Cited by 735Neuroinflammation and Neurodegeneration MechanismsImmune Response and InflammationInflammasome and immune disorders

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TLR Signaling Tailors Innate Immune Responses in Human Microglia and Astrocytes

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Jack, Carolyn S, Arbour, Nathalie, Manusow, Joshua, Montgrain, Vivianne, Blain, Manon, McCrea, Ellie, Shapiro, Aaron, Antel, Jack P·2005·The Journal of Immunology

DOI 10.4049/jimmunol.175.7.4320

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Abstract

The specific signals mediating the activation of microglia and astrocytes as a prelude to, or consequence of, CNS inflammation continue to be defined. We investigated TLRs as novel receptors mediating innate immune responses in human glial cells. We find that microglia express mRNA for TLRs 1-9, whereas astrocytes express robust TLR3, low-level TLR 1, 4, 5, and 9, and rare-to-undetectable TLR 2, 6, 7, 8, and 10 mRNA (quantitative real-time PCR). We focused on TLRs 3 and 4, which can signal through both the MyD88-dependent and -independent pathways, and on the MyD88-restricted TLR2. By flow cytometry, we established that microglia strongly express cell surface TLR2; TLR3 is expressed at higher levels intracellularly. Astrocytes express both cell surface and intracellular TLR3. All three TLRs trigger microglial activation upon ligation. TLR3 signaling induces the strongest proinflammatory polarizing response, characterized by secretion of high levels of IL-12, TNF-alpha, IL-6, CXCL-10, and IL-10, and the expression of IFN-beta. CXCL-10 and IL-10 secretion following TLR4 ligation are comparable to that of TLR3; however, other responses were lower or absent. TLR2-mediated responses are dominated by IL-6 and IL-10 secretion. Astrocytes respond to TLR3 ligation, producing IL-6, CXCL-10, and IFN-beta, implicating these cells as contributors to proinflammatory responses. Initial TLR-mediated glial activation also regulates consequent TLR expression; while TLR2 and TLR3 are subject to positive feedback, TLR4 is down-regulated in microglia. Astrocytes up-regulate all three TLRs following TLR3 ligation. Our data indicate that activation of innate immune responses in the CNS is not homogeneous but rather tailored according to cell type and environmental signal.

