)

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Article Neurosciences

Microglia, synaptic dynamics and forgetting

Chao Wang et al.

Summary: Microglia play a crucial role in regulating synaptic dynamics, impacting memory and forgetting, especially under pathological conditions. Uncovering their mechanisms not only helps understand the physiological functions of microglia in the brain, but also provides new strategies for preventing and treating memory impairment.

BRAIN RESEARCH BULLETIN (2021)

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Article Biology

Multi-scale modeling for systematically understanding the key roles of microglia in AD development

Zhiwei Ji et al.

Summary: Alzheimer's disease is the leading cause of age-related dementia, affecting over 5 million people in the United States. Current therapies are largely palliative and multiple potential drug candidates have failed in late-stage clinical trials. Studies suggest that microglia-mediated neuroinflammation may be responsible for therapy failures and play a crucial role in the development of AD, but the specific activation profile and phenotypic changes of microglia are poorly understood.

COMPUTERS IN BIOLOGY AND MEDICINE (2021)

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TREM2-dependent lipid droplet biogenesis in phagocytes is required for remyelination

Garyfallia Gouna et al.

Summary: Microglia play a key role in promoting myelin repair after demyelinating injury, with cholesterol esterification being essential for myelin debris clearance and lipid droplet generation. TREM2 is crucial for adapting to excess cholesterol exposure and regulating lipid droplet formation, ultimately impacting the innate immune response and remyelination.

JOURNAL OF EXPERIMENTAL MEDICINE (2021)

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Review Immunology

Microglia in Alzheimer's disease at single-cell level. Are there common in humans and mice?

Yun Chen et al.

Summary: Alzheimer's disease is characterized by the activation of microglia in response to amyloid beta peptides and tau aggregates, leading to the conversion of homeostatic microglia into disease-associated microglia. Different populations of reactive microglia have been identified, suggesting that microglia play a critical role in disease progression. Further research into the impact of microglia in AD pathogenesis is needed to better understand the parallels and discrepancies between human and mouse models.

JOURNAL OF EXPERIMENTAL MEDICINE (2021)

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Article Cell Biology

Role of glial cells in the generation of sex differences in neurodegenerative diseases and brain aging

Julie A. Chowen et al.

Summary: Diseases and changes in the nervous system related to aging often exhibit sex-specific characteristics, with glial cells playing a major role in the endogenous response of neural tissue. The sex-specific response of glial cells is influenced by sex chromosome genes, gonadal hormones, and neuroactive steroid hormone metabolites. This response may be crucial in understanding and potentially treating sex differences in pathological alterations of the nervous system.

MECHANISMS OF AGEING AND DEVELOPMENT (2021)

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Plaque-associated human microglia accumulate lipid droplets in a chimeric model of Alzheimer's disease

Christel Claes et al.

Summary: The study found that lipid droplet accumulation occurs in human DAM xMGs in Alzheimer's disease, but is reduced in TREM2-R47H DAM xMGs, as it is caused by TREM2-mediated changes in plaque proximity and reactivity.

MOLECULAR NEURODEGENERATION (2021)

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Article Biochemistry & Molecular Biology

The acute phase protein lactoferrin is a key feature of Alzheimer's disease and predictor of A beta burden through induction of APP amyloidogenic processing

Andrew Tsatsanis et al.

Summary: Amyloidogenic processing of the amyloid precursor protein leads to the formation of amyloid-beta peptide plaques in Alzheimer's disease. Early cortical changes in AD also involve neuroinflammation and elevated iron levels. The activation of the innate immune system in the brain is a neuroprotective response to infection, but persistent neuroinflammation is linked to AD neuropathology through unknown mechanisms.

MOLECULAR PSYCHIATRY (2021)

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Astrocytic interleukin-3 programs microglia and limits Alzheimer's disease

Cameron S. McAlpine et al.

Summary: Communication within the glial cell ecosystem is essential for neuronal and brain health. This study demonstrates that astrocyte-sourced interleukin-3 programs microglia to ameliorate the pathology of Alzheimer's disease by enhancing their ability to clear aggregates of beta-amyloid and tau, ultimately restricting disease progression and cognitive decline. These findings highlight IL-3 as a key mediator of astrocyte-microglia cross-talk and a potential therapeutic target for Alzheimer's disease.

NATURE (2021)

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Microglial activation and tau propagate jointly across Braak stages

Tharick A. Pascoal et al.

