Cited by 422Neuroinflammation and Neurodegeneration MechanismsInflammasome and immune disordersTraumatic Brain Injury and Neurovascular Disturbances

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Microglial priming and enhanced reactivity to secondary insult in aging, and traumatic CNS injury, and neurodegenerative disease

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Norden, Diana M., Muccigrosso, Megan M., Godbout, Jonathan P.·2015·Neuropharmacology

DOI 10.1016/j.neuropharm.2014.10.028PMC PMC4430467

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Abstract

Glia of the central nervous system (CNS) help to maintain homeostasis in the brain and support efficient neuronal function. Microglia are innate immune cells of the brain that mediate responses to pathogens and injury. They have key roles in phagocytic clearing, surveying the local microenvironment and propagating inflammatory signals. An interruption in homeostasis induces a cascade of conserved adaptive responses in glia. This response involves biochemical, physiological and morphological changes and is associated with the production of cytokines and secondary mediators that influence synaptic plasticity, cognition and behavior. This reorganization of host priorities represents a beneficial response that is normally adaptive but may become maladaptive when the profile of microglia is compromised. For instance, microglia can develop a primed or pro-inflammatory mRNA, protein and morphological profile with aging, traumatic brain injury and neurodegenerative disease. As a result, primed microglia exhibit an exaggerated inflammatory response to secondary and sub-threshold challenges. Consequences of exaggerated inflammatory responses by microglia include the development of cognitive deficits, impaired synaptic plasticity and accelerated neurodegeneration. Moreover, impairments in regulatory systems in these circumstances may make microglia more resistant to negative feedback and important functions of glia can become compromised and dysfunctional. Overall, the purpose of this review is to discuss key concepts of microglial priming and immune-reactivity in the context of aging, traumatic CNS injury and neurodegenerative disease. This article is part of a Special Issue entitled 'Neuroimmunology and Synaptic Function'.

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Aged brain and neuroimmune responses to COVID-19: post-acute sequelae and modulatory effects of behavioral and nutritional interventions
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Influence of biological sex on neuroinflammatory dynamics in the aging brain
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Wagner, A. K., & Kumar, R. G. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.09.011 · Cited by 24
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Peroxisom proliferator-activated receptor-γ coactivator-1α in neurodegenerative disorders: A promising therapeutic target
Yang, Y.-N., Zhang, M.-Q., Yu, F.-L., Han, B., Bao, M.-Y., Yan-He, Yan-he, & Zhang, Y. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115717 · Cited by 26
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Kim, J., Jeong, Y., Lee, E. J., Park, J., Seo, H., & Kim, H.-S. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.09.129 · Cited by 25
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Cai, X., Lin, S., Geng, Z., Luo, L., Liu, Y.-J., Zhang, Z., Liu, W., Chen, X., Li, X., Yan, J., et al. (2020) · Neurochemical Research · doi:10.1007/s11064-020-02984-6 · Cited by 24
Progressive long‐term spatial memory loss following repeat concussive and subconcussive brain injury in mice, associated with dorsal hippocampal neuron loss, microglial phenotype shift, and vascular abnormalities
Honig, M. G., Dorian, C. C., Worthen, J. D., Micetich, A. C., Mulder, I. A., Sanchez, K. B., Pierce, W. F., Mar, N. A. D., & Reiner, A. J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14711 · Cited by 26
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Susceptibility to acute cognitive dysfunction in aged mice is underpinned by reduced white matter integrity and microgliosis
Healy, D., Murray, C., McAdams, C., Power, R. W., Hollier, P.-L., Lambe, J., Tortorelli, L. S., López-Rodríguez, A. B., & Cunningham, C. M. (2024) · Communications Biology · doi:10.1038/s42003-023-05662-9 · Cited by 24
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Makinde, H. M., Just, T. B., Cuda, C. M., Perlman, H., & Schwulst, S. J. (2017) · Shock · doi:10.1097/shk.0000000000000859 · Cited by 24
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The effects of living in an outdoor enclosure on hippocampal plasticity and anxiety‐like behavior in response to nematode infection
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Authors: Norden, D. M., Muccigrosso, M. M., & Godbout, J. P.
Affiliations: The Ohio State University (US)
The Ohio State University Wexner Medical Center (US)
Corresponding author: Godbout, Jonathan P.
ORCID: Godbout, Jonathan P.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2015-09
Volume: 96
Issue: Pt A
Pages: 29-41
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2014.10.028
PMC: PMC4430467
OpenAlex: W2051504363
Cited by: 413
References: 156
Citations by year: 2026: 37 · 2025: 36 · 2024: 28 · 2023: 31 · 2022: 37 · 2021: 44 · 2020: 41 · 2019: 33 · 2018: 41 · 2017: 34 · 2016: 29 · 2015: 21
FWCI: 2.26
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (R01-AG-033028)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Keywords: microglial priming, microglial activation, aging, traumatic brain injury, neurodegenerative diseases, neuroinflammation, secondary injury, cognitive impairment, synaptic plasticity, neurodegeneration, innate immunity, neuroimmunology
MeSH terms: Aging, Astrocytes, Brain Injuries, Encephalitis, Craniocerebral Trauma, Humans, Male, Neuronal Plasticity, Microglia, Inflammation Mediators, Neurodegenerative Diseases, Illness Behavior

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Microglial priming and enhanced reactivity to secondary insult in aging, and traumatic CNS injury, and neurodegenerative disease

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