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Immunobiology of COVID-19: Mechanistic and therapeutic insights from animal models

Zoological research 2024年第4期45卷 747-766页

作者： Hong-Yi Zheng Tian-Zhang Song Yong-Tang Zheng State Key Laboratory of Genetic Evolution&Animal Models KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesCenter for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650223China national Resource center for non-human primates National Research Facility for Phenotypic&Genetic Analysis of Model Animals(Primate Facility)Kunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China

The distribution of the immune system throughout the body complicates in vitro assessments of coronavirus disease 2019(COVID-19)immunobiology,often resulting in a lack of reproducibility when extrapolated to the whole ***,developing animal models is imperative for a comprehensive understanding of the pathology and immunology of severe acute respiratory syndrome coronavirus 2(SARS-CoV-2)*** review summarizes current progress related to COVID-19 animal models,including non-human primates(NHPs),mice,and hamsters,with a focus on their roles in exploring the mechanisms of immunopathology,immune protection,and long-term effects of SARS-CoV-2 infection,as well as their application in immunoprevention and immunotherapy of SARS-CoV-2 *** among these animal models and their specific applications are also highlighted,as no single model can fully encapsulate all aspects of *** effectively address the challenges posed by COVID-19,it is essential to select appropriate animal models that can accurately replicate both fatal and non-fatal infections with varying courses and *** animal model libraries and associated research tools is key to resolving the global COVID-19 pandemic,serving as a robust resource for future emerging infectious diseases.

关键词： SARS-CoV-2 COVID-19 Animal models Infection immunology Immunotherapy

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Identification of novel mammalian viruses in tree shrews(Tupaia belangeri chinensis)

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Zoological research 2024年第2期45卷 429-438页

作者： Hong Zhou Ren-Rong Tian Xiu-Rong Wang Jin-Xuan Yang Yun-Xiao Wang Ming-Liang Zhao Xu-Dong Zhang Yu-Hua Ma Long-Bao Lv Edward CHolmes Yong-Tang Zheng Wei-Feng Shi School of Clinical and Basic Medical Sciences Shandong First Medical University&Shandong Academy of Medical SciencesJi’nanShandong 250117China Key Laboratory of Emerging Infectious Diseases in Universities of Shandong Shandong First Medical University and Shandong Academy of Medical SciencesTaianShandong 271000China Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences/Key Laboratory of Bioactive Peptides of Yunnan Province KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesCenter for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650223China School of Public Health Shandong First Medical University&Shandong Academy of Medical SciencesJi’nanShandong 250117China national Resource center for non-human primates Kunming Primate Research CenterKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China Sydney Institute for Infectious Diseases School of Medical SciencesThe University of SydneySydneyNew South Wales 2006Australia Department of Infectious Diseases Ruijin HospitalShanghai Jiao Tong University School of MedicineShanghai 200025China Shanghai Institute of Virology Shanghai Jiao Tong University School of MedicineShanghai 200025China

The Chinese tree shrew(Tupaia belangeri chinensis),a member of the mammalian order Scandentia,exhibits considerable similarities with primates,including humans,in aspects of its nervous,immune,and metabolic *** similarities have established the tree shrew as a promising experimental model for biomedical research on cancer,infectious diseases,metabolic disorders,and mental health ***,we used metatranscriptomic sequencing to analyze plasma,as well as oral and anal swab samples,from 105 healthy asymptomatic tree shrews to identify the presence of potential zoonotic *** total,eight mammalian viruses with complete genomes were identified,belonging to six viral families,including Flaviviridae,Hepeviridae,Parvovirinae,Picornaviridae,Sedoreoviridae,and ***,the presence of rotavirus was recorded in tree shrews for the first *** viruses-hepacivirus 1,parvovirus,and picornavirus-exhibited low genetic similarity(high similarity(>94%)to known viral *** analyses also revealed that the rotavirus and mammalian orthoreovirus identified in this study may be novel *** findings provide insights into the diverse viral spectrum present in captive Chinese tree shrews,highlighting the necessity for further research into their potential for crossspecies transmission.

