Review: microglia of the aged brain: primed to be activated and resistant to regulation

Norden, D. M.; Godbout, J. P.

doi:10.1111/j.1365-2990.2012.01306.x

Cited by 792Neuroinflammation and Neurodegeneration MechanismsInflammasome and immune disordersTryptophan and brain disorders

Review: microglia of the aged brain: primed to be activated and resistant to regulation

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Norden, D. M., Godbout, J. P.·2013·Neuropathology and Applied Neurobiology

DOI 10.1111/j.1365-2990.2012.01306.xPMC PMC3553257

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Abstract

Innate immunity within the central nervous system ( CNS ) is primarily provided by resident microglia. Microglia are pivotal in immune surveillance and also facilitate the co‐ordinated responses between the immune system and the brain. For example, microglia interpret and propagate inflammatory signals that are initiated in the periphery. This transient microglial activation helps mount the appropriate physiological and behavioural response following peripheral infection. With normal ageing, however, microglia develop a more inflammatory phenotype. For instance, in several models of ageing there are increased pro‐inflammatory cytokines in the brain and increased expression of inflammatory receptors on microglia. This increased inflammatory status of microglia with ageing is referred to as primed, reactive or sensitized. A modest increase in the inflammatory profile of the CNS and altered microglial function in ageing has behavioural and cognitive consequences. Nonetheless, there are major differences in microglial biology between young and old age when the immune system is challenged and microglia are activated. In this context, microglial activation is amplified and prolonged in the aged brain compared with adults. The cause of this amplified microglial activation may be related to impairments in several key regulatory systems with age that make it more difficult to resolve microglial activation. The consequences of impaired regulation and microglial hyper‐activation following immune challenge are exaggerated neuroinflammation, sickness behaviour, depressive‐like behaviour and cognitive deficits. Therefore the purpose of this review is to discuss the current understanding of age‐associated microglial priming, consequences of priming and reactivity, and the impairments in regulatory systems that may underlie these age‐related deficits.

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Crossref · 10.1111/j.1365-2990.2012.01306.x

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Astrocytes and microglia become hyper-activated with age.
“Astrocytes and microglia, mediators of the innate immune response of the central nervous system, become hyper-activated with age (Baruch et al., 2014; Norden and Godbout, 2013).”
From Loss of epigenetic information as a cause of mammalian aging (2023) · cites this paper as Norden and Godbout, 2013
The section “Astrocytes also have a more inflammatory profile with age” reports age-related changes resembling an activated astrocytic profile. The Abstract and “Innate immune challenge leads to prolonged and exaggerated neuroinflammation” describe aged microglia as primed, with hyper-activation occurring following immune challenge. The claim omits that condition and overstates what the review says about activation with age alone. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Astrocytes demonstrate similar age-related changes, including elevated GFAP expression and hypertrophic morphology, suggesting a transition toward a proinflammatory state.
“Astrocytes also demonstrate similar age-related changes, including elevated glial fibrillary acidic protein (GFAP) expression and hypertrophic morphology (160), both of which suggest a transition toward a proinflammatory state.”
From Connecting aging biology and inflammation in the omics era (2022) · cites this paper as [160]
The primed state is thought to make aged microglia disproportionately reactive to immunological challenges, leading to prolonged neuroinflammation and cognitive deficits associated with age.
“This state of ‘priming’ is thought to make aged microglia disproportionately reactive to immunological challenges, leading to prolonged neuroinflammation and the cognitive deficits associated with age [65,66].”
From Untangling senescent and damage‐associated microglia in the aging and diseased brain (2023) · cites this paper as [65]
This morphological profile of the aged microglia first reported in rats has also been confirmed in mice, gerbils, and dogs.
“This morphological profile of the aged microglia first reported in rats has also been confirmed in mice, gerbils, and dogs (Hwang et al, 2008;Korhonen et al, 1997;Norden and Godbout, 2013;Streit and Xue, 2010).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Norden and Godbout, 2013

