Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses
The COVID-19 pandemic presents a major threat to global public health. Several lines of evidence have shown that the Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2), along with two other highly pathogenic coronaviruses, SARS-CoV and Middle East Respiratory Syndrome (MERS-CoV) originated...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2024-12-01
|
| Series: | Emerging Microbes and Infections |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/22221751.2024.2327368 |
| _version_ | 1826947170110013440 |
|---|---|
| author | Qianchun Gong Rendi Jiang Lina Ji Haofeng Lin Meiqin Liu Xiaofang Tang Yong Yang Wei Han Jing Chen Zishuo Guo Qi Wang Qian Li Xi Wang Tingting Jiang Shizhe Xie Xinglou Yang Peng Zhou Zhengli Shi Xinhua Lin |
| author_facet | Qianchun Gong Rendi Jiang Lina Ji Haofeng Lin Meiqin Liu Xiaofang Tang Yong Yang Wei Han Jing Chen Zishuo Guo Qi Wang Qian Li Xi Wang Tingting Jiang Shizhe Xie Xinglou Yang Peng Zhou Zhengli Shi Xinhua Lin |
| author_sort | Qianchun Gong |
| collection | DOAJ |
| description | The COVID-19 pandemic presents a major threat to global public health. Several lines of evidence have shown that the Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2), along with two other highly pathogenic coronaviruses, SARS-CoV and Middle East Respiratory Syndrome (MERS-CoV) originated from bats. To prevent and control future coronavirus outbreaks, it is necessary to investigate the interspecies infection and pathogenicity risks of animal-related coronaviruses. Currently used infection models, including in vitro cell lines and in vivo animal models, fail to fully mimic the primary infection in human tissues. Here, we employed organoid technology as a promising new model for studying emerging pathogens and their pathogenic mechanisms. We investigated the key host-virus interaction patterns of five human coronaviruses (SARS-CoV-2 original strain, Omicron BA.1, MERS-CoV, HCoV-229E, and HCoV-OC43) in different human respiratory organoids. Five indicators, including cell tropism, invasion preference, replication activity, host response and virus-induced cell death, were developed to establish a comprehensive evaluation system to predict coronavirus interspecies infection and pathogenicity risks. Using this system, we further examined the pathogenicity and interspecies infection risks of three SARS-related coronaviruses (SARSr-CoV), including WIV1 and rRsSHC014S from bats, and MpCoV-GX from pangolins. Moreover, we found that cannabidiol, a non-psychoactive plant extract, exhibits significant inhibitory effects on various coronaviruses in human lung organoid. Cannabidiol significantly enhanced interferon-stimulated gene expression but reduced levels of inflammatory cytokines. In summary, our study established a reliable comprehensive evaluation system to analyse infection and pathogenicity patterns of zoonotic coronaviruses, which could aid in prevention and control of potentially emerging coronavirus diseases. |
| first_indexed | 2024-04-24T18:51:25Z |
| format | Article |
| id | doaj.art-2b52432738554d6daade9907a163132b |
| institution | Directory Open Access Journal |
| issn | 2222-1751 |
| language | English |
| last_indexed | 2025-02-17T21:26:20Z |
| publishDate | 2024-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Emerging Microbes and Infections |
| spelling | doaj.art-2b52432738554d6daade9907a163132b2024-12-07T04:40:17ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512024-12-0113110.1080/22221751.2024.2327368Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronavirusesQianchun Gong0Rendi Jiang1Lina Ji2Haofeng Lin3Meiqin Liu4Xiaofang Tang5Yong Yang6Wei Han7Jing Chen8Zishuo Guo9Qi Wang10Qian Li11Xi Wang12Tingting Jiang13Shizhe Xie14Xinglou Yang15Peng Zhou16Zhengli Shi17Xinhua Lin18State Key Laboratory of Genetic Engineering, Greater Bay Area Institute of Precision Medicine (Guangzhou), School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai, People’s Republic of ChinaState Key Laboratory of Genetic Engineering, Greater Bay Area Institute of Precision Medicine (Guangzhou), School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai, People’s Republic of ChinaSchool of Life Sciences, Inner Mongolia University, Hohhot, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaThe First Affiliated Hospital of Guangzhou Medical University, Guangzhou Medical University, Guangzhou, People’s Republic of ChinaState Key Laboratory of Genetic Engineering, Greater Bay Area Institute of Precision Medicine (Guangzhou), School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai, People’s Republic of ChinaThe First Affiliated Hospital of Guangzhou Medical University, Guangzhou Medical University, Guangzhou, People’s Republic of ChinaSchool of Life Sciences, Inner Mongolia University, Hohhot, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaThe First Affiliated Hospital of Guangzhou Medical University, Guangzhou Medical University, Guangzhou, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaYunnan Key Laboratory of Biodiversity