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Curcumin alleviates traumatic brain injury induced by gas explosion through modulating gut microbiota and suppressing the LPS/TLR4/MyD88/NF-κB pathway

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Abstract

Gas explosions (GE) are a prevalent and widespread cause of traumatic brain injury (TBI) in coal miners. However, the impact and mechanism of curcumin on GE-induced TBI in rats remain unclear. In this study, we simulated GE-induced TBI in rats and administered curcumin orally at a dose of 100 mg/kg every other day for 7 days to modulate the gut microbiota in TBI rats. We employed 16S rRNA sequencing and LC–MS/MS metabolomic analysis to investigate changes in the intestinal flora and its metabolic profile. Additionally, we utilized ELISA, protein assays, and immunohistochemistry to assess neuroinflammatory signaling molecules for validation. In a rat TBI model, GE resulted in weight loss, pathological abnormalities, and cortical hemorrhage. Treatment with curcumin significantly mitigated histological abnormalities and microscopic mitochondrial structural changes in brain tissue. Furthermore, curcumin treatment markedly ameliorated GE-induced brain dysfunction by reducing the levels of several neuroinflammatory signaling molecules, including neuron-specific enolase, interleukin (IL)-1β, IL-6, and cryptothermic protein 3. Notably, curcumin reshaped the gut microbiome by enhancing evenness, richness, and composition. Prevotella_9, Alloprevotella, Bacilli, Lactobacillales, Proteobacteria, and Gammaproteobacteria were identified as prominent members of the gut microbiota, increasing the linear discriminant analysis scores and specifically enhancing the abundance of bacteria involved in the nuclear factor (NF)-κB signaling pathway, such as Lachnospiraceae and Roseburia. Additionally, there were substantial alterations in serum metabolites associated with metabolic NF-κB signaling pathways in the model group. Curcumin administration reduced serum lipopolysaccharide levels and downregulated downstream Toll-like receptor (TLR)4/myeloid differentiation primary response 88 (MyD88)/NF-κB signaling. Furthermore, curcumin alleviated GE-induced TBI in rats by modulating the gut microbiota and its metabolites. Based on these protective effects, curcumin may exert its influence on the gut microbiota and the TLR4/MyD88/NF-κB signaling pathways to ameliorate GE-induced TBI.

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Data availability

All data used in this study are included in this manuscript.

Abbreviations

H&E:

Hematoxylin and eosin

GE:

Gas explosion

TBI:

Traumatic brain injury

ANOVA:

Analysis of variance

ELISA:

Enzyme-linked immunosorbent assay

LPS:

Lipopolysaccharide

TLR4:

Toll-like receptor 4

MyD88:

Myeloid differentiation primary response 88

NF-κB:

Nuclear factor-kappa beta

NSE:

Neuron-specific enolase

IL-10:

Interleukin-10

IL-1β:

Interleukin-1β

IL-6:

Interleukin-6

NLRP3:

Cryptothermic protein 3

KEGG:

Kyoto Encyclopedia of Genes and Genomes

TNF-α:

Tumor necrosis factor-α

ns:

No significant difference

DEMs:

Differentially expressed metabolites

RDA:

Redundancy analysis

HPLC:

High-pressure liquid chromatography

TEM:

Transmission electron microscopy

DAB:

Diaminobenzidine

PCA:

Principal component analysis

OPLS-DA:

Orthogonal partial least-squares discriminant analysis

PCoA:

Principal sequence analysis

COG:

Orthologous genes

QC:

Quality control

ESI:

Electrospray ionization

VIP:

Variable importance projection

HMDB:

Human metabolome database

CCA:

Canonical correspondence analysis

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Acknowledgements

We thank our team for their valuable assistance, and we would like to thank Wuhan Servicebio Technology Co., Ltd. (http://www.servicebio.cn/) for technical support in the H&E and IHC assays of brain tissues. We would also like to thank the Shanghai OE Biotech Co., Ltd. and the Shanghai Luming Biological Technology Co., Ltd. for their assistance in the analysis of metabolome and transcriptome data. Moreover, we thank the technical platforms BMKCloud (www.biocloud.net), Wekemo Bioincloud (www.bioincloud.tech/), and Personalbio GenesCloud (www.genescloud.cn/) for their analysis support in the combined analysis of multiple omics and environmental factor researches.

Funding

This work was supported by the National Natural Science Foundation of China (grant numbers U2004102 and U1904209), the Science and Technology Project of Henan Province (grant number 232102311071), and the Natural Science Foundation of Henan Province (grant number 202300410312).

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Authors and Affiliations

  1. Department of Environmental and Occupational Health, School of Public Health, Xinxiang Medical University, Xinxiang, 453003, Henan, China

    Xinwen Dong, Lvfei Deng, Yaguang Su, Xiaofeng Han, Sanqiao Yao, Weidong Wu & Yichun Bai

  2. Institute of Toxicology, College of Preventive Medicine, Army Medical University, Chongqing, 400038, China

    Jia Cao

  3. Institute of Trauma and Orthopedics, Xinxiang Medical University, Xinxiang, 453003, Henan, China

    Linqiang Tian

  4. Department of Pathology, The Fifth Affiliated Hospital of Zhengzhou University, Zhengzhou, 450052, Henan, China

    Guizhi Wang

  5. Institutes of Health Central Plains, Xinxiang Medical University, 601 Jinsui Street Xinxiang, Henan, 453003, China

    Wenjie Ren

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Contributions

XD: investigation and writing—original draft. WW: writing—original draft. LD, YS, and XH: formal analysis, software, supervision, and validation. YB: data testing and analysis. SY: funding acquisition. GW participated in an experiment. JC and LT provided experimental materials. WR: writing—review and editing and supervision. All authors contributed to the article and approved the submitted version.

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Correspondence to Wenjie Ren.

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This study was approved by the Zoology Animal and Medical Ethics Committee of Xinxiang Medical University (No. XYLL-2020007). Ethical treatment of animals was ensured, and the study was performed in line with ethical standards to protect the welfare of animals involved in research.

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Dong, X., Deng, L., Su, Y. et al. Curcumin alleviates traumatic brain injury induced by gas explosion through modulating gut microbiota and suppressing the LPS/TLR4/MyD88/NF-κB pathway. Environ Sci Pollut Res 31, 1094–1113 (2024). https://doi.org/10.1007/s11356-023-30708-0

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