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  3. An immune cell atlas reveals the dynamics of human macrophage specification during prenatal development

An immune cell atlas reveals the dynamics of human macrophage specification during prenatal development

  • Cell. 2023 Sep 6;S0092-8674(23)00908-X. doi: 10.1016/j.cell.2023.08.019.
Zeshuai Wang 1,  Zhisheng Wu 2,  Hao Wang 3,  Ruoqing Feng 4,  Guanlin Wang 5,  Muxi Li 6,  Shuang-Yin Wang 7,  Xiaoyan Chen 3,  Yiyi Su 1,  Jun Wang 4,  Weiwen Zhang 8,  Yuzhou Bao 9,  Zhenwei Lan 6,  Zhuo Song 10,  Yiheng Wang 11,  Xianyang Luo 12,  Lingyu Zhao 13,  Anli Hou 14,  Shuye Tian 15,  Hongliang Gao 14,  Wenbin Miao 14,  Yingyu Liu 3,  Huilin Wang 3,  Cui Yin 8,  Zhi-Liang Ji 6,  Mingqian Feng 16,  Hongkun Liu 17,  Lianghui Diao 18,  Ido Amit 7,  Yun Chen 19,  Yong Zeng 18,  Florent Ginhoux 20,  Xueqing Wu 21,  Yuanfang Zhu 22,  Hanjie Li 23
Affiliations

Affiliations

  • 1 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China.
  • 2 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; School of Chemistry and Chemical Engineering, Southeast University, Nanjing, China.
  • 3 Maternal Fetal Medicine Institute, Department of Obstetrics and Gynaecology, Shenzhen Baoan Women's and Children's Hospital, Jinan University, Shenzhen, China.
  • 4 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
  • 5 Shanghai Key Laboratory of Metabolic Remodeling and Health, Institute of Metabolism and Integrative Biology, Centre for Evolutionary Biology, Fudan University, Shanghai, China; Shanghai Qi Zhi Institute, Shanghai, China. Electronic address: [email protected].
  • 6 State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen University, Xiamen, China.
  • 7 Department of Systems Immunology, Weizmann Institute of Science, Rehovot, Israel.
  • 8 Department of Gynaecology & Obstetrics, Shenzhen University General Hospital, Shenzhen University, Shenzhen, China.
  • 9 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; State Key Laboratory of Cellular Stress Biology, School of Life Sciences, Faculty of Medicine and Life Sciences, Xiamen University, Xiamen, China.
  • 10 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Maternal Fetal Medicine Institute, Department of Obstetrics and Gynaecology, Shenzhen Baoan Women's and Children's Hospital, Jinan University, Shenzhen, China.
  • 11 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; College of Biological Sciences, China Agricultural University, Beijing, China.
  • 12 The Brain Cognition and Brain Disease Institute, Shenzhen-Hong Kong Institute of Brain Science, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.
  • 13 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Graduate School of Peking Union Medical College, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing, China.
  • 14 University of Chinese Academy of Sciences Shenzhen Hospital, Shenzhen, China.
  • 15 Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen 518055, China.
  • 16 College of Life Science and Technology, Huazhong Agricultural University, Wuhan, China.
  • 17 Jinxin Fertility Group Limited, Chengdu, China.
  • 18 Shenzhen Key Laboratory for Reproductive Immunology of Peri-Implantation, Shenzhen Zhongshan Institute for Reproduction and Genetics, Shenzhen Zhongshan Urology Hospital, Shenzhen, China.
  • 19 School of Chemistry and Chemical Engineering, Southeast University, Nanjing, China; Department of Immunology, Nanjing Medical University, Nanjing, China.
  • 20 Shanghai Institute of Immunology, Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China; INSERM U1015, Gustave Roussy Cancer Campus, Villejuif 94800, France; Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (A(∗)STAR), 8A Biomedical Grove, Immunos, Singapore 138648, Singapore; Translational Immunology Institute, SingHealth Duke-NUS Academic Medical Centre, Singapore 169856, Singapore. Electronic address: [email protected].
  • 21 Department of Gynaecology & Obstetrics, Shenzhen University General Hospital, Shenzhen University, Shenzhen, China. Electronic address: [email protected].
  • 22 Maternal Fetal Medicine Institute, Department of Obstetrics and Gynaecology, Shenzhen Baoan Women's and Children's Hospital, Jinan University, Shenzhen, China. Electronic address: [email protected].
  • 23 Key Laboratory of Quantitative Synthetic Biology, Shenzhen Institute of Synthetic Biology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China. Electronic address: [email protected].
PMID: 37703875 DOI: 10.1016/j.cell.2023.08.019
Abstract

Macrophages are heterogeneous and play critical roles in development and disease, but their diversity, function, and specification remain inadequately understood during human development. We generated a single-cell RNA sequencing map of the dynamics of human macrophage specification from PCW 4-26 across 19 tissues. We identified a microglia-like population and a proangiogenic population in 15 macrophage subtypes. Microglia-like cells, molecularly and morphologically similar to microglia in the CNS, are present in the fetal epidermis, testicle, and heart. They are the major immune population in the early epidermis, exhibit a polarized distribution along the dorsal-lateral-ventral axis, and interact with neural crest cells, modulating their differentiation along the melanocyte lineage. Through spatial and differentiation trajectory analysis, we also showed that proangiogenic macrophages are perivascular across fetal organs and likely yolk-sac-derived as microglia. Our study provides a comprehensive map of the heterogeneity and developmental dynamics of human macrophages and unravels their diverse functions during development.

Keywords

angiogenesis; developmental immunology; human immunology; immune cell atlas; macrophage; microglia; microglia-like cells; neural crest cells; perivascular macrophages; scRNA-seq.

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