M1-type polarized macrophage contributes to brain damage through CXCR3.2/CXCL11 pathways after RGNNV infection in grouper

ABSTRACT

The vertebrate central nervous system (CNS) is the most complex system of the body. The CNS, especially the brain, is generally regarded as immune-privileged. However, the specialized immune strategies in the brain and how immune cells, specifically macrophages in the brain, respond to virus invasion remain poorly understood. Therefore, this study aimed to examine the potential immune response of macrophages in the brain of orange-spotted groupers (Epinephelus coioides) following red-spotted grouper nervous necrosis virus (RGNNV) infection. We observed that RGNNV induced macrophages to produce an inflammatory response in the brain of orange-spotted grouper, and the macrophages exhibited M1-type polarization after RGNNV infection. In addition, we found RGNNV-induced macrophage M1 polarization via the CXCR3.2- CXCL11 pathway. Furthermore, we observed that RGNNV triggered M1 polarization in macrophages, resulting in substantial proinflammatory cytokine production and subsequent damage to brain tissue. These findings reveal a unique mechanism for brain macrophage polarization, emphasizing their role in contributing to nervous tissue damage following viral infection in the CNS.

KEYWORDS:

• Central nervous system
• RGNNV
• macrophage
• CXCR3.2
• proinflammatory

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author’ contributions

Qing Wang: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Writing – original draft. Weiqi Qin: Conceptualization, Funding acquisition, Project administration, Validation, Writing – review & editing. Huihong Zhao: Data curation, Writing – review & editing. Kaishan Liang: Formal analysis, Methodology, Writing – original draft. Minlin Zhang: Formal analysis, Investigation, Methodology, Software. Jiantao Liang: Investigation. Xiaoling Zuo: Formal analysis, Investigation, Software, Validation. Xianze Jia: Methodology. Jinhong Shan: Methodology. Songyong Gan: Methodology. Ding Liu: Methodology. Zongyang Li: Investigation, Methodology. Jie Yu: Software. Zijie Xuan: Methodology. Liyuan Luo: Methodology.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors without undue reservation to any qualified researcher. The raw data in DOI: 10.17632/f5gd8tsgy9.1.

Ethics statement

All relevant ethical safeguards were met for animal experimentation, and all animal experiments in this study were approved by the Animal Care and Use Committee of the College of Marine Sciences, South China Agricultural University.

Supplemental data

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2024.2355971

Additional information

Funding

This work was supported by the grants from the National Natural Science Foundation of China [42176103, U20A20102], the National Key Research and Development Program of China [2022YFD2400502], the Guangdong Provincial Natural Science Foundation [2022A1515012505], The talent team tender grant of Zhanjiang marine equipment and biology [2021E05035].