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Neuropilin-1high monocytes protect against neonatal inflammation

Cellular & Molecular Immunology (2024)Cite this article

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Abstract

Neonates are susceptible to inflammatory disorders such as necrotizing enterocolitis (NEC) due to their immature immune system. The timely appearance of regulatory immune cells in early life contributes to the control of inflammation in neonates, yet the underlying mechanisms of which remain poorly understood. In this study, we identified a subset of neonatal monocytes characterized by high levels of neuropilin-1 (Nrp1), termed Nrp1high monocytes. Compared with their Nrp1low counterparts, Nrp1high monocytes displayed potent immunosuppressive activity. Nrp1 deficiency in myeloid cells aggravated the severity of NEC, whereas adoptive transfer of Nrp1high monocytes led to remission of NEC. Mechanistic studies showed that Nrp1, by binding to its ligand Sema4a, induced intracellular p38-MAPK/mTOR signaling and activated the transcription factor KLF4. KLF4 transactivated Nos2 and enhanced the production of nitric oxide (NO), a key mediator of immunosuppression in monocytes. These findings reveal an important immunosuppressive axis in neonatal monocytes and provide a potential therapeutic strategy for treating inflammatory disorders in neonates.

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Fig. 1: Identification of Nrp1high monocytes in neonates.
Fig. 2: Nrp1high monocytes display strong immunosuppressive effects.
Fig. 3: Transcriptional and chromatin accessibility profiling of Nrp1high monocytes.
Fig. 4: Ligation of Nrp1-Sema4a induces p38-MAPK/mTORC1 signaling in monocytes.
Fig. 5: The KLF4-NOS2 axis contributes to the immunosuppressive function of Nrp1high monocytes.
Fig. 6: The presence of Nrp1 in monocytes plays a protective role in neonatal inflammation.

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Data availability

All data reported in this paper will be shared by the lead contact upon reasonable request. The current bulk RNA-seq, ATAC-seq and scRNA-seq data have been deposited in the NCBI Gene Expression Omnibus database and are publicly available as of the date of publication (GSE263510 for bulk RNA-seq and ATAC-seq data; GSE254449 for scRNA-seq data, respectively.).

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (No. 81925018 and 82130049 to J. Zhou; No. 82001660 to X. Zheng) and the China Postdoctoral Science Foundation (No. 2021M692406 to X. Zheng).

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Author notes

  1. These authors contributed equally: Xiaoqing Zheng, Wen Lei, Yongmei Zhang.

Authors and Affiliations

  1. Tianjin Institute of Immunology, Key Laboratory of Immune Microenvironment and Disease (Ministry of Education), The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics, International Joint Laboratory of Ocular Diseases (Ministry of Education), State Key Laboratory of Experimental Hematology, Department of Immunology, Tianjin Medical University, Tianjin, 300070, China

    Xiaoqing Zheng, Yongmei Zhang, Zhi Yao & Jie Zhou

  2. Institute of Pediatric Health and Disease, Guangdong Provincial Key Laboratory of Major Obstetric Diseases, Guangdong Provincial Clinical Research Center for Obstetrics and Gynecology, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510150, China

    Xiaoqing Zheng, Fan Wu & Chonghong Jia

  3. Key Laboratory of Immune Mechanism and Intervention on Serious Disease in Hebei Province, Department of Immunology, Hebei Medical University, Shijiazhuang, 050017, China

    Xiaoqing Zheng & Ruihong Zeng

  4. Pediatric Immunity and Healthcare Biomedical Co., Ltd, Guangzhou, 510320, China

    Wen Lei

  5. Department of Neurology, Institute of Neuroimmunology, Tianjin Medical University General Hospital, Tianjin, 300052, China

    Han Jin & Qiang Liu

  6. Department of Gynecology and Obstetrics, Tianjin Medical University General Hospital, Tianjin, 300052, China

    Cha Han

  7. Department of Neonatology, Guangzhou Key Laboratory of Neonatal Intestinal Diseases, The Third Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510150, China

    Fan Wu & Chonghong Jia

  8. Department of Gastroenterology, Guangzhou Institute of Pediatrics, Guangzhou Women and Children’s Medical Center, Guangzhou Medical University, Guangzhou, 510623, China

    Zhanghua Chen & Yuxia Zhang

  9. Department of oncology, The Second Hospital of Tianjin Medical University, Tianjin Key Laboratory of Precision Medicine for Sex Hormones and Diseases, Tianjin, 300211, China

    Haitao Wang

  10. Department of Pharmacology, Tianjin Key Laboratory of Inflammatory Biology, School of Basic Medical Sciences, Tianjin Medical University, Tianjin, 300070, China

    Ying Yu

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  1. Xiaoqing Zheng
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Contributions

JZ conceived and supervised this study. XZ performed most of the experiments, analyzed the data and wrote the manuscript. YZ participated in the animal model and flow cytometry analysis. WL, HJ and ZC performed the bulk RNA-seq, ATAC-seq and scRNA-seq analyses. FW and CJ provided the human peripheral blood samples. CH, RZ, YZ, HW, QL, ZY and YY provided help in project design and manuscript revision. JZ wrote the manuscript with input from all of the authors.

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Correspondence to Jie Zhou.

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The authors declare no competing interests. J.Z. is an editorial board member of Cellular & Molecular Immunology, but she has not been involved in the peer review or the decision-making of the article.

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Zheng, X., Lei, W., Zhang, Y. et al. Neuropilin-1high monocytes protect against neonatal inflammation. Cell Mol Immunol (2024). https://doi.org/10.1038/s41423-024-01157-7

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