关键词： Tree shrew(Tupaia belangeri chinensis) Meta-transcriptomic sequencing Mammalian viruses Genomic analysis

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HR121 targeting HR2 domain in S2 subunit of spike protein can serve as a broad-spectrum SARS-CoV-2 inhibitor via intranasal administration

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Acta Pharmaceutica Sinica B 2023年第8期13卷 3339-3351页

作者： Ying Lu Fan Shen Wen-Qiang He An-Qi Li Ming-Hua Li Xiao-Li Feng Yong-Tang Zheng Wei Pang Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences/Key Laboratory of Bioactive Peptides of Yunnan Province KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesCenter for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunming 650223China University of Chinese Academy of Sciences Beijing 100049China kunming national high-level biosafety research center for non-human primates Center for Biosafety MegaScienceKunming Institute of ZoologyChinese Academy of SciencesKunming 650107China

The continuously emerging SARS-CoV-2 variants pose a great challenge to the efficacy of current drugs,this necessitates the development of broad-spectrum antiviral *** the previous study,we designed a recombinant protein,heptad repeat(HR)121,as a variant-proof ***,we found it can act as a fusion inhibitor and demonstrated broadly neutralizing activities against SARS-CoV-2 and its main *** analysis suggested that HR121 targets the HR2 domain in SARS-CoV-2 spike(S)2 subunit to block virus-cell *** experiments demonstrated that HR121 can bind HR2 at serological-pH and endosomal-pH,highlighting its inhibition capacity when SARS-CoV-2 enters via either cellular membrane fusion or endosomal ***,HR121 can effectively inhibit SARS-CoV-2 and Omicron variant pseudoviruses entering the cells,as well as block authentic SARSCoV-2 and Omicron BA.2 replications in human pulmonary alveolar epithelial *** intranasal administration to Syrian golden hamsters,it can protect hamsters from SARS-CoV-2 and Omicron BA.2 ***,our results suggest that HR121 is a potent drug candidate with broadly neutralizing activities against SARS-CoV-2 and its variants.

关键词： SARS-CoV-2 S2 subunit Heptad repeat 2 HR121 Fusion inhibitor Intranasal administration Variants Omicron BA.2

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Infectivity of SARS-CoV-2 and protection against reinfection in rats

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Zoological research 2022年第6期43卷 945-948页

作者： Dandan Yu Yanghaopeng Long Ling Xu Jian-Bao Han Jiawei Xi Jianlin Xu Lu-Xiu Yang Xiao-Li Feng Qing-Cui Zou Wang Qu Jiangwei Lin Ming-Hua Li Yong-Gang Yao Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650201China kunming national high-level biosafety research center for non-human primates Center for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China kunming College of Life Science University of Chinese Academy of SciencesKunmingYunnan 650204China

DEAR EDITOR,The severe acute respiratory syndrome coronavirus 2(SARS-CoV-2) pandemic remains an important global public health issue. In this study, we unexpectedly found that wildtype Sprague-Dawley(SD) rats can be infected with the SARS-CoV-2 prototype. Our results showed direct experimental evidence of the infectivity of SARS-CoV-2 infection, subsequent pathogenicity, and protection against reinfection in rats.

关键词： infection rats acute

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Characteristics of replication and pathogenicity of SARS-CoV-2 Alpha and Delta isolates

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Virologica Sinica 2022年第6期37卷 804-812页

作者： Xiao-Li Feng Dandan Yu Mi Zhang Xiaohong Li Qing-Cui Zou Wentai Ma Jian-Bao Han Ling Xu Cuixian Yang Wang Qu Zhong-Hua Deng Junyi Long Yanghaopeng Long Mingkun Li Yong-Gang Yao Xing-Qi Dong Jianxiong Zeng Ming-Hua Li kunming national high-level biosafety research center for non-human primates Center for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunming650107China Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences and KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesKunming Institute of ZoologyChinese Academy of SciencesKunming650201China national Resource center for non-human primates National Research Facility for Phenotypic&Genetic Analysis of Model Animals(Primate Facility)Kunming Institute of ZoologyChinese Academy of SciencesKunming650107China Department of Infectious Diseases Yunnan Provincial Infectious Diseases HospitalKunming650301China Key Laboratory of Genomic and Precision Medicine Beijing Institute of GenomicsChinese Academy of Sciencesand China National Center for BioinformationBeijing100101China University of Chinese Academy of Sciences Beijing100049China center for Excellence in Animal Evolution and Genetics Chinese Academy of SciencesKunming650201China kunming College of Life Science University of Chinese Academy of SciencesKunming650204China Yunnan Key Laboratory of Biodiversity Information Kunming Institute of ZoologyChinese Academy of SciencesKunming650201China

