Cited by 1,047Neuroinflammation and Neurodegeneration MechanismsNeurological Disease Mechanisms and TreatmentsInflammasome and immune disorders

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Microglial Activation and Chronic Neurodegeneration

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Lull, Melinda E., Block, Michelle L.·2010·Neurotherapeutics

DOI 10.1016/j.nurt.2010.05.014PMC PMC2951017

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Abstract

Microglia, the resident innate immune cells in the brain, have long been implicated in the pathology of neurodegenerative diseases. Accumulating evidence points to activated microglia as a chronic source of multiple neurotoxic factors, including tumor necrosis factor-α, nitric oxide, interleukin-1β, and reactive oxygen species (ROS), driving progressive neuron damage. Microglia can become chronically activated by either a single stimulus (e.g., lipopolysaccharide or neuron damage) or multiple stimuli exposures to result in cumulative neuronal loss with time. Although the mechanisms driving these phenomena are just beginning to be understood, reactive microgliosis (the microglial response to neuron damage) and ROS have been implicated as key mechanisms of chronic and neurotoxic microglial activation, particularly in the case of Parkinson's disease. We review the mechanisms of neurotoxicity associated with chronic microglial activation and discuss the role of neuronal death and microglial ROS driving the chronic and toxic microglial phenotype.

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BackgroundInfluential
Microglial TIR-domain-containing adapter-inducing interferon-β (TRIF) deficiency promotes retinal ganglion cell survival and axon regeneration via nuclear factor-κB
Lin, S., Liang, Y., Zhang, J., Bian, C., Zhou, H., Guo, Q., Xiong, Y., Li, S., & Su, B. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-39 · Cited by 39
“Several lines of evidence suggest that upstream of the pro-inflammatory release, the microglial innate immunological responses are involved in microglial activation [44,45].”
Background
Reduction of the RNA Binding Protein TIA1 Exacerbates Neuroinflammation in Tauopathy
LeBlang, C. J., Medalla, M., Nicoletti, N. W., Hays, E. C., Zhao, J., Shattuck, J. E., Cruz, A. L., Wolozin, B. L., & Luebke, J. I. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00285 · Cited by 38
“…pathology in neurodegenerative diseases, including tauopathies such as Alzheimer’s Disease (AD) and Frontotemporal dementia (reviews: Mrak and Griﬃn, 2005; Block et al., 2007; Lull and Block, 2010; Perry et al., 2010; Cunningham, 2013; Laurent et al., 2018; Ransohoﬀ and El Khoury, 2019).”
p38α Mitogen-Activated Protein Kinase—An Emerging Drug Target for the Treatment of Alzheimer’s Disease
Detka, J., Płachtij, N., Strzelec, M., Manik, A., & Sałat, K. (2024) · Molecules · doi:10.3390/molecules29184354 · Cited by 40
“They do so by changing their phenotype, which causes a shift in their functions [72]—in normal conditions, they exhibit a phagocytic function in removing damaged neurons, but in the activated state they show a secretory role [73].”
Background
Beneficial effects of liraglutide (GLP1 analog) in the hippocampal inflammation
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“The numerical density per area (NA) of immunoreactive cells was estimated by counting the number of marked cells (N) in four slides per animal (n = 5 animals/group): NA = N / AT (Mandarim-de-Lacerda et al. 2010).”
Method
Cigarette Smoke Exposure Induces Neurocognitive Impairments and Neuropathological Changes in the Hippocampus
Dobric, A., Luca, S. N. D., Seow, H. J., Wang, H., Brassington, K., Chan, S. M. H., Mou, K., Erlich, J. R., Liong, S., Selemidis, S., et al. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.893083 · Cited by 37
Tau aggregates improve the Purinergic receptor P2Y12-associated podosome rearrangements in microglial cells
Chinnathambi, S., Das, R. R., & Desale, S. E. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2023.119477 · Cited by 37
A single intranasal dose of human mesenchymal stem cell-derived extracellular vesicles after traumatic brain injury eases neurogenesis decline, synapse loss, and BDNF-ERK-CREB signaling
Kodali, M., Madhu, L. N., Reger, R. L., Milutinovic, B. S., Upadhya, R., Attaluri, S., Shuai, B., Shankar, G., & Shetty, A. K. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1185883 · Cited by 39
“Moreover, persistent microglial activation interferes with brain tissue repair and promotes neurodegeneration (Lull and Block, 2010; Gyengesi et al., 2019).”
Background
T1AM/TAAR1 System Reduces Inflammatory Response and β-Amyloid Toxicity in Human Microglial HMC3 Cell Line
Polini, B., Ricardi, C., Bertolini, A., Carnicelli, V., Rutigliano, G., Saponaro, F., Zucchi, R., & Chiellini, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411569 · Cited by 37
“Since chronic inflammatory activation of microglia is correlated with common NDDs, functional modulation of microglial phenotypes could represent a valid therapeutic strategy [10,12,13].”
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“…oxygen species (ROS) and reactive nitrogen species (RNS), cause disruptions in neurogenesis, neuronal excitability, synaptic transmission, synaptic plasticity and neuronal survival 5-7 , disturbances which have been implicated in the development and progression of neuropsychiatric disorders 8 .”
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Tmem30a deficiency leads to retinal rod bipolar cell degeneration
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Neuroinflammatory responses in Parkinson’s disease: relevance of Ibuprofen in therapeutics
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Purpurogallin exerts anti-inflammatory effects in lipopolysaccharide-stimulated BV2 microglial cells through the inactivation of the NF-κB and MAPK signaling pathways
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Chronic Traumatic Encephalopathy: Is Latency in Symptom Onset Explained by Tau Propagation?Preprint
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Comparison of sirtuin 3 levels in ALS and Huntington's disease-differential effects in human tissue samples vs. transgenic mouse models
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“When comparing cell culture data, one has to additionally take into account that the prevalence of the different cell types changes during tissue inflammation (Lull and Block, 2010).”
Background
Minimally Toxic Dose of Lipopolysaccharide and α-Synuclein Oligomer Elicit Synergistic Dopaminergic Neurodegeneration: Role and Mechanism of Microglial NOX2 Activation
Zhang, W., Gao, J.-H., Yan, Z.-F., Huang, X.-Y., Guo, P., Sun, L., Liu, Z., Hu, Y., Zuo, L.-J., Yu, S.-Y., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-016-0308-2 · Cited by 37
Inhibition of TRPM2 by AG490 Is Neuroprotective in a Parkinson’s Disease Animal Model
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Metal nanoparticles in neuroinflammation: impact on microglial dynamics and CNS function
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“neuroectoderm; however, recent evidence demonstrates they share some common monocyte markers and therefore stem from the myeloid cell line.(1,2) Moreover, in certain situations microglia are completely indistinguishable from bone marrowderived peripheral macrophages,(3)”