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“For instance, TLR 2 and TLR 3 are the prevalent TLRs in astrocytes and are both highly expressed in RNA and protein levels in human white matter samples and human astrocyte cultures of embryonic origin, respectively (53, 56), however, an alternate study reported TLR 2 mRNA level as negligible in astrocytes obtained fr…”
Background
Neurotropin alleviates cognitive impairment by inhibiting TLR4/MyD88/NF-κB inflammation signaling pathway in mice with vascular dementia
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“dsRNA binding to TLR3 initiates a signaling cascade causing IjBa phosphorylation and degradation leading to the nuclear translocation of NFjB and transcription of pro-inflammatory genes (Carpentier et al., 2005; Jack et al., 2005; Kim et al., 2008) including those displayed in our Results (Figs.”
BackgroundInfluential
Quantification of the functional expression of the Ca2+-activated K+channel KCa3.1 on microglia from adult human neocortical tissue
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“Experimental support for considering these microglia as resting cells were lack of basic TNF-a release and negligible gene expression levels of TNF-a, IL-6, and IL-1b combined with a massive upregulation and secretion upon challenge with the standard proinflammatory molecule LPS, a response in accordance with the expr…”
Background
RNA Nanotherapeutics for the Amelioration of Astroglial Reactivity
Smith, J. A., Braga, A., Verheyen, J., Basilico, S., Bandiera, S., Alfaro‐Cervelló, C., Peruzzotti‐Jametti, L., Shu, D., Haque, F., Guo, P., et al. (2017) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2017.11.008 · Cited by 22
Contrasting effect of the latency-reversing agents bryostatin-1 and JQ1 on astrocyte-mediated neuroinflammation and brain neutrophil invasion
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“inflammatory potential on astrocytes [19, 20].”
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Involvement of CLEC16A in Activation of Astrocytes After LPS Treated
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“Previous studies report that TLR3 stimulation induces interferon regulatory factor (IRF)-3 activation, which increases the production of IFN-β and improves EAE [34].”
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Toll-like Receptors in Viral Encephalitis
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Host immune responses in the central nervous system during fungal infections
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“TLRs in microglia— Microglia constitutively express Toll-like receptors (TLRs), such as TLR1–9, TLR11–13 in mice 72,73 and TLR1–10 in humans 74,75 , together with their adaptor proteins.”
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“However, upon ligation of the TLR’s, astrocytes have shown to increase TLR protein expression and the release of cytokines (Bsibsi et al., 2007; Jack et al., 2005).”
Background
Brain heterogeneity leads to differential innate immune responses and modulates pathogenesis of viral infections.
Zegenhagen, L., Kurhade, C., Koniszewski, N., Överby, A. K., & Kröger, A. (2016) · Cytokine & growth factor reviews · doi:10.1016/j.cytogfr.2016.03.006 · Cited by 20
Prevention of the Severity of Post-ischemic Inflammation and Brain Damage by Simultaneous Knockdown of Toll-like Receptors 2 and 4
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Viral mimetic priming enhances α-synuclein-induced degeneration: Implications for Parkinson’s disease
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TLR-3 receptor activation protects the very immature brain from ischemic injury
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“In the human CNS, microglia express TLRs 1 to 9, astrocytes express robust TLR-3 and low-level TLRs 1,4,5,9 and oligodendrocytes express TLR-3 and TLR-2 [3,4].”
Background
Interleukin-18 in chronic pain: Focus on pathogenic mechanisms and potential therapeutic targets
Ju, J., Li, Z., Jia, X., Peng, X., Wang, J., & Gao, F. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107089 · Cited by 24
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Enteric Neural Disruption in Necrotizing Enterocolitis Occurs in Association With Myenteric Glial Cell CCL20 Expression
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Taking a Toll on Self-Renewal: TLR-Mediated Innate Immune Signaling in Stem Cells
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“coli LPS [7].”
BackgroundInfluential
The Potential Therapeutic Role of the HMGB1-TLR Pathway in Epilepsy
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The Innate and Adaptive Immune Cells in Alzheimer’s and Parkinson’s Diseases
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“In the context of AD and PD, some members of the Toll-like receptor (TLR) family, which can recognize protein aggregates in these diseases, are involved in the disease progression [31].”
Background
Glaucoma and microglia-induced neuroinflammation
Ishikawa, M., Izumi, Y., Sato, K., Sato, T., Zorumski, C. F., Kunikata, H., & Nakazawa, T. (2023) · Frontiers in Ophthalmology · doi:10.3389/fopht.2023.1132011 · Cited by 31
“TLR4 is associated with both neuro-inflammation and clearance of protein aggregates in neurodegenerative disorders (32).”
Background
Toll-Like Receptors in Brain Abscess
Esen, N., & Kielian, T. (2009) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-00549-7_3 · Cited by 19
“…direct evidence for the presence of TLRs in astrocytes (Bsibsi et al. 2002 ; Bowman et al. 2003 ; Esen et al. 2004 ; Carpentier et al. 2005 ; Jack et al. 2005) ; however, the number of TLRs expressed is much lower compared to microglia, which may be explained by the fact that microglia are…”
Background
Innate Immune Responses in the CNS: Role of Toll-Like Receptors, Mechanisms, and Therapeutic Opportunities in Multiple Sclerosis
Podda, G., Nyirenda, M., Crooks, J. E., & Gran, B. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9483-3 · Cited by 19
“In cultures of human microglia, ligation of TLR4 by LPS or TLR3 by dsRNA induced the secretion of CXCL10, which is thought to attract T cells to MS lesions (Jack et al. 2005).”
Role of Infiltrating Microglia/Macrophages in Glioma
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Vitamin D Regulates MerTK-Dependent Phagocytosis in Human Myeloid Cells
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Imiquimod and interferon-alpha augment monocyte-mediated astrocyte secretion of MCP-1, IL-6 and IP-10 in a human co-culture system
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Isolation of Human Brain Endothelial Cells and Characterization of Lipid Raft-Associated Proteins by Mass Spectroscopy
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Principles of Astrogliopathology
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“The PAMPs are exogenous agents associated with pathogens such as bacteria, viruses or prions; these factors stimulate Toll-like receptors (TLRs) widely expressed in astrocytes (Jack et al. 2005; Kielian 2006).”
Background
Defensive Perimeter in the Central Nervous System: Predominance of Astrocytes and Astrogliosis during Recovery from Varicella-Zoster Virus Encephalitis
Carpenter, J. E., Clayton, A. C., Halling, K. C., Bonthius, D. J., Buckingham, E. M., Jackson, W., Dotzler, S. M., Card, J. P., Enquist, L. W., & Grose, C. F. (2015) · Journal of Virology · doi:10.1128/jvi.02389-15 · Cited by 18
“Instead, they participate in several functions, including energy metabolism, ion exchange, and glutamate homeostasis, as well as acting as sentinels for viral infection via their expression of the Toll-like receptor 3 (TLR3) (39, 40).”
Background
Choroidal Neovascular Membranes Express Toll-Like Receptor 3
Maloney, S., Antecka, E., Orellana, M. E., Fernandes, B. F., Odashiro, A. N., Eghtedari, M., & Burnier, M. N. (2010) · Ophthalmic Research · doi:10.1159/000313989 · Cited by 18
Phosphatidylinositol 4-phosphate 5-kinase α contributes to Toll-like receptor 2-mediated immune responses in microglial cells stimulated with lipoteichoic acid
Nguyen, T. T. N., Seo, E., Choi, J., Le, O. T. T., Kim, J. Y., Jou, I., & Lee, S. Y. (2017) · Cellular Signalling · doi:10.1016/j.cellsig.2017.07.009 · Cited by 19
Phosphoinositide turnover in Toll-like receptor signaling and trafficking
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“croglia and astrocytes express most TLRs and function as immune effector cells (33, 34).”
Background
Hormesis of methylmercury-human serum albumin conjugate on N9 microglia via ERK/MAPKs and STAT3 signaling pathways
Tan, Q., Zhang, M., Geng, L., Xia, Z., Li, C., Usman, M., Du, Y., Wei, L., & Bi, H. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.10.017 · Cited by 17
Suppressed microglial E prostanoid receptor 1 signaling selectively reduces tumor necrosis factor alpha and interleukin 6 secretion from toll‐like receptor 3 activation
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“…explored the activation of the TLRs known to be expressed functionally by microglia (Block et al., 2007) by ligands that have relative specificity at the concentrations used (Iliev et al., 2004; Jack et al., 2005; Olson and Miller, 2004; Park et al., 2006; Ribes et al., 2009; Shah et al., 2009).”
Background
Inhibition of spinal 15-LOX-1 attenuates TLR4-dependent, nonsteroidal anti-inflammatory drug–unresponsive hyperalgesia in male rats
Gregus, A. M., Buczynski, M. W., Dumlao, D. S., Norris, P. C., Rai, G., Simeonov, A. M., Maloney, D. J., Jadhav, A., Xu, Q., Wei, S. C., et al. (2018) · Pain · doi:10.1097/j.pain.0000000000001373 · Cited by 17
Genetics of COVID ‐19 and myalgic encephalomyelitis/chronic fatigue syndrome: a systematic review
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Counting the Toll of Inflammation on Schizophrenia—A Potential Role for Toll-like Receptors
Patlola, S. R., Donohoe, G. J., & McKernan, D. P. (2023) · Biomolecules · doi:10.3390/biom13081188 · Cited by 18
“Stimulation studies demonstrate that human microglial cells from foetal cerebral tissue [39] responded to ligands that activate TLR2, 3, and 4 by releasing cytokines such as interleukin-6 (IL-6) and tumour necrosis factor-α (TNF-α), whereas astrocytes elicited a response only to polyinosinic:polycytidylic acid (poly I…”
Background
Role of toll-like receptor 2 in ischemic demyelination and oligodendrocyte death
Choi, J. Y., Cui, Y., Kang, Y. M., Kim, J., Lee, S. J., & Kim, B. G. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.01.146 · Cited by 16
MMHD [(S,E)-2-Methyl-1-(2-methylthiazol-4-yl) hexa-1,5-dien-ol], a Novel Synthetic Compound Derived From Epothilone, Suppresses Nuclear Factor-κB–Mediated Cytokine Expression in Lipopolysaccharide-Stimulated BV-2 Microglia
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High glucose-induced defective thrombospondin-1 release from astrocytes via TLR9 activation contributes to the synaptic protein loss
Zhao, Y., Pu, D., Sun, Y., Chen, J., Luo, C., Wang, M., Zhou, J., Lv, A., Zhu, S., Liao, Z., et al. (2017) · Experimental Cell Research · doi:10.1016/j.yexcr.2017.12.030 · Cited by 16

