Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system

Liu, W.; Tang, Y.; Feng, J.

doi:10.1016/j.lfs.2011.05.011

Cited by 303Neuroinflammation and Neurodegeneration MechanismsNeuroscience and Neuropharmacology ResearchTraumatic Brain Injury and Neurovascular Disturbances

Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system

Liu, W., Tang, Y., Feng, J.·2011·Life Sciences

DOI 10.1016/j.lfs.2011.05.011

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Abstract

Microglia and astrocytes in the central nervous system are now recognized as active participants in various pathological conditions such as trauma, stroke, or chronic neurodegenerative disorders. Their activation is closely related with the development and severity of diseases. Interestingly, activation of microglia and astrocytes occurs with a spatially and temporarily distinct pattern. The present review explores the cross talk in the process of their activation. Microglia, activated earlier than astrocytes, promote astrocytic activation. On the other hand, activated astrocytes not only facilitate activation of distant microglia, but also inhibit microglial activities. Molecules contributing to their intercommunication include interleukin-1 (IL-1), adenosine triphosphate (ATP), and transforming growth factor beta (TGF-β). A better understanding about the cross talk between activation of microglia and astrocytes would be helpful to elucidate the role of glial cells in pathological conditions, which could accelerate the development of treatment for various diseases.

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Activated astrocytes release ATP that can activate purinergic receptors on neighboring microglia, resulting in microglial activation.
“Previous research has shown that activated astrocytes release adenosine triphosphate (ATP) that can activate the purinergic receptors on neighboring microglia, resulting in microglial activation (Figure 3A) (Davalos et al., 2005;Liu et al., 2011;Schipke et al., 2002;Verderio and Matteoli, 2001).”
From Single-cell resolution analysis of the crosstalk between chemogenically activated astrocytes and microglia (2020) · cites this paper as Liu et al., 2011
Activated astrocytes release ATP which activates the purinergic receptors on microglia, resulting in microglial activation.
“As mentioned earlier, activated astrocytes release ATP which activates the purinergic receptors on microglia, resulting in microglial activation (Figure 3A) (Davalos et al., 2005;Liu et al., 2011;Schipke et al., 2002;Verderio and Matteoli, 2001).”
From Single-cell resolution analysis of the crosstalk between chemogenically activated astrocytes and microglia (2020) · cites this paper as Liu et al., 2011