Summary: The study found a correlation between microglial activation and tau accumulation in patients with Alzheimer's disease, following a Braak-like pattern. The co-occurrence of A β, tau, and microglial abnormalities was identified as the strongest predictor of cognitive impairment in the study population.

NATURE MEDICINE (2021)

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A large-scale nanoscopy and biochemistry analysis of postsynaptic dendritic spines

Martin S. Helm et al.

Summary: Dendritic spines can be classified into mushroom-like and stubby shapes, which exhibit similar average protein copy numbers and topologies but differ in their correlation to synaptic strength. Stubby spines are less likely to respond adequately to dynamic changes in synaptic transmission compared to mushroom spines, possibly leading to their disappearance during brain maturation. This study provides a molecular view of dendritic spines through electron microscopy, quantitative biochemistry, super-resolution microscopy, and 3D molecular visualizations.

NATURE NEUROSCIENCE (2021)

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Overexpressing low-density lipoprotein receptor reduces tau-associated neurodegeneration in relation to apoE-linked mechanisms

Yang Shi et al.

Summary: Overexpressing the LDLR metabolic receptor in P301S tauopathy mice reduces brain apoE levels and improves tau pathology and neurodegeneration. This leads to enhanced catabolism in microglial immunometabolism and preservation of myelin integrity under neurodegenerative conditions. Additionally, LDLR-overexpressing mice show less reactive astrocyte activation in tauopathy.

NEURON (2021)

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ApoE and immunity in Alzheimer's disease and related tauopathies: Low-density lipoprotein receptor to the rescue

Andrew S. Mendiola et al.

Summary: The study in Neuron shows a protective role for LDLR in tau pathology, with brain overexpression of LDLR reducing apoE levels, suppressing microglial activation, preserving myelin, and ameliorating neurodegeneration, suggesting potential new therapies.

NEURON (2021)

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Autophagy deficiency modulates microglial lipid homeostasis and aggravates tau pathology and spreading

Yin Xu et al.

Summary: Studies indicate that microglial-specific autophagy, represented by Atg7, plays a crucial role in regulating lipid metabolism and neuroinflammation. Deletion of Atg7 in microglia leads to a proinflammatory status and exacerbates intraneuronal tau pathology.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2021)

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Microglial morphology in Alzheimer's disease and after Aβ immunotherapy

Diana K. Franco-Bocanegra et al.

Summary: The study found that reactive/amoeboid microglia are the most common type in the aged human brain, Alzheimer's disease does not affect the number of microglia but decreases ramified microglia, and immunotherapy can increase ramified microglia.

SCIENTIFIC REPORTS (2021)

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Plasma lipidome is dysregulated in Alzheimer's disease and is associated with disease risk genes

Yue Liu et al.

Summary: Lipidomics research in Alzheimer's disease identifies specific lipid species that are dysregulated in AD patients and may aid in distinguishing them from healthy controls. Certain lipid classes, such as sphingomyelins, cholesterol esters, and triglycerides, show good classification accuracy in relation to AD. Furthermore, the study reveals associations between plasma lipid profiles and genetic risk factors for AD, shedding light on the pathobiology of the disease.

TRANSLATIONAL PSYCHIATRY (2021)

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Argyro Thalia Delizannis et al.

Summary: The study highlights the complex interplay between microglia, tau pathology, and A beta plaques in the context of Alzheimer's disease. It suggests that microglial function and gene expression, particularly related to TREM2, play crucial roles in the progression of the disease. The findings indicate that targeting microglial depletion and gene variations may offer new therapeutic strategies for AD.

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Abnormal brain cholesterol homeostasis in Alzheimer's disease-a targeted metabolomic and transcriptomic study

Vijay R. Varma et al.

Summary: The study reveals abnormalities in brain cholesterol biosynthesis and catabolism in patients with AD, leading to unstable cholesterol levels and accumulation of cytotoxic oxidized sterols. These changes were not observed in patients with Parkinson's disease, suggesting a specificity to AD.

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ANNUAL REVIEW OF NEUROSCIENCE, VOL 35 (2012)

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Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model

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Soluble protein oligomers in neurodegeneration:: lessons from the Alzheimer's amyloid β-peptide

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Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment

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ATP mediates rapid microglial response to local brain injury in vivo

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Intrathecal inflammation precedes development of Alzheimer's disease

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Iba1 is an actin-cross-linking protein in macrophages/microglia

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Two distal downstream enhancers direct expression of the human apolipoprotein E gene to astrocytes in the brain

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Cell death or synaptic loss in Alzheimer disease

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Sequence of Aβ-protein deposition in the human medial temporal lobe

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