Northern pig-tailed macaques (<i>Macaca leonina</i>) infected with SARS-CoV-2 show rapid viral clearance and persistent immune response

Tian-Zhang Song; Hong-Yi Zheng; Jian-Bao Han; Xiao-Li Feng; Feng-Liang Liu; Xiang Yang; Lin Jin; Rong-Hua Luo; Ren-Rong Tian; Chao Liu; Ming-Hua Li; Hou-Rong Cai; Yong-Tang Zheng

doi:10.24272/j.issn.2095-8137.2020.334

Volume 42 Issue 3

May 2021

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Article Navigation > Zoological Research > 2021 > 42(3): 350-353

Tian-Zhang Song, Hong-Yi Zheng, Jian-Bao Han, Xiao-Li Feng, Feng-Liang Liu, Xiang Yang, Lin Jin, Rong-Hua Luo, Ren-Rong Tian, Chao Liu, Ming-Hua Li, Hou-Rong Cai, Yong-Tang Zheng. Northern pig-tailed macaques (Macaca leonina) infected with SARS-CoV-2 show rapid viral clearance and persistent immune response. Zoological Research, 2021, 42(3): 350-353. doi: 10.24272/j.issn.2095-8137.2020.334

Citation:

Tian-Zhang Song, Hong-Yi Zheng, Jian-Bao Han, Xiao-Li Feng, Feng-Liang Liu, Xiang Yang, Lin Jin, Rong-Hua Luo, Ren-Rong Tian, Chao Liu, Ming-Hua Li, Hou-Rong Cai, Yong-Tang Zheng. Northern pig-tailed macaques (Macaca leonina) infected with SARS-CoV-2 show rapid viral clearance and persistent immune response. Zoological Research, 2021, 42(3): 350-353. doi: 10.24272/j.issn.2095-8137.2020.334

Citation:

Tian-Zhang Song, Hong-Yi Zheng, Jian-Bao Han, Xiao-Li Feng, Feng-Liang Liu, Xiang Yang, Lin Jin, Rong-Hua Luo, Ren-Rong Tian, Chao Liu, Ming-Hua Li, Hou-Rong Cai, Yong-Tang Zheng. Northern pig-tailed macaques (Macaca leonina) infected with SARS-CoV-2 show rapid viral clearance and persistent immune response. Zoological Research, 2021, 42(3): 350-353. doi: 10.24272/j.issn.2095-8137.2020.334

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Northern pig-tailed macaques (Macaca leonina) infected with SARS-CoV-2 show rapid viral clearance and persistent immune response

doi: 10.24272/j.issn.2095-8137.2020.334

1.
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 Diseases, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China
2.
Kunming National High-Level Biosafety Research Center for Non-Human Primates, Center for Biosafety Mega-Science, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650107, China
3.
National Resource Center for Non-Human Primates, and National Research Facility for Phenotypic & Genetic Analysis of Model Animals (Primate Facility), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650107, China
4.
Department of Respiratory and Critical Care Medicine, Affiliated Drum Tower Hospital of Nanjing University, Nanjing, Jiangsu 210008, China

#These authors contributed equally to this work

Funds: This work was partly supported by the National Key R&D Program of China (2020YFC0842000), National Science and Technology Major Projects of Infectious Disease Funds (2017ZX10304402, 2018ZX10301406-003), the National Natural Science Foundation of China (U1802284, U1902210), National Resource Center for Non-Human Primates

More Information

Corresponding author: E-mail: zhengyt@mail.kiz.ac.cn
Received Date: 2020-11-17
Accepted Date: 2021-04-28

Published Online: 2021-05-13

Publish Date: 2021-05-18

Abstract

Abstract

Coronavirus disease 2019 (COVID-19), which is caused by severe acute respiratory syndrome coronavirus (SARS-CoV-2), has become an unprecedented global health emergency. At present, SARS-CoV-2-infected nonhuman primates are considered the gold standard animal model for COVID-19 research. Here, we showed that northern pig-tailed macaques (Macaca leonina, NPMs) supported SARS-CoV-2 replication. Furthermore, compared with rhesus macaques, NPMs showed rapid viral clearance in lung tissues, nose swabs, throat swabs, and rectal swabs, which may be due to higher expression of interferon (IFN)-α in lung tissue. However, the rapid viral clearance was not associated with good outcome. In the second week post infection, NPMs developed persistent or even more severe inflammation and body injury compared with rhesus macaques. These results suggest that viral clearance may have no relationship with COVID-19 progression and SARS-CoV-2-infected NPMs could be considered as a critically ill animal model in COVID-19 research.
- SARS-CoV-2,
- COVID-19,
- Primate animal models,
- Northern pig-tailed macaques (Macaca leonina),
- Immune response

#These authors contributed equally to this work

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References(20)