BackgroundInfluential
Anti-neuroinflammatory and neuroprotective effects of the Lindera neesiana fruit in vitro
Subedi, L., Gaire, B. P., Do, M. H., Lee, T. H., & Kim, S. Y. (2016) · Phytomedicine · doi:10.1016/j.phymed.2016.05.002 · Cited by 36
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Novel Neuroprotective Potential of Crocin in Neurodegenerative Disorders: An Illustrated Mechanistic Review
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Cellular and Molecular Interactions in CNS Injury: The Role of Immune Cells and Inflammatory Responses in Damage and Repair
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CD74 indicates microglial activation in experimental diabetic retinopathy and exogenous methylglyoxal mimics the response in normoglycemic retina
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“Several studies provide evidence that activated microglia can secret multiple neurotoxic factors, including tumor necrosis factor, nitric oxide, interleukin-1ß and reactive oxygen species, driving progressive neuron damage [22, 23].”
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ALX/FPR2 Modulates Anti-Inflammatory Responses in Mouse Submandibular Gland
Wang, C.-S., Wee, Y., Yang, C.-H., Melvin, J. E., & Baker, O. J. (2016) · Scientific Reports · doi:10.1038/srep24244 · Cited by 35
Vaccinium bracteatum Thunb. Exerts Anti-Inflammatory Activity by Inhibiting NF-κB Activation in BV-2 Microglial Cells
Kwon, S., Ma, S.-X., Ko, Y., Seo, J., Lee, B. R., Lee, T. H., Kim, S. Y., Lee, S., & Jang, C. (2016) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2015.205 · Cited by 35
“Activation of microglia and the consequent release of proinflammatory and/or cytotoxic factors, such as tumor necrosis factor-alpha (TNF-α), interleukin-1 beta (IL-1b), interleukin-6 (IL-6), nitric oxide (NO), prostaglandin E2 (PGE2), and reactive oxygen species (ROS) are believed to contribute to neurodegenerative pr…”
Background
Benzyl isothiocyanate inhibits inflammasome activation in E. coli LPS-stimulated BV2 cells
Lee, C.-M., Lee, D.-S., Jung, W., Yoo, J. S., Yim, M., Choi, Y. H., Park, S.-G., Seo, S., Choi, J. S., Lee, Y., et al. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2667 · Cited by 35
Indomethacin promotes survival of new neurons in the adult murine hippocampus accompanied by anti-inflammatory effects following MPTP-induced dopamine depletion
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Mechanisms underlying select chemotherapeutic-agent-induced neuroinflammation and subsequent neurodegeneration
McLeary, F. A., Davis, A., Rudrawar, S., Perkins, A. V., & Anoopkumar‐Dukie, S. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.09.034 · Cited by 36
Regulated Necrosis Orchestrates Microglial Cell Death in Manganese-Induced Toxicity
Alcon, S. P., Gorojod, R. M., & Kotler, M. L. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.10.006 · Cited by 35
Niacin mitigates blood–brain barrier tight junctional proteins dysregulation and cerebral inflammation in ketamine rat model of psychosis: Role of GPR109A receptor
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FAM19A3, a novel secreted protein, modulates the microglia/macrophage polarization dynamics and ameliorates cerebral ischemia
Shao, Y., Deng, T., Zhang, T., Li, P., & Wang, Y. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.01.003 · Cited by 34
“Otherwise, several studies have also stated that M1 microglia release proinflammatory mediators that contribute to neuronal dysfunction and cell death [20,23].”
Background
Aqueous Extract of Dendropanax morbiferus Leaves Effectively Alleviated Neuroinflammation and Behavioral Impediments in MPTP‐Induced Parkinson’s Mouse Model
Park, S., Karthivashan, G., Ko, H. M., Cho, D.-Y., Kim, J.-S., Cho, D. J., Ganesan, P., Su-Kim, I., & Choi, D. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/3175214 · Cited by 35
“Increasing evidence suggests that the activation of resting glial cells was attained either by direct factors, that is, toxins, pathogens, or endogenous proteins, or by indirect factors due to neuronal death cascades [6, 7].”
Background
Ebselen prevents cigarette smoke-induced cognitive dysfunction in mice by preserving hippocampal synaptophysin expression
Luca, S. N. D., Brassington, K., Chan, S. M. H., Dobric, A., Mou, K., Seow, H. J., & Vlahos, R. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02432-y · Cited by 34
“Furthermore, studies have shown that microglia are not only sensitive to oxidative stress, but activated microglia are also capable of producing ROS themselves, thereby perpetuating the oxidative burden [30] and neurocognitive dysfunction seen in COPD.”
Background
Mechanisms of microRNA-132 in central neurodegenerative diseases: A comprehensive review
Mu, C., Gao, M., Xu, W., Sun, X., Chen, T., Xu, H., & Qiu, H. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.116029 · Cited by 37
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“Microglia are immune response cells in the brain and their uncontrolled activation is reported to promote neuronal degeneration (Lull & Block, 2010).”
Background
EriB targeted inhibition of microglia activity attenuates MPP+ induced DA neuron injury through the NF-κB signaling pathway
Dou, F., Chu, X., Zhang, B., Liang, L., Lü, G., Ding, J., & Chen, S. (2018) · Molecular Brain · doi:10.1186/s13041-018-0418-z · Cited by 34
Can krill oil be of use for counteracting neuroinflammatory processes induced by high fat diet and aging?
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Microglia dependent BDNF and proBDNF can impair spatial memory performance during persistent inflammatory pain
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Cognitive and Neuronal Link With Inflammation: A Longitudinal Study in People With and Without HIV Infection
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The Combined Effects of Lysophospholipids against Lipopolysaccharide-induced Inflammation and Oxidative Stress in Microglial Cells
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Pomegranate (Punica granatum L.) Attenuates Neuroinflammation Involved in Neurodegenerative Diseases
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“However, the chronic activation of microglia, specifically mediated by microglia proinflammatory M1 phenotype, leads to the production of proinflammatory cytokines that contribute to the progression of various neurodegenerative diseases [18].”
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Elevated Glucose and Interleukin-1β Differentially Affect Retinal Microglial Cell Proliferation
Baptista, F. I., Aveleira, C. A., Castilho, Á., & Ambrósio, A. F. (2017) · Mediators of Inflammation · doi:10.1155/2017/4316316 · Cited by 34
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Background
Understanding the Molecular Progression of Chronic Traumatic Encephalopathy in Traumatic Brain Injury, Aging and Neurodegenerative Disease
Ruchika, F., Shah, S., Neupane, D., Vijay, R., Mehkri, Y., & Lucke-Wold, B. P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031847 · Cited by 37
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Background