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Background
Differential deregulation of astrocytic calcium signalling by amyloid-β, TNFα, IL-1β and LPS.
Ronco, V., Grolla, A., Glasnov, T., Canonico, P., Verkhratsky, A., Genazzani, A., & Lim, D. (2014) · Cell Calcium · doi:10.1016/j.ceca.2014.02.016 · Cited by 82 · see citing works
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Microglia–Astrocyte Interaction in Neural Development and Neural Pathogenesis
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In vivo Imaging of Glial Activation in Alzheimer's Disease
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“It is worth noting that astrocytes and microglia communicate with each other and this cross talk is important in promoting glial activation (8, 9).”
Background
Microglial HO‐1 induction by curcumin provides antioxidant, antineuroinflammatory, and glioprotective effects
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Rehmannioside A attenuates cognitive deficits in rats with vascular dementia (VD) through suppressing oxidative stress, inflammation and apoptosis.
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Inhibition of activated astrocyte ameliorates lipopolysaccharide- induced depressive-like behaviors
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LPS Preconditioning Attenuates Apoptosis Mechanism by Inhibiting NF-κB and Caspase-3 Activity: TLR4 Pre-activation in the Signaling Pathway of LPS-Induced Neuroprotection
Sangaran, P. G., Ibrahim, Z. A., Chik, Z., Mohamed, Z., & Ahmadiani, A. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02227-3 · Cited by 78 · see citing works
Insensitivity of astrocytes to interleukin 10 signaling following peripheral immune challenge results in prolonged microglial activation in the aged brain
Norden, D. M., Trojanowski, P. J., Walker, F. R., & Godbout, J. P. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.04.014 · Cited by 73 · see citing works
The psychoneuroimmunology of pregnancy
Sherer, M. L., Posillico, C. K., & Schwarz, J. M. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.10.006 · Cited by 93 · see citing works
Sex differences in astrocyte and microglia responses immediately following middle cerebral artery occlusion in adult mice
Morrison, H. W., & Filosa, J. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.09.047 · Cited by 82 · see citing works
“…signaling which can result in glutamate excitotoxicity (Nedergaard et al., 2010) or through the release of astrocytederived proteins and small molecular messengers such as ATP, TNFα, and S100β, which further increases neuroinflammation (Agulhon et al., 2012; Liu et al., 2011; Pascual et al., 2012).”
Background
Astrocytes inhibit nitric oxide-dependent Ca2+dynamics in activated microglia: Involvement of ATP released via pannexin 1 channels
Orellana, J. A., Montero, T. D., & Rommy von Bernhardi, M. (2013) · Glia · doi:10.1002/glia.22573 · Cited by 82 · see citing works
“Microglia and astrocytes respond to any injury with a spatial and temporal distinctive pattern of activation in the inflamed CNS, their crosstalk appearing to be critical for neuronal fate (Liu et al., 2011).”
Background
C-Phycocyanin protects against acute tributyltin chloride neurotoxicity by modulating glial cell activity along with its anti-oxidant and anti-inflammatory property: A comparative efficacy evaluation with N-acetyl cysteine in adult rat brain
Mitra, S., Siddiqui, W. A., & Khandelwal, S. (2015) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2015.06.016 · Cited by 67 · see citing works
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Sex steroid hormone-mediated functional regulation of microglia-like BV-2 cells during hypoxia
Habib, P., Dreymueller, D., Ludwig, A., Beyer, C., & Dang, J. (2013) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2013.06.003 · Cited by 67 · see citing works
“In addition, the control of microglia-triggered devastating inflammatory damage to neurons is not only regulated by their capability to directly sense lesioned cells by trans-membrane receptors [43] but comparably by the receptivity for soluble regulatory molecules produced and secreted by activated and lesion-intrins…”
Peroxisome deficiency but not the defect in ether lipid synthesis causes activation of the innate immune system and axonal loss in the central nervous system
Bottelbergs, A., Verheijden, S., Van Veldhoven, P. P., Just, W., Devos, R., & Baes, M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-61 · Cited by 66 · see citing works
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An examination of changes in maternal neuroimmune function during pregnancy and the postpartum period
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Neuroinflammation: Microglial Activation During Sepsis
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“Cell density for the three cocultured system was determined by the ratio of initial seeding cells which should be equal to 10% neuron, 9–18% microglia, and 72–81% astrocytes, and which corresponds to the cell ratio in a human brain.(31,32) To induce inflammation responses prior to NP treatment, bottom chamber cells we…”
Method
Prolonged Dysfunction of Astrocytes and Activation of Microglia Accelerate Degeneration of Dopaminergic Neurons in the Rat Substantia Nigra and Block Compensation of Early Motor Dysfunction Induced by 6-OHDA
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“On the other hand, activated astrocytes can facilitate activation of distant microglia, as well as inhibit microglial activity [21].”
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Modulation of Pain and Itch by Spinal Glia
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Role of neurons and glia in the CNS actions of the renin-angiotensin system in cardiovascular control
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“Additionally, astrocytes and microglia interact with each other to regulate neuronal function (8, 14, 15, 100, 116).”
Background
Microglia and Astroglia—The Potential Role in Neuroinflammation Induced by Pre- and Neonatal Exposure to Lead (Pb)
Gąssowska-Dobrowolska, M., Chlubek, M., Kolasa, A., Tomasiak, P., Korbecki, J., Skowrońska, K., Tarnowski, M., Masztalewicz, M., & Baranowska‐Bosiacka, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129903 · Cited by 74 · see citing works
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Background
Glucocorticoid receptor in astrocytes regulates midbrain dopamine neurodegeneration through connexin hemichannel activity
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“Thus, for example, in vitro TGF-β secreted from astrocytes was shown to curb microglial production of TNF-α and reactive oxygen species [36] whereas evidence from in vivo PD animal models and in vitro astrocytemicroglia cultures indicates that IL-1β, TNF-α, I-CAM1 or ATP released from astrocytes can enhance microglial…”
Microglia are less pro‐inflammatory than myeloid infiltrates in the hippocampus of mice exposed to status epilepticus
Vinet, J., Vainchtein, I. D., Spano, C., Giordano, C., Bordini, D., Curia, G., Dominici, M., Boddeke, H. W. G. M., Eggen, B. J. L., & Biagini, G. (2016) · Glia · doi:10.1002/glia.23008 · Cited by 61 · see citing works
“Astrocytes have been shown to produce IL-1b after seizures (De Simoni et al., 2000; Librizzi et al., 2012; Liu et al., 2011).”
Background
Trasmembrane chemokines CX3CL1 and CXCL16 drive interplay between neurons, microglia and astrocytes to counteract pMCAO and excitotoxic neuronal death
Rosito, M., Lauro, C., Chece, G., Porzia, A., Monaco, L., Mainiero, F., Catalano, M., Limatola, C., & Trettel, F. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00193 · Cited by 60 · see citing works
“It is now established that both microglia and astrocytes can play dual roles in the CNS having either detrimental or beneficial effects participating and enhancing inflammatory conditions, or limiting neuroinflammation, favoring repair and enhancing neuronal survival (Liu et al., 2011).”
Mesial temporal lobe epilepsy with psychiatric comorbidities: a place for differential neuroinflammatory interplay
