Microglia drive transient insult-induced brain injury by chemotactic recruitment of CD8+ T lymphocytes
The crosstalk between the nervous and immune systems has gained increasing attention for its emerging role in neurological diseases. Radiation-induced brain injury (RIBI) remains the most common medical complication of cranial radiotherapy, and its pathological mechanisms have yet to be elucidated....
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| Published in | Neuron (Cambridge, Mass.) Vol. 111; no. 5; pp. 696 - 710.e9 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.03.2023
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The crosstalk between the nervous and immune systems has gained increasing attention for its emerging role in neurological diseases. Radiation-induced brain injury (RIBI) remains the most common medical complication of cranial radiotherapy, and its pathological mechanisms have yet to be elucidated. Here, using single-cell RNA and T cell receptor sequencing, we found infiltration and clonal expansion of CD8+ T lymphocytes in the lesioned brain tissues of RIBI patients. Furthermore, by strategies of genetic or pharmacologic interruption, we identified a chemotactic action of microglia-derived CCL2/CCL8 chemokines in mediating the infiltration of CCR2+/CCR5+ CD8+ T cells and tissue damage in RIBI mice. Such a chemotactic axis also participated in the progression of cerebral infarction in the mouse model of ischemic injury. Our findings therefore highlight the critical role of microglia in mediating the dysregulation of adaptive immune responses and reveal a potential therapeutic strategy for non-infectious brain diseases.
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•Combined scRNA and TCR sequencing of human brain tissues with injury•Infiltrated CD8+ T cells participate in radiation-induced and ischemic brain injuries•Disease-associated microglial cluster featured with CCL2 and CCL8 expression•Microglia-derived CCL2/CCL8 mediate brain infiltration of CD8+ T cells
Using single-cell transcriptomic and immune repertoire sequencing, Shi et al. identify a chemotactic action mediated by microglia-derived CCL2/CCL8 chemokines in recruiting CD8+ T cells. These cause brain injuries in radiation-induced brain injury and ischemic stroke models, providing mechanistic insight and a potential therapeutic strategy for non-infectious brain diseases. |
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| AbstractList | The crosstalk between the nervous and immune systems has gained increasing attention for its emerging role in neurological diseases. Radiation-induced brain injury (RIBI) remains the most common medical complication of cranial radiotherapy, and its pathological mechanisms have yet to be elucidated. Here, using single-cell RNA and T cell receptor sequencing, we found infiltration and clonal expansion of CD8
T lymphocytes in the lesioned brain tissues of RIBI patients. Furthermore, by strategies of genetic or pharmacologic interruption, we identified a chemotactic action of microglia-derived CCL2/CCL8 chemokines in mediating the infiltration of CCR2
/CCR5
CD8
T cells and tissue damage in RIBI mice. Such a chemotactic axis also participated in the progression of cerebral infarction in the mouse model of ischemic injury. Our findings therefore highlight the critical role of microglia in mediating the dysregulation of adaptive immune responses and reveal a potential therapeutic strategy for non-infectious brain diseases. The crosstalk between the nervous and immune systems has gained increasing attention for its emerging role in neurological diseases. Radiation-induced brain injury (RIBI) remains the most common medical complication of cranial radiotherapy, and its pathological mechanisms have yet to be elucidated. Here, using single-cell RNA and T cell receptor sequencing, we found infiltration and clonal expansion of CD8+ T lymphocytes in the lesioned brain tissues of RIBI patients. Furthermore, by strategies of genetic or pharmacologic interruption, we identified a chemotactic action of microglia-derived CCL2/CCL8 chemokines in mediating the infiltration of CCR2+/CCR5+ CD8+ T cells and tissue damage in RIBI mice. Such a chemotactic axis also participated in the progression of cerebral infarction in the mouse model of ischemic injury. Our findings therefore highlight the critical role of microglia in mediating the dysregulation of adaptive immune responses and reveal a potential therapeutic strategy for non-infectious brain diseases. [Display omitted] •Combined scRNA and TCR sequencing of human brain tissues with injury•Infiltrated CD8+ T cells participate in radiation-induced and ischemic brain injuries•Disease-associated microglial cluster featured with CCL2 and CCL8 expression•Microglia-derived CCL2/CCL8 mediate brain infiltration of CD8+ T cells Using single-cell transcriptomic and immune repertoire sequencing, Shi et al. identify a chemotactic action mediated by microglia-derived CCL2/CCL8 chemokines in recruiting CD8+ T cells. These cause brain injuries in radiation-induced brain injury and ischemic stroke models, providing mechanistic insight and a potential therapeutic strategy for non-infectious brain diseases. |
