Bone marrow–derived emergency monopoiesis drives brain–lung axis injury after traumatic brain injury via IL-1

Traumatic brain injury (TBI) presents a major clinical burden, often resulting in both acute neurological impairment and pulmonary dysfunction, underscoring the complex and poorly understood brain-lung axis. Although dual-organ injury is well-documented, the mechanistic basis linking brain trauma to peripheral organ damage has remained elusive. In this study, we integrate clinical observations, single-cell RNA sequencing of skull bone marrow (BM) from TBI patients, and preclinical mouse models to uncover a rapid, IL-1-driven emergency monopoiesis response initiated within 24 h post-injury. We demonstrate that TBI induces accelerated, myeloid-skewed hematopoiesis in the cranial BM, marked by the expansion and mobilization of proinflammatory monocytes. This immune activation correlates strongly with both neurological decline and acute lung injury. Mechanistically, we identify IL-1 signaling as a master regulator of this pathological hematopoietic reprogramming. Disruption of IL-1R1 signaling, either globally or selectively within the hematopoietic compartment, attenuates emergency monopoiesis, preserves blood-brain barrier integrity, and reduces inflammatory infiltration in both the brain and lungs. These findings establish emergency monopoiesis as a central driver of multi-organ injury in TBI and reveal the BM niche as a critical yet underappreciated target in post-traumatic systemic pathology. By targeting IL-1R1-dependent hematopoietic activation, this study proposes a novel therapeutic strategy to interrupt the harmful brain-lung immune crosstalk and improve clinical outcomes in acute TBI.

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Publication Details

Journal
Journal of Neuroinflammation
Published
2025-11-05
DOI
https://doi.org/10.1186/s12974-025-03589-y
Primary Topic
Neuroinflammation and Neurodegeneration Mechanisms
Type
article
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article

Bone marrow–derived emergency monopoiesis drives brain–lung axis injury after traumatic brain injury via IL-1

Jieli Chen, Zhigang Cai, Yafan Liu, Kaibin Shi et al.
Journal of Neuroinflammation
Neuroinflammation and Neurodegeneration Mechanisms
article

Bone marrow–derived emergency monopoiesis drives brain–lung axis injury after traumatic brain injury via IL-1

Jieli Chen, Zhigang Cai, Yafan Liu, Kaibin Shi, Zhuyu Gao, Jianning Zhang, Yichi Zhang, Ying Fu, Tianrui Ma, Yang Li, Jingjing Liu, Tao Zhu, Rui Li, Zilong Zhao, Jie Lin, Zijian Zhou, Kaifeng Pang, Hao Zhang, Lujia Tang, Lorie Chen Cai
article en

Abstract

Traumatic brain injury (TBI) presents a major clinical burden, often resulting in both acute neurological impairment and pulmonary dysfunction, underscoring the complex and poorly understood brain-lung axis. Although dual-organ injury is well-documented, the mechanistic basis linking brain trauma to peripheral organ damage has remained elusive. In this study, we integrate clinical observations, single-cell RNA sequencing of skull bone marrow (BM) from TBI patients, and preclinical mouse models to uncover a rapid, IL-1-driven emergency monopoiesis response initiated within 24 h post-injury. We demonstrate that TBI induces accelerated, myeloid-skewed hematopoiesis in the cranial BM, marked by the expansion and mobilization of proinflammatory monocytes. This immune activation correlates strongly with both neurological decline and acute lung injury. Mechanistically, we identify IL-1 signaling as a master regulator of this pathological hematopoietic reprogramming. Disruption of IL-1R1 signaling, either globally or selectively within the hematopoietic compartment, attenuates emergency monopoiesis, preserves blood-brain barrier integrity, and reduces inflammatory infiltration in both the brain and lungs. These findings establish emergency monopoiesis as a central driver of multi-organ injury in TBI and reveal the BM niche as a critical yet underappreciated target in post-traumatic systemic pathology. By targeting IL-1R1-dependent hematopoietic activation, this study proposes a novel therapeutic strategy to interrupt the harmful brain-lung immune crosstalk and improve clinical outcomes in acute TBI.

Journal of NeuroinflammationVol. 22(1)
Fujian Medical University (CN), Capital Medical University (CN), Tianjin Medical University General Hospital (CN), Tianjin Huanhu Hospital (CN), Ministry of Education (KR), First Affiliated Hospital of Fujian Medical University (CN), Ministry of Science and Technology (LA), Tianjin Medical University (CN)
Openalex Percentile: Top 60%
Neuroinflammation and Neurodegeneration Mechanisms
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