Authors: Jack, C. S., Arbour, N., Manusow, J., Montgrain, V., Blain, M., McCrea, E., Shapiro, A., & Antel, J. P.
Affiliations: Montreal Neurological Institute and Hospital (CA)
ORCID: Jack, Carolyn S
Arbour, Nathalie
Shapiro, Aaron
Antel, Jack P
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2005-10-01
Volume: 175
Issue: 7
Pages: 4320-4330
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.175.7.4320
OpenAlex: W2165413779
Cited by: 734
References: 46
Citations by year: 2026: 17 · 2025: 21 · 2024: 15 · 2023: 34 · 2022: 44 · 2021: 42 · 2020: 25 · 2019: 26 · 2018: 36 · 2017: 39 · 2016: 38 · 2015: 40 · 2014: 33 · 2013: 59 · 2012: 44
FWCI: 20.39
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Keywords: Toll-like receptors, microglia, astrocytes, glial activation, TLR3, TLR4, TLR2, MyD88 signaling, neuroinflammation, inflammatory cytokines, CXCL10, IL-10, interferon-beta, innate immunity
MeSH terms: Adult, Antigens, Differentiation, Astrocytes, Fetus, Humans, Immunity, Innate, Receptors, Immunologic, Signal Transduction, Interleukin-10, Microglia, Interleukin-12, Adaptor Proteins, Signal Transducing, Myeloid Differentiation Factor 88

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TLR Signaling Tailors Innate Immune Responses in Human Microglia and Astrocytes

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