Authors: Lull, M. E., & Block, M. L.
Affiliations: Virginia Commonwealth University (US)
Corresponding author: Block, Michelle L.
ORCID: Lull, Melinda E.
Block, Michelle L.
Venue: Neurotherapeutics
Publisher: Elsevier BV
Published: 2010-10
Volume: 7
Issue: 4
Pages: 354-365
ISSN: 1878-7479 (ISSN-L)
DOI: 10.1016/j.nurt.2010.05.014
PMC: PMC2951017
OpenAlex: W2050320551
Cited by: 1,047
References: 182
Citations by year: 2026: 50 · 2025: 112 · 2024: 94 · 2023: 60 · 2022: 84 · 2021: 95 · 2020: 84 · 2019: 78 · 2018: 83 · 2017: 76 · 2016: 73 · 2015: 43 · 2014: 38 · 2013: 28 · 2012: 30
FWCI: 14.71
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4696 d)
Locations: Neurotherapeutics (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Fisher Digital Publications (St. John Fisher College) (submittedVersion)
Funders: National Institutes of Health
National Institute of Environmental Health Sciences (R01ES016951, R00ES01549)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: microglial activation, neurodegeneration, reactive microgliosis, reactive oxygen species, neuroinflammation, neurotoxicity, Parkinson's disease, neuronal cell death, lipopolysaccharide, TNF-α, nitric oxide, IL-1β
MeSH terms: Animals, Chronic Disease, Dopamine, Humans, Models, Biological, Neurons, Oxidation-Reduction, Signal Transduction, Reactive Oxygen Species, Microglia, NADPH Oxidases, Neurodegenerative Diseases

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