The continuously arising of SARS-CoV-2 variants has been posting a great threat to public health safety globally,from B.1.17(Alpha), B.1.351(Beta), P.1(Gamma), B.1.617.2(Delta) to B.1.1.529(Omicron). The emerging or reemerging of the SARS-CoV-2 variants of concern is calling for the constant monitoring of their epidemics,pathogenicity and immune escape. In this study, we aimed to characterize replication and pathogenicity of the Alpha and Delta variant strains isolated from patients infected in Laos. The amino acid mutations within the spike fragment of the isolates were determined via sequencing. The more efficient replication of the Alpha and Delta isolates was documented than the prototyped SARS-CoV-2 in Calu-3 and Caco-2 cells, while such features were not observed in Huh-7, Vero E6 and HPA-3 cells. We utilized both animal models of human ACE2(hACE2)transgenic mice and hamsters to evaluate the pathogenesis of the isolates. The Alpha and Delta can replicate well in multiple organs and cause moderate to severe lung pathology in these animals. In conclusion, the spike protein of the isolated Alpha and Delta variant strains was characterized, and the replication and pathogenicity of the strains in the cells and animal models were also evaluated.

关键词： SARS-CoV-2 Variants of concern(VOC) Alpha Delta hACE2 transgenic mice Hamster

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Single-nucleus transcriptomic profiling of multiple organs in a rhesus macaque model of SARS-CoV-2 infection

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Zoological research 2022年第6期43卷 1041-1062页

作者： Qiang Ma Wenji Ma Tian-Zhang Song Zhaobo Wu Zeyuan Liu Zhenxiang Hu Jian-Bao Han Ling Xu Bo Zeng Bosong Wang Yinuo Sun Dan-Dan Yu Qian Wu Yong-Gang Yao Yong-Tang Zheng Xiaoqun Wang State Key Laboratory of Brain and Cognitive Science Institute of BiophysicsChinese Academy of SciencesBeijing 100101China University of Chinese Academy of Sciences Beijing 100049China Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650223China kunming national high-level biosafety research center for non-human primates Center for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China national Resource center for non-human primates National Research Facility for Phenotypic&Genetic Analysis of Model Animals(Primate Facility)Kunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China LivzonBio Inc.ZhuhaiGuangdong 519045China State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal UniversityBeijing 100875China IDG/McGovern Institute for Brain research Beijing Normal UniversityBeijing 100875China Advanced Innovation center for human Brain Protection Beijing Institute for Brain DisordersCapital Medical UniversityBeijing 100069China

Infection with severe acute respiratory syndrome coronavirus 2(SARS-CoV-2) causes diverse clinical manifestations and tissue injuries in multiple ***, cellular and molecular understanding of SARS-CoV-2 infection-associated pathology and immune defense features in different organs remains incomplete. Here, we profiled approximately 77 000single-nucleus transcriptomes of the lung, liver,kidney, and cerebral cortex in rhesus macaques(Macaca mulatta) infected with SARS-CoV-2 and healthy controls. Integrated analysis of the multiorgan dataset suggested that the liver harbored the strongest global transcriptional alterations. We observed prominent impairment in lung epithelial cells, especially in AT2 and ciliated cells, and evident signs of fibrosis in fibroblasts. These lung injury characteristics are similar to those reported in patients with coronavirus disease 2019(COVID-19).Furthermore, we found suppressed MHC class I/II molecular activity in the lung, inflammatory response in the liver, and activation of the kynurenine pathway,which induced the development of an immunosuppressive microenvironment. Analysis of the kidney dataset highlighted tropism of tubule cells to SARS-CoV-2, and we found membranous nephropathy(an autoimmune disease) caused by podocyte dysregulation. In addition, we identified the pathological states of astrocytes and oligodendrocytes in the cerebral cortex, providing molecular insights into COVID-19-related neurological implications. Overall, our multi-organ single-nucleus transcriptomic survey of SARS-CoV-2-infected rhesus macaques broadens our understanding of disease features and antiviral immune defects caused by SARS-CoV-2 infection,which may facilitate the development of therapeutic interventions for COVID-19.

