SARS-CoV-2 envelope protein causes acute respiratory distress syndrome (ARDS)-like pathological damages and constitutes an antiviral target

被引:126
作者
Xia, Bingqing [1 ,2 ]
Shen, Xurui [1 ,2 ]
He, Yang [1 ,2 ]
Pan, Xiaoyan [3 ]
Liu, Feng-Liang [4 ,5 ]
Wang, Yi [1 ,2 ]
Yang, Feipu [1 ,2 ]
Fang, Sui [1 ]
Wu, Yan [3 ]
Duan, Zilei [4 ,5 ]
Zuo, Xiaoli [1 ]
Xie, Zhuqing [1 ,6 ]
Jiang, Xiangrui [1 ,2 ]
Xu, Ling [4 ,5 ]
Chi, Hao [1 ,2 ]
Li, Shuangqu [1 ,2 ]
Meng, Qian [1 ]
Zhou, Hu [1 ,2 ]
Zhou, Yubo [1 ,2 ]
Cheng, Xi [1 ,2 ]
Xin, Xiaoming [6 ]
Jin, Lin [4 ,5 ]
Zhang, Hai-Lin [7 ]
Yu, Dan-Dan [4 ,5 ]
Li, Ming-Hua [8 ]
Feng, Xiao-Li [8 ]
Chen, Jiekai [9 ,10 ,11 ]
Jiang, Hualiang [1 ,2 ]
Xiao, Gengfu [3 ]
Zheng, Yong-Tang [4 ,5 ,6 ,8 ]
Zhang, Lei-Ke [3 ]
Shen, Jingshan [1 ,2 ]
Li, Jia [1 ,2 ,12 ]
Gao, Zhaobing [1 ,2 ,12 ,13 ]
机构
[1] Chinese Acad Sci, Shanghai Inst Mat Med, Stake Key Lab Drug Res, CAS Key Lab Receptor Res, Shanghai, Peoples R China
[2] Univ Chinese Acad Sci, Beijing, Peoples R China
[3] Chinese Acad Sci, Ctr Biosafety Mega Sci, Wuhan Inst Virol, State Key Lab Virol, Wuhan, Hubei, Peoples R China
[4] Chinese Acad Sci, Key Lab Anim Models & Human Dis Mech, Kunming, Yunnan, Peoples R China
[5] Chinese Acad Sci, Kunming Inst Zool, KIZ CUHK Joint Lab Bioresources & Mol Res Common, Kunming, Yunnan, Peoples R China
[6] Shanghai Univ Med & Hlth Sci, Shanghai, Peoples R China
[7] Chinese Acad Sci, Kunming Inst Zool, State Key Lab Genet Resources & Evolut, Kunming, Yunnan, Peoples R China
[8] Chinese Acad Sci, Ctr Biosafety Mega Sci, Kunming Natl High Level Biosafety Res Ctr Nonhuma, Kunming Inst Zool, Kunming, Yunnan, Peoples R China
[9] Ctr Cell Fate & Lineage CCLA, Guangzhou Regenerat Med & Hlth Guangdong Lab, Guangzhou, Guangdong, Peoples R China
[10] Chinese Acad Sci, Guangzhou Inst Biomed & Hlth, Guangdong Prov Key Lab Stem Cell & Regenerat Med, CAS Key Lab Regenerat Biol, Guangzhou, Guangdong, Peoples R China
[11] Guangzhou Med Univ, Joint Sch Life Sci, Guangzhou, Guangdong, Peoples R China
[12] Chinese Acad Sci, Inst Drug Discovery Innovat, Zhongshan Inst Drug Discovery, Zhongshan, Guangdong, Peoples R China
[13] Fudan Univ, Sch Pharm, Shanghai, Peoples R China
基金
中国国家自然科学基金;
关键词
CORONAVIRUS DISEASE 2019; ION-CHANNEL ACTIVITY; CELL ENTRY; SARS; COVID-19; MLKL; INFLAMMASOME; EPIDEMIOLOGY;
D O I
10.1038/s41422-021-00519-4
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Cytokine storm and multi-organ failure are the main causes of SARS-CoV-2-related death. However, the origin of excessive damages caused by SARS-CoV-2 remains largely unknown. Here we show that the SARS-CoV-2 envelope (2-E) protein alone is able to cause acute respiratory distress syndrome (ARDS)-like damages in vitro and in vivo. 2-E proteins were found to form a type of pH-sensitive cation channels in bilayer lipid membranes. As observed in SARS-CoV-2-infected cells, heterologous expression of 2-E channels induced rapid cell death in various susceptible cell types and robust secretion of cytokines and chemokines in macrophages. Intravenous administration of purified 2-E protein into mice caused ARDS-like pathological damages in lung and spleen. A dominant negative mutation lowering 2-E channel activity attenuated cell death and SARS-CoV-2 production. Newly identified channel inhibitors exhibited potent anti-SARS-CoV-2 activity and excellent cell protective activity in vitro and these activities were positively correlated with inhibition of 2-E channel. Importantly, prophylactic and therapeutic administration of the channel inhibitor effectively reduced both the viral load and secretion of inflammation cytokines in lungs of SARS-CoV-2-infected transgenic mice expressing human angiotensin-converting enzyme 2 (hACE-2). Our study supports that 2-E is a promising drug target against SARS-CoV-2.