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Age and neuroinflammation: a lifetime of psychoneuroimmune consequences
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Exaggerated sickness behavior and brain proinflammatory cytokine expression in aged mice in response to intracerebroventricular lipopolysaccharide
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Immune surveillance of mouse brain perivascular spaces by blood‐borne macrophages
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Life and Death of Microglia
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An Age-Related Decline in Interleukin-10 May Contribute to the Increased Expression of Interleukin-6 in Brain of Aged Mice
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Lipopolysaccharide-induced interleukin (IL)-4 receptor-α expression and corresponding sensitivity to the M2 promoting effects of IL-4 are impaired in microglia of aged mice
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The mosaic of brain glial hyperactivity during normal ageing and its attenuation by food restriction
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BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1β administration
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Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents
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Wheel running attenuates microglia proliferation and increases expression of a proneurogenic phenotype in the hippocampus of aged mice
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Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer’s disease
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Interleukin-6 in the aging brain
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Neurons, glia, and plasticity in normal brain aging
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Minocycline Down-regulates MHC II Expression in Microglia and Macrophages through Inhibition of IRF-1 and Protein Kinase C (PKC)α/βII
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Dietary Supplementation with Vitamin E Reverses the Age-related Deficit in Long Term Potentiation in Dentate Gyrus
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Inflammatory processes in the aging mouse brain: Participation of dendritic cells and T-cells
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Little Exercise, Big Effects: Reversing Aging and Infection-Induced Memory Deficits, and Underlying Processes
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Eicosapentaenoic acid confers neuroprotection in the amyloid-β challenged aged hippocampus
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Differences in the early inflammatory responses to toxin-induced demyelination are associated with the age-related decline in CNS remyelination
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The Anti-inflammatory Cytokine, Interleukin (IL)-10, Blocks the Inhibitory Effect of IL-1β on Long Term Potentiation
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Aging and glial responses to lipopolysaccharide in vitro: greater induction of IL-1 and IL-6, but smaller induction of neurotoxicity
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Concurrent hippocampal induction of MHC II pathway components and glial activation with advanced aging is not correlated with cognitive impairment
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Consuming a diet supplemented with resveratrol reduced infection-related neuroinflammation and deficits in working memory in aged mice
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IL‐4 attenuates the neuroinflammation induced by amyloid‐β in vivo and in vitro
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Cognitive and neuroinflammatory consequences of mild repeated stress are exacerbated in aged mice
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TGFβ directs gene expression of activated microglia to an anti‐inflammatory phenotype strongly focusing on chemokine genes and cell migratory genes
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Analysis of gial acidic fibrillary protein in the human entorhinal cortex during aging and in Alzheimer's disease
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Age and Neuroinflammation: A Lifetime of Psychoneuroimmune Consequences
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Exercise increases neural stem cell number in a growth hormone-dependent manner, augmenting the regenerative response in aged mice
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Aging and a Peripheral Immune Challenge Interact to Reduce Mature Brain-Derived Neurotrophic Factor and Activation of TrkB, PLCγ1, and ERK in Hippocampal Synaptoneurosomes
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CD200 fusion protein decreases microglial activation in the hippocampus of aged rats
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Enhanced IL‐1β production in response to the activation of hippocampal glial cells impairs neurogenesis in aged mice
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Alternatively activated myeloid (M2) cells enhance cognitive function in immune compromised mice
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Neuro–glia interaction effects on GFAP gene: a novel role for transforming growth factor‐β1
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Human medial temporal lobe in aging: Anatomical basis of memory preservation
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Architectural changes to CA1 pyramidal neurons in adult and aged mice after peripheral immune stimulation
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A Pivotal Role for Interleukin-4 in Atorvastatin-associated Neuroprotection in Rat Brain
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Macrosialin increases during normal brain aging are attenuated by caloric restriction
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Aging and infection reduce expression of specific brain-derived neurotrophic factor mRNAs in hippocampus
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Cognitive and Behavioral Consequences of Impaired Immunoregulation in Aging
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Adverse Effect of a Presenilin-1 Mutation in Microglia Results in Enhanced Nitric Oxide and Inflammatory Cytokine Responses to Immune Challenge in the Brain
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A novel anti-inflammatory role of NCAM-derived mimetic peptide, FGL
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Central inhibition of interleukin-1β ameliorates sickness behavior in aged mice
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IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344 × BN F1 rats
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Aging sensitizes mice to behavioral deficits induced by central HIV-1 gp120
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Increased IL-1β in cortex of aged rats is accompanied by downregulation of ERK and PI-3 kinase
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Proliferative Response of Microglia and Macrophages in the Adult Mouse Eye after Optic Nerve Lesion
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Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning
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Systemic lipopolysaccharide (LPS)-induced microglial activation results in different temporal reduction of CD200 and CD200 receptor gene expression in the brain
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Age-related changes in the hippocampus (loss of synaptophysin and glial–synaptic interaction) are modified by systemic treatment with an NCAM-derived peptide, FGL
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Dual modulation of synaptic transmission in the nucleus tractus solitarius by prostaglandin E2 synthesized downstream of IL‐1β
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Comparison of Ionized Calcium-binding Adapter Molecule 1 Immunoreactivity of the Hippocampal Dentate Gyrus and CA1 Region in Adult and Aged Dogs
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Authors: Norden, D. M., & Godbout, J. P.
Affiliations: The Ohio State University (US)
Corresponding author: Godbout, J. P.
ORCID: Godbout, J. P.
Venue: Neuropathology and Applied Neurobiology
Publisher: Wiley
Published: 2013-01-22
Volume: 39
Issue: 1
Pages: 19-34
ISSN: 0305-1846 (ISSN-L)
1365-2990
DOI: 10.1111/j.1365-2990.2012.01306.x
PMC: PMC3553257
OpenAlex: W1622777525
Cited by: 792
References: 153
Citations by year: 2026: 55 · 2025: 42 · 2024: 63 · 2023: 55 · 2022: 73 · 2021: 89 · 2020: 74 · 2019: 55 · 2018: 64 · 2017: 61 · 2016: 44 · 2015: 49 · 2014: 43 · 2013: 22 · 2012: 2
FWCI: 3.45
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Neuropathology and Applied Neurobiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Aging (R01AG033028)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: microglia, brain aging, microglial priming, microglial activation, neuroinflammation, innate immunity, inflammatory cytokines, sickness behavior, depression-like behavior, cognitive impairment
MeSH terms: Aging, Animals, Brain, Humans, Immunity, Innate, Inflammation, Microglia

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