关键词： SARS-CoV-2 Rhesus macaque Animal model Single-nucleus RNA sequencing Antiviral immune defects Multiple organs

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Direct infection of SARS-CoV-2 in human iPSC-derived 3D cardiac organoids recapitulates COVID-19 myocarditis

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Virologica Sinica 2023年第6期38卷 971-974页

作者： Weijie Wang Jinxuan Yang Pinfang Kang Jinsong Bai Xiaoli Feng Liuqi Huang Yiming Zhang Yuechun Wu Bi Tang Hongju Wang JianJie Jiang Minghua Li Bing Zhao Xinglou Yang Department of Cardiovascular Disease The First Affiliated Hospital of Bengbu Medical CollegeBengbu233004China Yunnan Key Laboratory of Biodiversity Information Kunming Institute of ZoologyChinese Academy of SciencesKunming650201China State Key Laboratory of Genetic Engineering School of Life SciencesZhongshan HospitalFudan UniversityShanghai200438China kunming Third People's Hospital Kunming650041China kunming national high-level biosafety research center for non-human primates Kunming Institute of ZoologyChinese Academic of SciencesKunming650107China Institute of Organoid Technology Kunming Medical UniversityKunming650500China

Dear editor,The pandemic of coronavirus disease-19(COVID-19)has lasted for more than three years,causing lots of extra death and posing a serious threat to public *** pandemic swept the last global safety island in a matter of months,coinciding with the switch of zero-COVID policy of *** causative agent,SARS-CoV-2,spreads globally and then lurks in the population with sporadic outbreaks in local ***,the sequelae of convalescent COVID-19 patients receded *** pantissue tropism of SARS-CoV-2 results in a wide range of symptoms in patients,including cardiovascular *** complications occur in 20%–44%of hospitalized patients,which is an independent risk factor for COVID-19 mortality(Ma et al.,2022;Patone et al.,2022).Survivors of acute COVID-19 also have a substantial risk of cardiovascular disease burden lasting up to one year(Xie et al.,2022).

关键词： cardiovascular mortality acute

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Aging induces severe SIV infection accompanied by an increase in follicular CD8+T cells with overactive STAT3 signaling

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Cellular & Molecular Immunology 2022年第9期19卷 1042-1053页

作者： Hong-Yi Zheng Xue-Hui Wang Xiao-Yan He Min Chen Ming-Xu Zhang Xiao-Dong Lian Jia-Hao Song Yan Hu Wei Pang Yun Wang Zheng-Fei Hu Long-Bao Lv Yong-Tang Zheng Key Laboratory of Animal Models and human Disease Mechanisms of Chinese Academy of Sciences KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesCenter for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan650223China School of Life Sciences University of Science and Technology of ChinaHefeiAnhui230026China kunming College of Life Science University of Chinese Academy of SciencesKunmingYunnan650204China national Resource center for non-human primates National Research Facility for Phenotypic&Genetic Analysis of Model Animals(Primate Facility)Kunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan650107China

The number of elderly people living with HIV is increasing globally,and the condition of this population is relatively complicated due to the dual effects of aging and HIV ***,the impact of HIV infection combined with aging on the immune homeostasis of secondary lymphoid organs remains ***,we used the simian immunodeficiency virus mac239(SIVmac239)strain to infect six young and six old Chinese rhesus macaques(ChRMs)and compared the infection characteristics of the two groups in the chronic stage through multiplex immunofluorescence staining of lymph *** results showed that the SIV production and CD4/CD8 ratio inversion in old ChRMs were more severe than those in young ChRMs in both the peripheral blood and the lymph nodes,especially when a large number of CD8+T cells infiltrated the follicles and germinal ***3 in these follicular CXCR5+CD8+T cells was highly activated,with high expression of granzyme B,which might be caused by the severe inflammatory milieu in the follicles of old *** study indicates that aging may be a cofactor involved in SIV-induced immune disorders in secondary lymphoid tissues,affecting the effective antiviral activity of highly enriched follicular CXCR5+CD8+cells.