Kandratavicius, L., Peixoto-Santos, J. E., Monteiro, M. R., Scandiuzzi, R. C., Carlotti, C. G., Assirati, J. A., Hallak, J. E. C., & Leite, J. P. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0266-z · Cited by 55 · see citing works
“In fact, the crosstalk between activated microglia and reactive astrocytes seems crucial to the maintenance of chronic gliosis [38].”
Background
Chronic Administration of the Methylxanthine Propentofylline Impairs Reinstatement to Cocaine by a GLT-1-Dependent Mechanism
Reissner, K., Brown, R., Spencer, S. M., Tran, P. K., Thomas, C. A., & Kalivas, P. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.223 · Cited by 59 · see citing works
“Beyond sustaining normal nervous system function, in many instances of injury or disease, the activation of both microglia and astrocytes is a fundamentally important process (Liu et al, 2011).”
Astrocyte-targeted production of interleukin-6 reduces astroglial and microglial activation in the cuprizone demyelination model: Implications for myelin clearance and oligodendrocyte maturation: IL-6 in Demyelination
Petković, F., Campbell, I. L., Gonzalez, B., & Castellano, B. (2016) · Glia · doi:10.1002/glia.23043 · Cited by 59 · see citing works
“Astrocytes may play an important role in this process as a potent source of various cytokines and chemokines (Liu et al., 2011; Skripueltz et al., 2013).”
Background
Transient Receptor Potential Canonical 3 Inhibitor Pyr3 Improves Outcomes and Attenuates Astrogliosis After Intracerebral Hemorrhage in Mice
Munakata, M., Shirakawa, H., Nagayasu, K., Miyanohara, J., Miyake, T., Nakagawa, T., Katsuki, H., & Kaneko, S. (2013) · Stroke · doi:10.1161/strokeaha.113.679332 · Cited by 72 · see citing works
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Glial smog: Interplay between air pollution and astrocyte-microglia interactions
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Neuroimmune and Inflammatory Signals in Complex Disorders of the Central Nervous System
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Connexins and Pannexins: New Insights into Microglial Functions and Dysfunctions
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Tadmouri, A., Champagnat, J., & Morin-Surun, M. P. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23336 · Cited by 61 · see citing works
“…neurons, and microglia contribute to normal synaptic plasticity (for review see Ben Achour and Pascual, 2010; Pascual et al., 2012) and could also participate in various pathologies such as neurodegenerative diseases and to brain reactions to ischemia or injury (for review see Liu et al., 2011).”
Background
Early‐life stress increases the survival of midbrain neurons during postnatal development and enhances reward‐related and anxiolytic‐like behaviors in a sex‐dependent fashion
Chocyk, A., Majcher‐Maślanka, I., Przyborowska, A., Maćkowiak, M., & Wędzony, K. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.05.002 · Cited by 44 · see citing works
“Although we found dysregulation of non-neuronal cell functioning, it is worth mentioning that these cells, which are sources of neurotrophins, antioxidants and cytokines, are strongly involved in brain maturation and may affect neural cell survival (Seth and Koul, 2008; Liu et al., 2011).”
Background
Glia, sympathetic activity and cardiovascular disease
Marina, N., Teschemacher, A., Kasparov, S., & Gourine, A. (2016) · Experimental Physiology · doi:10.1113/ep085713 · Cited by 47 · see citing works
“Indeed, in an animal model of heart failure, the expression of the pro-inflammatory cytokines interleukin-1β (IL-1β) and tumour necrosis factor-α (TNF-α) was found to be significantly increased in at least one brain site that controls sympathetic outflow, namely the hypothalamic paraventricular nucleus (Kang et al. 20…”
BackgroundInfluential
Microglia-Astrocyte Cross Talk through IL-18/IL-18R Signaling Modulates Migraine-like Behavior in Experimental Models of Migraine.
Gong, Q., Lin, Y., Lu, Z.-N., & Xiao, Z.-M. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.10.019 · Cited by 46 · see citing works
Neuroimmune communication in hypertension and obesity: A new therapeutic angle?
de Kloet, A. D., Krause, E. G., Shi, P. D., Zubcevic, J. A., Raizada, M. K., & Sumners, C. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.02.005 · Cited by 45 · see citing works
“Moreover, astrocytes and microglia interact to regulate one another's function and the function of neurons (Kloss et al., 1997; Bezzi et al., 2001a, 2001b; Belanger et al., 2011; Liu et al., 2011).”
Background
Remodeling Microenvironment for Endogenous Repair through Precise Modulation of Chondroitin Sulfate Proteoglycans Following Spinal Cord Injury.
Sun, X., Liu, H.-Q., Tan, Z., Hou, Y., Pang, M., Chen, S., Xiao, L., Yuan, Q., Liu, B., Rong, L., et al. (2022) · Small · doi:10.1002/smll.202205012 · Cited by 45 · see citing works
Physical exercise modulates the astrocytes polarization, promotes myelin debris clearance and remyelination in chronic cerebral hypoperfusion rats
Jiang, T., Luo, J., Pan, X., Zheng, H., Yang, H., Zhang, L., & Hu, X. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119526 · Cited by 50 · see citing works
Hypothalamic Neuropeptide Brain Protection: Focus on Oxytocin
Panaro, M. A., Benameur, T., & Porro, C. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051534 · Cited by 48 · see citing works
“In this regard, microglia also activate astrocytes that in turn can modulate the activation and recruitment of other immunocompetent cells to the injury site, thus contributing to exacerbating the inflammatory picture or, alternatively, to promoting the resolution of the neuroinflammation process [62].”
Background
Environmental Signals on Microglial Function during Brain Development, Neuroplasticity, and Disease
Chagas, L. D. S., Sandre, P. C., Ribeiro, N. C. A. R. E., Marcondes, H., Silva, P. O., Savino, W., & Serfaty, C. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062111 · Cited by 50 · see citing works
“Activated astrocytes not only facilitate activation of distant microglia, but also limit microglial activities [56].”
Background
Activation of sphingosine-1-phosphate receptor 1 in the spinal cord produces mechano-hypersensitivity through the activation of inflammasome and IL-1β pathway
Doyle, T., Chen, Z., Durante, M., & Salvemini, D. (2019) · Journal of Pain · doi:10.1016/j.jpain.2019.02.007 · Cited by 44 · see citing works
The effect of aged microglia on synaptic impairment and its relevance in neurodegenerative diseases
Triviño, J. J., & von Bernhardi, R. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.104982 · Cited by 43 · see citing works
Syringin exerts neuroprotective effects in a rat model of cerebral ischemia through the FOXO3a/NF-κB pathway.
Tan, J.-Y., Luo, J., Meng, C., Jiang, N., Cao, J., & Zhao, J. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.107268 · Cited by 43 · see citing works
Pathological Neuroinflammatory Conversion of Reactive Astrocytes Is Induced by Microglia and Involves Chromatin Remodeling
Villarreal, A., Vidos, C., Busso, M. M., Cieri, M. B., & Ramos, A. J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.689346 · Cited by 47 · see citing works
Gunn rats with glial activation in the hippocampus show prolonged immobility time in the forced swimming test and tail suspension test
Arauchi, R., Hashioka, S., Tsuchie, K., Miyaoka, T., Tsumori, T., Limoa, E., Azis, I. A., Oh‐Nishi, A., Miura, S., Otsuki, K., et al. (2018) · Brain and Behavior · doi:10.1002/brb3.1028 · Cited by 43 · see citing works
Microglia and astroglia: the role of neuroinflammation in lead toxicity and neuronal injury in the brain
Liu, J.-T., Dong, M.-H., Zhang, J.-Q., Bai, Y., Kuang, F., & Chen, L.-W. (2015) · Neuroimmunology and Neuroinflammation · doi:10.4103/2347-8659.156980 · Cited by 42 · see citing works
“The response of microglia and astrocytes to neuroinflammation Liu et al.[18] has proposed that activation of microglia in response to pathological conditions such as trauma, stroke, or neurodegenerative disorders occurs before activation of astrocytes.”
BackgroundInfluential

