Cited by 334Advanced Glycation End Products researchNeuroinflammation and Neurodegeneration MechanismsImmune Response and Inflammation

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DAMP Signaling is a Key Pathway Inducing Immune Modulation after Brain Injury

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Liesz, Arthur, Dalpke, Alexander, Mracsko, Eva, Roth, Stefan, Zhou, Wei, Yang, Huan, Na, Shin-Young, Akhisaroglu, Mustafa, Fleming, Thomas, Eigenbrod, Tatjana, Nawroth, Peter P., Tracey, Kevin J., Veltkamp, Roland·2015·The Journal of Neuroscience

DOI 10.1523/jneurosci.2439-14.2015PMC PMC4293412

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Abstract

Acute brain lesions induce profound alterations of the peripheral immune response comprising the opposing phenomena of early immune activation and subsequent immunosuppression. The mechanisms underlying this brain-immune signaling are largely unknown. We used animal models for experimental brain ischemia as a paradigm of acute brain lesions and additionally investigated a large cohort of stroke patients. We investigated the inflammatory potency of HMGB1 and its signaling pathways by immunological in vivo and in vitro techniques. Features of the complex behavioral sickness behavior syndrome were characterized by homecage behavior analysis. HMGB1 downstream signaling, particularly with RAGE, was studied in various transgenic animal models and by pharmacological blockade. Our results indicate that HMGB1 was released from the ischemic brain in the hyperacute phase of stroke in mice and patients. Cytokines secreted in the periphery in response to brain injury induced sickness behavior, which could be abrogated by inhibition of the HMGB1-RAGE pathway or direct cytokine neutralization. Subsequently, HMGB1-release induced bone marrow egress and splenic proliferation of bone marrow-derived suppressor cells, inhibiting the adaptive immune responses in vivo and vitro. Furthermore, HMGB1-RAGE signaling resulted in functional exhaustion of mature monocytes and lymphopenia, the hallmarks of immune suppression after extensive ischemia. This study introduces the HMGB1-RAGE-mediated pathway as a key mechanism explaining the complex postischemic brain-immune interactions.

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Authors: Liesz, A., Dalpke, A., Mracsko, E., Roth, S., Zhou, W., Yang, H., Na, S.-Y., Akhisaroglu, M., Fleming, T., Eigenbrod, T., Nawroth, P. P., Tracey, K. J., & Veltkamp, R.
Affiliations: Heidelberg University (DE)
LMU Klinikum (DE)
Feinstein Institute for Medical Research (US)
ORCID: Liesz, Arthur
Dalpke, Alexander
Mracsko, Eva
Roth, Stefan
Zhou, Wei
Yang, Huan
Fleming, Thomas
Eigenbrod, Tatjana
Nawroth, Peter P.
Tracey, Kevin J.
Veltkamp, Roland
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2015-01-14
Volume: 35
Issue: 2
Pages: 583-598
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.2439-14.2015
PMC: PMC4293412
OpenAlex: W2128591402
Cited by: 334
References: 56
Citations by year: 2026: 25 · 2025: 23 · 2024: 24 · 2023: 26 · 2022: 39 · 2021: 31 · 2020: 31 · 2019: 33 · 2018: 32 · 2017: 16 · 2016: 33 · 2015: 21
FWCI: 27.74
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
Deutsche Forschungsgemeinschaft (SFB1118)
Medical Research Council (MR/L006758/1)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: HMGB1, RAGE, ischemic stroke, brain injury, sickness behavior, immunosuppression, suppressor cells, lymphopenia, cytokines
MeSH terms: Receptor for Advanced Glycation End Products, Adult, Aged, Aged, 80 and over, Animals, Bone Marrow, Female, Humans, Male, Mice, Inbred C57BL, Middle Aged, Receptors, Immunologic, Spleen, T-Lymphocytes, Signal Transduction, Case-Control Studies, Cytokines, Protein Isoforms, Infarction, Middle Cerebral Artery, Stroke, HMGB1 Protein, Mice

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DAMP Signaling is a Key Pathway Inducing Immune Modulation after Brain Injury

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