| Author | Li, Honghong Cheng, Jinping Lin, Wei-Jye Hu, Xia Li, Yi Tang, Yamei Wu, Long-Jun Jiang, Jingru Xie, Jiatian Xu, Yongteng Chen, Jiongxue Zeng, Junbo Yang, Yuhua Shi, Zhongshan Chen, Sitai Yu, Pei Liu, Qiang Zhang, Zhan Mei, Jinghong Huang, Jialin Ko, Ho Li, Shaojian He, Baixuan Chen, Siqi Cai, Jinhua |
| Author_xml | – sequence: 1 givenname: Zhongshan surname: Shi fullname: Shi, Zhongshan organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 2 givenname: Pei surname: Yu fullname: Yu, Pei organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 3 givenname: Wei-Jye surname: Lin fullname: Lin, Wei-Jye organization: Brain Research Center, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 4 givenname: Sitai surname: Chen fullname: Chen, Sitai organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 5 givenname: Xia surname: Hu fullname: Hu, Xia organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 6 givenname: Siqi surname: Chen fullname: Chen, Siqi organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 7 givenname: Jinping surname: Cheng fullname: Cheng, Jinping organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 8 givenname: Qiang surname: Liu fullname: Liu, Qiang organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 9 givenname: Yuhua surname: Yang fullname: Yang, Yuhua organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 10 givenname: Shaojian surname: Li fullname: Li, Shaojian organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 11 givenname: Zhan surname: Zhang fullname: Zhang, Zhan organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 12 givenname: Jiatian surname: Xie fullname: Xie, Jiatian organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 13 givenname: Jingru surname: Jiang fullname: Jiang, Jingru organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 14 givenname: Baixuan surname: He fullname: He, Baixuan organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 15 givenname: Yi surname: Li fullname: Li, Yi organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 16 givenname: Honghong surname: Li fullname: Li, Honghong organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 17 givenname: Yongteng surname: Xu fullname: Xu, Yongteng organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 18 givenname: Junbo surname: Zeng fullname: Zeng, Junbo organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 19 givenname: Jialin surname: Huang fullname: Huang, Jialin organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 20 givenname: Jinghong surname: Mei fullname: Mei, Jinghong organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 21 givenname: Jinhua surname: Cai fullname: Cai, Jinhua organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 22 givenname: Jiongxue surname: Chen fullname: Chen, Jiongxue organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China – sequence: 23 givenname: Long-Jun surname: Wu fullname: Wu, Long-Jun organization: Department of Neurology & Department of Immunology, Mayo Clinic, Rochester, MN 55905, USA – sequence: 24 givenname: Ho surname: Ko fullname: Ko, Ho organization: Division of Neurology, Department of Medicine and Therapeutics & Li Ka Shing Institute of Health Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China – sequence: 25 givenname: Yamei orcidid: 0000-0002-6353-6107 surname: Tang fullname: Tang, Yamei email: tangym@mail.sysu.edu.cn organization: Department of Neurology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou 510120, China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36603584$$D View this record in MEDLINE/PubMed |
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| Keywords | radiation-induced brain injury CD8+ T cell microglia ischemic stroke chemoattraction CD8(+) T cell |
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| SubjectTerms | Animals Brain - metabolism Brain Injuries - pathology CD8+ T cell CD8-Positive T-Lymphocytes - metabolism chemoattraction Chemokine CCL2 - metabolism ischemic stroke Mice Mice, Inbred C57BL microglia Microglia - physiology radiation-induced brain injury |
| Title | Microglia drive transient insult-induced brain injury by chemotactic recruitment of CD8+ T lymphocytes |
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