References

[1]	Chen L, Liu HG, Liu W, Liu J, Liu K, Shang J, et al. 2020. Analysis of clinical features of 29 patients with 2019 novel coronavirus pneumonia. Chinese Journal of Tuberculosis and Respiratory Diseases, 43(3): 203−208. (in Chinese)
[2]	Gao Y, Li TT, Han MF, Li XY, Wu D, Xu YH, et al. 2020. Diagnostic utility of clinical laboratory data determinations for patients with the severe COVID-19. Journal of Medical Virology, 92(7): 791−796. doi: 10.1002/jmv.25770
[3]	Hadjadj J, Yatim N, Barnabei L, Corneau A, Boussier J, Smith N, et al. 2020. Impaired type I interferon activity and inflammatory responses in severe COVID-19 patients. Science, 369(6504): 718−724. doi: 10.1126/science.abc6027
[4]	Kalaiyarasu S, Kumar M, Kumar DS, Bhatia S, Dash SK, Bhat S, et al. 2016. Highly pathogenic avian influenza H5N1 virus induces cytokine dysregulation with suppressed maturation of chicken monocyte-derived dendritic cells. Microbiology and Immunology, 60(10): 687−693. doi: 10.1111/1348-0421.12443
[5]	Karras A, Thervet E, Legendre C, the Groupe Coopératif de transplantation d'Ile de France. 2004. Hemophagocytic syndrome in renal transplant recipients: report of 17 cases and review of literature. Transplantation, 77(2): 238−243. doi: 10.1097/01.TP.0000107285.86939.37
[6]	Lau SK, Lau CCY, Chan KH, Li CP, Chen HL, Jin DY, et al. 2013. Delayed induction of proinflammatory cytokines and suppression of innate antiviral response by the novel Middle East respiratory syndrome coronavirus: implications for pathogenesis and treatment. The Journal of General Virology, 94(12): 2679−2690. doi: 10.1099/vir.0.055533-0
[7]	Lu SY, Zhao Y, Yu WH, Yang Y, Gao JH, Wang JB, et al. 2020. Comparison of nonhuman primates identified the suitable model for COVID-19. Signal Transduction and Targeted Therapy, 5(1): 157. doi: 10.1038/s41392-020-00269-6
[8]	Mantlo E, Bukreyeva N, Maruyama J, Paessler S, Huang C. 2020. Antiviral activities of type I interferons to SARS-CoV-2 infection. Antiviral Research, 179: 104811. doi: 10.1016/j.antiviral.2020.104811
[9]	Munster VJ, Feldmann F, Williamson BN, van Doremalen N, Pérez-Pérez L, Schulz J, et al. 2020. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature, 585(7824): 268−272. doi: 10.1038/s41586-020-2324-7
[10]	Ohta H, Yumara-Yagi K, Sakata N, Inoue M, Kawa-Ha K. 1994. Capillary leak syndrome in patients with hemophagocytic lymphohistiocytosis. Acta Paediatrica, 83(10): 1113−1114. doi: 10.1111/j.1651-2227.1994.tb13000.x
[11]	Pang W, Song JH, Lu Y, Zhang XL, Zheng HY, Jiang J, et al. 2018. Host restriction factors APOBEC3G/3F and other interferon-related gene expressions affect early HIV-1 infection in northern pig-tailed macaque (Macaca leonina). Frontiers in Immunology, 9: 1965. doi: 10.3389/fimmu.2018.01965
[12]	Pang W, Zhang GH, Jiang J, Zheng HY, Zhang LT, Zhang XL, et al. 2017. HIV-1 can infect northern pig-tailed macaques (Macaca leonina) and form viral reservoirs in vivo. Science Bulletin, 62(19): 1315−1324. doi: 10.1016/j.scib.2017.09.020
[13]	Schoggins JW, Rice CM. 2011. Interferon-stimulated genes and their antiviral effector functions. Current Opinion in Virology, 1(6): 519−525. doi: 10.1016/j.coviro.2011.10.008
[14]	Shan C, Yao YF, Yang XL, Zhou YW, Gao G, Peng Y, et al. 2020. Infection with novel coronavirus (SARS-CoV-2) causes pneumonia in Rhesus macaques. Cell Research, 30(8): 670−677. doi: 10.1038/s41422-020-0364-z
[15]	Shimizu M. 2019. Clinical features of cytokine storm syndrome. In: Cron RQ, Behrens EM. Cytokine Storm Syndrome. Cham: Springer, 31–41.
[16]	Song TZ, Han JB, Yang X, Li MH, Zheng YT. 2021. Tissue distribution of SARS-CoV-2 in non-human primates after combined intratracheal and intranasal inoculation. Science China Life Sciences. doi: 10.1007/s11427-020-1877-4.
[17]	Song TZ, Zheng HY, Han JB, Jin L, Yang X, Liu FL, et al. 2020. Delayed severe cytokine storm and immune cell infiltration in SARS-CoV-2-infected aged Chinese rhesus macaques. Zoological Research, 41(5): 503−516. doi: 10.24272/j.issn.2095-8137.2020.202
[18]	Woo PCY, Tung ETK, Chan KH, Lau CCY, Lau SKP, Yuen KY. 2010. Cytokine profiles induced by the novel swine-origin influenza A/H1N1 virus: implications for treatment strategies. The Journal of Infectious Diseases, 201(3): 346−353. doi: 10.1086/649785
[19]	Zhang MX, Zheng HY, Jiang J, Song JH, Chen M, Xiao Y, et al. 2018. Northern pig-tailed macaques (Macaca leonina) maintain superior CD4⁺ T-cell homeostasis during SIVmac239 infection. European Journal of Immunology, 48(2): 384−385. doi: 10.1002/eji.201747284
[20]	Zheng HW, Li H, Guo L, Liang Y, Li J, Wang X, et al. 2020. Virulence and pathogenesis of SARS-CoV-2 infection in rhesus macaques: a nonhuman primate model of COVID-19 progression. PLoS Pathogens, 16(11): e1008949. doi: 10.1371/journal.ppat.1008949