引用
收藏
页码:847 / 860
页数:14
相关论文
共 77 条
[11]  
Havlichek Daniel Jr, 2020, N Engl J Med, V382, pe68, DOI 10.1056/NEJMc2008043
[12]   SARS and MERS: recent insights into emerging coronaviruses [J].
de Wit, Emmie ;
van Doremalen, Neeltje ;
Falzarano, Darryl ;
Munster, Vincent J. .
NATURE REVIEWS MICROBIOLOGY, 2016, 14 (08) :523-534
[13]  
Del Valle DM, 2020, NAT MED, V26, P1636, DOI [10.1038/s41591-020-1051-9, 10.1101/2020.05.28.20115758]
[14]   Pore-forming activity and structural autoinhibition of the gasdermin family [J].
Ding, Jingjin ;
Wang, Kun ;
Liu, Wang ;
She, Yang ;
Sun, Qi ;
Shi, Jianjin ;
Sun, Hanzi ;
Wang, Da-Cheng ;
Shao, Feng .
NATURE, 2016, 535 (7610) :111-+
[15]   Structurally Resolved SARS-CoV-2 Antibody Shows High Efficacy in Severely Infected Hamsters and Provides a Potent Cocktail Pairing Strategy [J].
Du, Shuo ;
Cao, Yunlong ;
Zhu, Qinyu ;
Yu, Pin ;
Qi, Feifei ;
Wang, Guopeng ;
Du, Xiaoxia ;
Bao, Linlin ;
Deng, Wei ;
Zhu, Hua ;
Liu, Jiangning ;
Nie, Jianhui ;
Zheng, Yinghui ;
Liang, Haoyu ;
Liu, Ruixue ;
Gong, Shuran ;
Xu, Hua ;
Yisimayi, Ayijiang ;
Lv, Qi ;
Wang, Bo ;
He, Runsheng ;
Han, Yunlin ;
Zhao, Wenjie ;
Bai, Yali ;
Qu, Yajin ;
Gao, Xiang ;
Ji, Chenggong ;
Wang, Qisheng ;
Gao, Ning ;
Huang, Weijin ;
Wang, Youchun ;
Xie, X. Sunney ;
Su, Xiao-dong ;
Xiao, Junyu ;
Qin, Chuan .
CELL, 2020, 183 (04) :1013-+
[16]   Neurological associations of COVID-19 [J].
Ellul, Mark A. ;
Benjamin, Laura ;
Singh, Bhagteshwar ;
Lant, Suzannah ;
Michael, Benedict Daniel ;
Easton, Ava ;
Kneen, Rachel ;
Defres, Sylviane ;
Sejvar, Jim ;
Solomon, Tom .
LANCET NEUROLOGY, 2020, 19 (09) :767-783
[17]   Remdesivir in covid-19 [J].
Ferner, Robin E. ;
Aronson, Jeffrey K. .
BMJ-BRITISH MEDICAL JOURNAL, 2020, 369
[18]  
Gaburjakova J, 2018, ADV BIOMEMBR LIPID, V27, P147, DOI 10.1016/bs.abl.2017.12.005
[19]   β-Coronaviruses Use Lysosomes for Egress Instead of the Biosynthetic Secretory Pathway [J].
Ghosh, Sourish ;
Dellibovi-Ragheb, Teegan A. ;
Kerviel, Adeline ;
Pak, Eowyn ;
Qiu, Qi ;
Fisher, Matthew ;
Takvorian, Peter M. ;
Bleck, Christopher ;
Hsu, Victor W. ;
Fehr, Anthony R. ;
Perlman, Stanley ;
Achar, Sooraj R. ;
Straus, Marco R. ;
Whittaker, Gary R. ;
de Haan, Cornelis A. M. ;
Kehrl, John ;
Altan-Bonnet, Gregoire ;
Altan-Bonnet, Nihal .
CELL, 2020, 183 (06) :1520-+
[20]   ESCRT-III Acts Downstream of MLKL to Regulate Necroptotic Cell Death and Its Consequences [J].
Gong, Yi-Nan ;
Guy, Cliff ;
Olauson, Hannes ;
Becker, Jan Ulrich ;
Yang, Mao ;
Fitzgerald, Patrick ;
Linkermann, Andreas ;
Green, Douglas R. .
CELL, 2017, 169 (02) :286-300