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Increased sympathetic outflow induced by emotional stress aggravates myocardial ischemia–reperfusion injury via activation of TLR7/MyD88/IRF5 signaling pathway

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Abstract

Background and objective

Emotional stress substantially increases the risk of ischemic cardiovascular diseases. Previous study indicates that sympathetic outflow is increased under emotional stress. We aim to investigate the role of increased sympathetic outflow induced by emotional stress in myocardial ischemia–reperfusion (I/R) injury, and explore the underlying mechanisms.

Methods and Results

We used Designer Receptors Exclusively Activated by Designer Drugs technique to activate the ventromedial hypothalamus (VMH), a critical emotion-related nucleus. The results revealed that emotional stress stimulated by VMH activation increased sympathetic outflow, enhanced blood pressure, aggravated myocardial I/R injury, and exacerbated infarct size. The RNA-seq and molecular detection demonstrated that toll-like receptor 7 (TLR7), myeloid differentiation factor 88 (MyD88), interferon regulatory factor 5 (IRF5), and downstream inflammatory markers in cardiomyocytes were significantly upregulated. Emotional stress-induced sympathetic outflow further exacerbated the disorder of the TLR7/MyD88/IRF5 inflammatory signaling pathway. While inhibition of the signaling pathway partially alleviated myocardial I/R injury aggravated by emotional stress-induced sympathetic outflow.

Conclusion

Increased sympathetic outflow induced by emotional stress activates TLR7/MyD88/IRF5 signaling pathway, ultimately aggravating I/R injury.

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Data availability

The datasets used and/or analyzed during this study are available from the corresponding author upon reasonable request. Requests to access these datasets should be directed to Prof. Hong Jiang, hong-jiang@whu.edu.cn.

Abbreviations

ANS:

Autonomic nervous system

BP:

Blood pressure

CAT:

Catalase

CNO:

Clozapine-N-oxide

c-TnT:

Cardiac troponin T

CVDs:

Cardiovascular diseases

ECG:

Electrocardiogram

ERP:

Effective refractory period

FPKM:

Fragments per kilobase million

GSH:

Glutathione

HF:

High frequency

HR:

Heart rate

HRV:

Heart rate variability

I/R:

Ischemia/reperfusion

IRF5:

Interferon regulatory factor 5

KEGG:

Kyoto Encyclopedia of Genes and Genomes

LDH:

Lactate dehydrogenase

LF:

Low frequency

LV:

Left ventricle

MDA:

Malondialdehyde

MyD88:

Myeloid differentiation factor 88

NE:

Norepinephrine

PRV-RFP:

Pseudo-rabies virus carrying red fluorescent protein

PVN:

Paraventricular nucleus

qRT-PCR:

Quantitative real-time PCR

RNA-seq:

RNA sequencing

SCG:

Superior cervical ganglion

SNS:

Sympathetic nervous system

SOD:

Superoxide dismutase

TLR7:

Toll-like receptor 7

VMH:

Ventromedial hypothalamus

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Funding

This work was supported by the grants from National Natural Science Foundation of China (No. 81871486, 81970287, 82100530), and the Foundation for Innovative Research Groups of Natural Science Foundation of Hubei Province, China (2021CFA010).

Author information

Author notes

  1. Zhihao Liu, Zihan Liu and Huixin Zhou have contributed equally to this study.

Authors and Affiliations

  1. Department of Cardiology, Renmin Hospital of Wuhan University, No. 238 Jiefang Road, Wuchang District, Wuhan, 430060, Hubei, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  2. Institute of Molecular Medicine, Renmin Hospital of Wuhan University, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  3. Hubei Key Laboratory of Autonomic Nervous System Modulation, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  4. Taikang Center for Life and Medical Sciences, Wuhan University, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  5. Cardiac Autonomic Nervous System Research Center of Wuhan University, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  6. Hubei Key Laboratory of Cardiology, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

  7. Cardiovascular Research Institute, Wuhan University, Wuhan, 430060, People’s Republic of China

    Zhihao Liu, Zihan Liu, Huixin Zhou, Yuyang Zhou, Xiao Xu, Zeyan Li, Fuding Guo, Yuhong Wang, Zhen Zhou, Liping Zhou, Yueyi Wang, Xiaoya Zhou, Hao Xia & Hong Jiang

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  1. Zhihao Liu
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Contributions

ZL, HJ, HX and XZ designed the study. ZL, ZL, HZ, YZ, XX, and ZL conducted the study. ZL HZ, FG, YW, and ZZ analyzed the data. ZL, ZL, LZ and YW drafted the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Xiaoya Zhou, Hao Xia or Hong Jiang.

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All experimental protocols in this study were approved by the Animal Ethics Committee of Wuhan University under approval number SY2019-030.

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Liu, Z., Liu, Z., Zhou, H. et al. Increased sympathetic outflow induced by emotional stress aggravates myocardial ischemia–reperfusion injury via activation of TLR7/MyD88/IRF5 signaling pathway. Inflamm. Res. 72, 901–913 (2023). https://doi.org/10.1007/s00011-023-01708-0

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