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Neuropilin-1 Mediates SARS-CoV-2 Infection in Bone Marrow-derived Macrophages

Junjie Gao, Hong Mei, Jing Sun, Hao Li, Yuege Huang, Yanhong Tang, Linwei Duan, Delin Liu, Qiyang Wang, Youshui Gao, Ke Song, Jincun Zhao, Changqing Zhang, Jia Liu
doi: https://doi.org/10.1101/2021.04.14.439793
Junjie Gao
1Department of Orthopaedics, Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital, Shanghai, 200233, China
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Hong Mei
2Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, 201210, China
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Jing Sun
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, 510182, China
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Hao Li
1Department of Orthopaedics, Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital, Shanghai, 200233, China
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Yuege Huang
2Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, 201210, China
4School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China
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Yanhong Tang
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, 510182, China
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Linwei Duan
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, 510182, China
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Delin Liu
5Centre for Orthopaedic Research, School of Surgery, The University of Western Australia, Nedlands, Western Australia, 6009, Australia
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Qiyang Wang
1Department of Orthopaedics, Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital, Shanghai, 200233, China
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Youshui Gao
1Department of Orthopaedics, Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital, Shanghai, 200233, China
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Ke Song
2Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, 201210, China
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Jincun Zhao
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, 510182, China
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  • For correspondence: liujia@shanghaitech.edu.cn
Changqing Zhang
1Department of Orthopaedics, Shanghai Jiao Tong University Affiliated Shanghai Sixth People’s Hospital, Shanghai, 200233, China
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  • For correspondence: liujia@shanghaitech.edu.cn
Jia Liu
2Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, 201210, China
4School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China
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  • For correspondence: liujia@shanghaitech.edu.cn
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Abstract

SARS-CoV-2 infection in human can cause medical complications across various tissues and organs. Despite of the advances to understanding the pathogenesis of SARS-CoV-2, its tissue tropism and interactions with host cells have not been fully understood. Existing clinical data have suggested possible SARS-CoV-2 infection in human skeleton system. In the present study, we found that authentic SARS-CoV-2 could efficiently infect human and mouse bone marrow-derived macrophages (BMMs) and alter the expression of macrophage chemotaxis and osteoclast-related genes. Importantly, in a mouse SARS-CoV-2 infection model that was enabled by the intranasal adenoviral (AdV) delivery of human angiotensin converting enzyme 2 (hACE2), SARS-CoV-2 was found to be present in femoral BMMs as determined by in situ immunofluorescence analysis. Using single-cell RNA sequencing (scRNA-Seq), we characterized SARS-CoV-2 infection in BMMs. Importantly, SARS-CoV-2 entry on BMMs appeared to be dependent on the expression of neuropilin-1 (NRP1) rather than the widely recognized receptor ACE2. It was also noted that unlike brain macrophages which displayed aging-dependent NRP1 expression, BMMs from neonatal and aged mice had constant NRP1 expression, making BMMs constantly vulnerable target cells for SARS-CoV-2. Furthermore, it was found that the abolished SARS-CoV-2 entry in BMM-derived osteoclasts was associated with the loss of NRP1 expression during BMM-to-osteoclast differentiation. Collectively, our study has suggested that NRP1 can mediate SARS-CoV-2 infection in BMMs, which precautions the potential impact of SARS-CoV-2 infection on human skeleton system.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted April 14, 2021.
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Neuropilin-1 Mediates SARS-CoV-2 Infection in Bone Marrow-derived Macrophages
Junjie Gao, Hong Mei, Jing Sun, Hao Li, Yuege Huang, Yanhong Tang, Linwei Duan, Delin Liu, Qiyang Wang, Youshui Gao, Ke Song, Jincun Zhao, Changqing Zhang, Jia Liu
bioRxiv 2021.04.14.439793; doi: https://doi.org/10.1101/2021.04.14.439793
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Neuropilin-1 Mediates SARS-CoV-2 Infection in Bone Marrow-derived Macrophages
Junjie Gao, Hong Mei, Jing Sun, Hao Li, Yuege Huang, Yanhong Tang, Linwei Duan, Delin Liu, Qiyang Wang, Youshui Gao, Ke Song, Jincun Zhao, Changqing Zhang, Jia Liu
bioRxiv 2021.04.14.439793; doi: https://doi.org/10.1101/2021.04.14.439793

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