Authors: Liu, W., Tang, Y., & Feng, J.
Affiliations: Guangzhou University of Chinese Medicine (CN)
Sun Yat-sen University (CN)
Corresponding author: Liu, W.
Tang, Y.
ORCID: Tang, Y.
Venue: Life Sciences
Publisher: Elsevier BV
Published: 2011-08
Volume: 89
Issue: 5-6
Pages: 141-146
ISSN: 0024-3205 (ISSN-L)
DOI: 10.1016/j.lfs.2011.05.011
OpenAlex: W2036224773
Cited by: 303
References: 84
Citations by year: 2026: 11 · 2025: 21 · 2024: 15 · 2023: 11 · 2022: 18 · 2021: 20 · 2020: 35 · 2019: 20 · 2018: 20 · 2017: 24 · 2016: 29 · 2015: 20 · 2014: 15 · 2013: 22 · 2012: 18
FWCI: 1.66
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Life Sciences (publishedVersion)
PubMed (publishedVersion)
Funders: Guangzhou University of Chinese Medicine
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Keywords: microglia, astrocytes, microglial activation, astrocyte activation, central nervous system pathology, neuroinflammation, stroke, traumatic brain injury, neurodegenerative diseases, interleukin-1, adenosine triphosphate, TGF-beta, glial communication
MeSH terms: Animals, Astrocytes, Cell Communication, Central Nervous System Diseases, Humans, Macrophage Activation, Microglia, Calcium Signaling, Receptor Cross-Talk

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Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system

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