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SIRT1-Mediated HMGB1 Deacetylation Suppresses Neutrophil Extracellular Traps Related to Blood–Brain Barrier Impairment After Cerebral Venous Thrombosis

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Abstract

Cerebral venous thrombosis (CVT) is a neurovascular disease with recently increasing incidence. Aseptic inflammatory responses play an important role in the pathology of CVT. Recent studies report that neutrophil extracellular traps (NETs) are major triggers of thrombosis and inflammation in stroke, but their effect on brain injury in CVT requires further validation. In this study, two CVT animal models were used to simulate superior sagittal sinus thrombosis and cortical vein thrombosis. The effects of brain tissue infiltration of NETs and the molecular mechanisms associated with NET formation were deeply explored in combination with proteomics, histology, and serology. The results showed that the cortical vein thrombosis model could be combined with more severe blood–brain barrier (BBB) disruption and showed more severe cerebral hemorrhage. Decreased Sirtuin 1 (SIRT1) expression promotes high mobility group box 1 (HMGB1) acetylation, causing increased cytosolic translocation and extracellular release, and HMGB1 can promote NET formation and recruitment. In addition, corticocerebral accumulation of NETs contributes to BBB damage. This establishes a vicious cycle between BBB damage and NET accumulation. SIRT1 mediated-HMGB1 deacetylation may play a critical role in attenuating BBB damage following CVT. This study employed a combined validation using models of venous sinus thrombosis and cortical vein thrombosis to investigate the deacetylation role of SIRT1, aiming to offer new insights into the pathological mechanisms of brain injury following CVT.

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Data Availability

The datasets generated and/or analyzed for the present study are available from the corresponding authors on reasonable request.

Abbreviations

ADC :

Apparent diffusion coefficient

BBB :

Blood-brain barrier

CV :

Cortical vein

CVT :

Cerebral venous thrombosis

CitH3 :

Citrullinated histone H3

COVID :

Coronavirus disease

DAPI :

4′,6-Diamidino-2-phenylindole

DMSO :

Dimethyl sulfoxide

DNase :

Deoxyribonuclease

DWI :

Diffusion-weighted imaging

ELISA :

Enzyme‑linked immunosorbent assay

EB :

Evans blue

GO :

Gene Ontology

HE :

Hematoxylin and eosin

HMGB1 :

High mobility group box 1

IL :

Interleukin

IP :

Immunoprecipitation

KEGG :

Kyoto Encyclopedia of Genes and Genomes

MPO :

Myeloperoxidase

NAD :

Nicotinamide adenosine dinucleotide

NET :

Neutrophil extracellular trap

OD :

Optical density

PBS :

Phosphate-buffered saline

SD :

Standard deviation

SDS :

Sodium dodecyl sulfate

SIRT1 :

Sirtuin 1

SMA :

Smooth muscle actin

SSS :

Superior sagittal sinus

TUNEL :

Terminal deoxynucleotidyl transferase dUTP nick-end labeling

WB :

Western blotting

ZO :

Zonula occludens

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Acknowledgements

Sincere appreciation is given to the teachers and our colleagues from Fuzong Clinical Medical College, who participated in this study with great cooperation.

Funding

This study was supported by Joint Funds for the Innovation of Science and Technology, Fujian province (no. 2019Y9045); Joint Funds for the Innovation of Science and Technology, Fujian province (no. 2019Y9042); China Postdoctoral Science Foundation (no. 2021M693955); and Startup Fund for Scientific Research at Fujian Medical University (no. 2020QH2040).

Author information

Author notes

  1. Shuwen Mu, Ziqi Li and Long Lin contributed equally to this work.

Authors and Affiliations

  1. Department of Neurosurgery, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou, 350025, China

    Shuwen Mu, Long Lin, Li Chen, Liang Xian, Kunzhe Lin & Shousen Wang

  2. Department of Neurosurgery, School of Medicine, Dongfang Affiliated Hospital of Xiamen University, Xiamen University, Xiamen, 361005, China

    Ziqi Li

  3. Department of Molecular Pathology, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, 350014, China

    Di Wang

  4. Department of Anesthesiology and Perioperative Medicine, 900th Hospital, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou, 350025, China

    Fei Yang

  5. Fujian University of Traditional Chinese Medicine, Fuzhou, 350122, China

    Yinghong Lin, Dan Ye & Yang Yang

  6. Department of Neurosurgery, 900th Hospital, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou, 350025, China

    Liangfeng Wei & Shousen Wang

  7. Laboratory of Basic Medicine, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou, 350025, China

    Yongjun Xu

  8. Laboratory of Basic Medicine, 900th Hospital, Fuzong Clinical Medical College of Fujian Medical University, Fuzhou, 350025, China

    Yongjun Xu

Authors
  1. Shuwen Mu
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  2. Ziqi Li
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  3. Long Lin
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  4. Di Wang
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  5. Fei Yang
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  6. Li Chen
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  7. Liang Xian
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  8. Kunzhe Lin
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  9. Yinghong Lin
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  10. Dan Ye
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  11. Yang Yang
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  12. Liangfeng Wei
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  13. Yongjun Xu
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  14. Shousen Wang
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Contributions

S.W., Y.X., and S.M. were responsible for the study concept and design. S.M., L.L., and L.X. performed animal model operation. S.M., Z.L., L.L., L.C., Y.L., D.Y., K.L., and Y.Y. performed the proteomic, histological, and serological experiments. S.M., D.W., F.Y., and L.W. were responsible for the data analyses. S.W. and Z.L. drafted the manuscript. S.W. and Y.X. critically reviewed the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Yongjun Xu or Shousen Wang.

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Ethics Approval

This experiment was approved by the Animal Care and Use Committee of Fujian Medical University (2020–051) and was conducted in accordance with the Guide for the Care and Use of Laboratory Animals.

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The authors declare no competing interests.

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Mu, S., Li, Z., Lin, L. et al. SIRT1-Mediated HMGB1 Deacetylation Suppresses Neutrophil Extracellular Traps Related to Blood–Brain Barrier Impairment After Cerebral Venous Thrombosis. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-03959-2

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