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Targeting Ferroptosis Promotes Functional Recovery by Mitigating White Matter Injury Following Acute Carbon Monoxide Poisoning

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Abstract

Survivors experiencing acute carbon monoxide poisoning (ACMP) tend to develop white matter injury (WMI). The mechanism of ACMP-induced WMI remains unclear. Considering the role of ferroptosis in initiating oligodendrocyte damage to deteriorate WMI, exploring therapeutic options to attenuate ferroptosis is a feasible approach to alleviating WMI. Our results indicated that ACMP induced accumulation of iron and reactive oxygen species (ROS) eventually leading to WMI and motor impairment after ACMP. Furthermore, ferrostatin-1 reduced iron and ROS deposition to alleviate ferroptosis, thereafter reducing WMI to promote the recovery of motor function. The nuclear factor erythroid-related factor 2 (Nrf2)/heme oxygenase-1 (HO-1) signaling pathway was found to be involved in alleviating ferroptosis as seen with the administration of ferrostatin-1. The present study rationalizes that targeting ferroptosis to alleviate WMI is a feasible therapeutic strategy for managing ACMP.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

ACMP:

Acute carbon monoxide poisoning

MRI:

Magnetic resonance imaging

WMI:

White matter injury

RCD:

Regulated cell death

ROS:

Reactive oxygen species

CNS:

Central nervous system

SCI:

Spinal cord injury

CIS:

Cerebral ischemic stroke

ICH:

Intracerebral hemorrhage

TBI:

Traumatic brain injury

SAH:

Subarachnoid hemorrhage

IREB2:

Iron-responsive element binding protein 2

PTGS2:

Prostaglandin-endoperoxide synthase 2

LFB:

Luxol fast blue

OFT:

Open field test

BMT:

Beam walking test

Hb:

Hemoglobin

PBS:

Phosphate-buffered solution

DHE:

Dihydroethidium

MDA:

Malondialdehyde

IF:

Immunofluorescent

IHC:

Immunohistochemistry

BSA:

Bovine serum albumin

BCA:

Bicinchoninic acid

TEM:

Transmission electron microscopy

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Funding

This research was supported by grants obtained from the National Natural Science Foundation of China (grant number 82060245), the Chinese Ministry of Education (grant number 2020–39), and the Science and Technology Project of Guizhou Province (grant number [2020]4Y149).

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  1. Shuhong Wang and Binyuan Xiong contributed equally to the manuscript.

Authors and Affiliations

  1. Department of Emergency, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou, 563000, China

    Shuhong Wang, Binyuan Xiong, Quan Hu, Xuheng Jiang, Ji Zhang, Lin Chen, Ruilie Wang, Mo Li, Xin Zhou, Tianxi Zhang, Hongfei Ge & Anyong Yu

  2. Department of Cardiology, The First People’s Hospital of Zunyi, Zunyi, Guizhou, 133012, China

    Yin Tian

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Contributions

Anyong Yu, Hongfei Ge, and Tianxi Zhang designed this research. Shuhong Wang, Binyuan Xiong, Yin Tian, Quan Hu, Xuheng Jiang, and Ji Zhang performed the experiments. Mo Li and Xin Zhou analyzed the data. Ruilie Wang provided technical support. Shuhong Wang wrote a preliminary draft of the manuscript. Hongfei Ge, Anyong Yu, and Tianxi Zhang designed the experiments and revised the manuscript. Anyong Yu made the hypothesis. All authors discussed and approved the final version of the manuscript.

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Correspondence to Tianxi Zhang, Hongfei Ge or Anyong Yu.

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All procedures were approved by the local authorities of Zunyi Medical University for the laboratory use of animals (approve no. KLLY(A)-2021–033). The Ethics Committee of the Affiliated Hospital of Zunyi Medical University supervised all the procedures. All experimental procedures were performed according to China’s animal welfare legislation for the protection of animals used for scientific purposes.

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Wang, S., Xiong, B., Tian, Y. et al. Targeting Ferroptosis Promotes Functional Recovery by Mitigating White Matter Injury Following Acute Carbon Monoxide Poisoning. Mol Neurobiol 61, 1157–1174 (2024). https://doi.org/10.1007/s12035-023-03603-5

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