Information, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, People’s Republic of ChinaThe First Affiliated Hospital of Guangzhou Medical University, Guangzhou Medical University, Guangzhou, People’s Republic of ChinaState Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, People’s Republic of ChinaState Key Laboratory of Genetic Engineering, Greater Bay Area Institute of Precision Medicine (Guangzhou), School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai, People’s Republic of ChinaThe COVID-19 pandemic presents a major threat to global public health. Several lines of evidence have shown that the Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2), along with two other highly pathogenic coronaviruses, SARS-CoV and Middle East Respiratory Syndrome (MERS-CoV) originated from bats. To prevent and control future coronavirus outbreaks, it is necessary to investigate the interspecies infection and pathogenicity risks of animal-related coronaviruses. Currently used infection models, including in vitro cell lines and in vivo animal models, fail to fully mimic the primary infection in human tissues. Here, we employed organoid technology as a promising new model for studying emerging pathogens and their pathogenic mechanisms. We investigated the key host-virus interaction patterns of five human coronaviruses (SARS-CoV-2 original strain, Omicron BA.1, MERS-CoV, HCoV-229E, and HCoV-OC43) in different human respiratory organoids. Five indicators, including cell tropism, invasion preference, replication activity, host response and virus-induced cell death, were developed to establish a comprehensive evaluation system to predict coronavirus interspecies infection and pathogenicity risks. Using this system, we further examined the pathogenicity and interspecies infection risks of three SARS-related coronaviruses (SARSr-CoV), including WIV1 and rRsSHC014S from bats, and MpCoV-GX from pangolins. Moreover, we found that cannabidiol, a non-psychoactive plant extract, exhibits significant inhibitory effects on various coronaviruses in human lung organoid. Cannabidiol significantly enhanced interferon-stimulated gene expression but reduced levels of inflammatory cytokines. In summary, our study established a reliable comprehensive evaluation system to analyse infection and pathogenicity patterns of zoonotic coronaviruses, which could aid in prevention and control of potentially emerging coronavirus diseases.https://www.tandfonline.com/doi/10.1080/22221751.2024.2327368Organoidevaluation systemcoronavirusinterspecies infectioncannabidiol |
| spellingShingle | Qianchun Gong Rendi Jiang Lina Ji Haofeng Lin Meiqin Liu Xiaofang Tang Yong Yang Wei Han Jing Chen Zishuo Guo Qi Wang Qian Li Xi Wang Tingting Jiang Shizhe Xie Xinglou Yang Peng Zhou Zhengli Shi Xinhua Lin Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses Emerging Microbes and Infections Organoid evaluation system coronavirus interspecies infection cannabidiol |
| title | Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses |
| title_full | Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses |
| title_fullStr | Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses |
| title_full_unstemmed | Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses |
| title_short | Establishment of a human organoid-based evaluation system for assessing interspecies infection risk of animal-borne coronaviruses |
| title_sort | establishment of a human organoid based evaluation system for assessing interspecies infection risk of animal borne coronaviruses |
| topic | Organoid evaluation system coronavirus interspecies infection cannabidiol |
| url | https://www.tandfonline.com/doi/10.1080/22221751.2024.2327368 |
| work_keys_str_mv | AT qianchungong establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT rendijiang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT linaji establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT haofenglin establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT meiqinliu establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT xiaofangtang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT yongyang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT weihan establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT jingchen establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT zishuoguo establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT qiwang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT qianli establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT xiwang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT tingtingjiang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT shizhexie establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT xinglouyang establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT pengzhou establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT zhenglishi establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses AT xinhualin establishmentofahumanorganoidbasedevaluationsystemforassessinginterspeciesinfectionriskofanimalbornecoronaviruses |