关键词： SIV Aging Follicle CD8 T cells

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Brain developmental and cortical connectivity changes in transgenic monkeys carrying the human-specific duplicated gene SRGAP2C

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national Science Review 2023年第11期10卷 45-60页

作者： Xiaoyu Meng Qiang Lin Xuerui Zeng Jin Jiang Min Li Xin Luo Kaimin Chen Haixu Wu Yan Hu Cirong Liu Bing Su State Key Laboratory of Genetic Resources and Evolution Kunming Institute of ZoologyChinese Academy of Sciences national Resource center for non-human primates Kunming Primate Research Centerand National Research Facility for Phenotypic and Genetic Analysis of Model Animals (Primate Facility)Kunming Institute of ZoologyChinese Academy of Sciences kunming College of Life Science University of Chinese Academy of Sciences center for Excellence in Brain Science and Intelligence Technology Institute of NeuroscienceCAS Key Laboratory of Primate NeurobiologyChinese Academy of Sciences center for Excellence in Animal Evolution and Genetics Chinese Academy of Sciences

human-specific duplicated genes contributed to phenotypic innovations during the origin of our own species, such as an enlarged brain and highly developed cognitive abilities. While prior studies on transgenic mice carrying the human-specific SRGAP2C gene have shown enhanced brain connectivity, the relevance to humans remains unclear due to the significant evolutionary gap between humans and rodents. In this study,to investigate the phenotypic outcome and underlying genetic mechanism of SRGAP2C, we generated transgenic cynomolgus macaques(Macaca fascicularis) carrying the human-specific SRGAP2C *** MRI imaging revealed delayed brain development with region-specific volume changes,accompanied by altered myelination levels in the temporal and occipital regions. On a cellular level, the transgenic monkeys exhibited increased deep-layer neurons during fetal neurogenesis and delayed synaptic maturation in adolescence. Moreover, transcriptome analysis detected neotenic expression in molecular pathways related to neuron ensheathment, synaptic connections, extracellular matrix and energy metabolism. Cognitively, the transgenic monkeys demonstrated improved motor planning and execution skills. Together, our findings provide new insights into the mechanisms by which the newly evolved gene shapes the unique development and circuitry of the human brain.

关键词： SRGAP2C transgenic monkey brain evolution brain development neurogenesis neoteny

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Delayed severe cytokine storm and immune cell infiltration in SARS-CoV-2-infected aged Chinese rhesus macaques

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Zoological research 2020年第5期41卷 503-516页

作者： Tian-Zhang Song Hong-Yi Zheng Jian-Bao Han Lin Jin Xiang Yang Feng-Liang Liu Rong-Hua Luo Ren-Rong Tian Hou-Rong Cai Xiao-Li Feng Chao Liu Ming-Hua Li Yong-Tang Zheng Key Laboratory of Animal Models and human Disease Mechanisms of the Chinese Academy of Sciences KIZ-CUHK Joint Laboratory of Bioresources and Molecular Research in Common DiseasesKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650223China kunming national high-level biosafety research center for non-human primates Center for Biosafety Mega-ScienceKunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China Department of Respiratory and Critical Care Medicine Affiliated Drum Tower Hospital of Nanjing UniversityNanjingJiangsu 210008China national Resource center for non-human primates National Research Facility for Phenotypic&Genetic Analysis of Model Animals(Primate Facility)Kunming Institute of ZoologyChinese Academy of SciencesKunmingYunnan 650107China

As of June 2020, Coronavirus Disease 2019(COVID-19) has killed an estimated 440 000 people worldwide, 74% of whom were aged ≥65 years,making age the most significant risk factor for death caused by severe acute respiratory syndrome coronavirus 2(SARS-CoV-2) infection. To examine the effect of age on death, we established a SARSCoV-2 infection model in Chinese rhesus macaques(Macaca mulatta) of varied ages. Results indicated that infected young macaques manifested impaired respiratory function, active viral replication, severe lung damage, and infiltration of CD11b^+ and CD8^+ cells in lungs at one-week post infection(wpi), but also recovered rapidly at 2 wpi. In contrast, aged macaques demonstrated delayed immune responses with a more severe cytokine storm, increased infiltration of CD11b^+ cells, and persistent infiltration of CD8^+ cells in the lungs at 2 wpi. In addition,peripheral blood T cells from aged macaques showed greater inflammation and chemotaxis, but weaker antiviral functions than that in cells from young macaques. Thus, the delayed but more severe cytokine storm and higher immune cell infiltration may explain the poorer prognosis of older aged patients suffering SARS-CoV-2 infection.

关键词： COVID-19 non-human primate animal model Elderly Immune response

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