SARS-CoV-2 infection and disease outcomes in non-human primate models: advances and implications

References

• Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–506.
   PubMed Web of Science ®Google Scholar
• Xu Z, Shi L, Wang Y, et al. Pathological findings of covid-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8:420–422.
   PubMed Web of Science ®Google Scholar
• Wang T, Du Z, Zhu F, et al. Comorbidities and multi-organ injuries in the treatment of covid-19. Lancet. 2020;395:e52.
   PubMed Web of Science ®Google Scholar
• Poon LLM, Peiris M. Emergence of a novel human coronavirus threatening human health. Nat Med. 2020;26:317–319.
   PubMed Web of Science ®Google Scholar
• Petersen E, Koopmans M, Go U, et al. Comparing sars-cov-2 with sars-cov and influenza pandemics. Lancet Infect Dis. 2020;20:e238–e244.
   PubMed Web of Science ®Google Scholar
• Blanco-Melo D, Nilsson-Payant BE, Liu WC, et al. Imbalanced host response to sars-cov-2 drives development of covid-19. Cell. 2020;181:1036–1045. e1039.
   PubMed Web of Science ®Google Scholar
• Yuan L, Tang Q, Cheng T, et al. Animal models for emerging coronavirus: progress and new insights. Emerg Microbes Infect. 2020;9:949–961.
   PubMed Web of Science ®Google Scholar
• Marsh M, Helenius A. Virus entry: open sesame. Cell. 2006;124:729–740.
   PubMed Web of Science ®Google Scholar
• Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579:270–273.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhao Z, Wang Y, et al. Single-cell rna expression profiling of ace2, the receptor of sars-cov-2. Am J Respir Crit Care Med. 2020;202:756–759.
   PubMed Web of Science ®Google Scholar
• Zou X, Chen K, Zou JW, et al. Single-cell rna-seq data analysis on the receptor ace2 expression reveals the potential risk of different human organs vulnerable to 2019-ncov infection. Front Med-Prc. 2020;14:185–192.
   PubMed Web of Science ®Google Scholar
• Zhao B, Ni C, Gao R, et al. Recapitulation of sars-cov-2 infection and cholangiocyte damage with human liver ductal organoids. Protein Cell. 2020;11:771–775.
   PubMed Web of Science ®Google Scholar
• Pontelli MC, Castro IA, Martins RB, et al. Infection of human lymphomononuclear cells by sars-cov-2. bioRxiv: the preprint server for biology; 2020.
   Google Scholar
• Zang R, Castro MF G, McCune BT, et al. Tmprss2 and tmprss4 promote sars-cov-2 infection of human small intestinal enterocytes. Sci Immunol. 2020;5: eabc3582.
   PubMed Web of Science ®Google Scholar
• Sungnak W, Huang N, Becavin C, et al. Sars-cov-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med. 2020;26:681–687.
   PubMed Web of Science ®Google Scholar
• Jiao L, Yang Y, Yu W, et al. The olfactory route is a potential way for sars-cov-2 to invade the central nervous system of rhesus monkeys. Signal Transduct Target Ther. 2021;6:169.
   Web of Science ®Google Scholar
• Lu S, Zhao Y, Yu W, et al. Comparison of nonhuman primates identified the suitable model for covid-19. Signal Transduct Target Ther. 2020;5:157.
   PubMed Web of Science ®Google Scholar
• Deng W, Bao L, Liu J, et al. Primary exposure to sars-cov-2 protects against reinfection in rhesus macaques. Science. 2020;369:818–823.
   PubMed Web of Science ®Google Scholar
• Deng W, Bao L, Gao H, et al. Ocular conjunctival inoculation of sars-cov-2 can cause mild covid-19 in rhesus macaques. Nat Commun. 2020;11:4400.
   PubMed Web of Science ®Google Scholar
• Woolsey C, Borisevich V, Prasad AN, et al. Establishment of an african green monkey model for covid-19 and protection against re-infection. Nat Immunol. 2021;22:86–98.
   PubMed Web of Science ®Google Scholar
• Munster VJ, Feldmann F, Williamson BN, et al. Respiratory disease in rhesus macaques inoculated with sars-cov-2. Nature. 2020;585:268–272.
   PubMed Web of Science ®Google Scholar
• Rockx B, Kuiken T, Herfst S, et al. Comparative pathogenesis of covid-19, mers, and sars in a nonhuman primate model. Science. 2020;368:1012–1015.
   PubMed Web of Science ®Google Scholar
• Shan C, Yao YF, Yang XL, et al. Infection with novel coronavirus (sars-cov-2) causes pneumonia in rhesus macaques. Cell Res. 2020;30:670–677.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Ren L, Zhang L, et al. Heightened innate immune responses in the respiratory tract of covid-19 patients. Cell Host Microbe. 2020;27:883–890. e882.
   PubMed Web of Science ®Google Scholar
• Giamarellos-Bourboulis EJ, Netea MG, Rovina N, et al. Complex immune dysregulation in covid-19 patients with severe respiratory failure. Cell Host Microbe. 2020;27:992–1000. e1003.
   PubMed Web of Science ®Google Scholar
• Cao X. Covid-19: Immunopathology and its implications for therapy. Nat Rev Immunol. 2020;20:269–270.
   PubMed Web of Science ®Google Scholar
• Ziegler CGK, Allon SJ, Nyquist SK, et al. Sars-cov-2 receptor ace2 is an interferon-stimulated gene in human airway epithelial cells and is detected in specific cell subsets across tissues. Cell. 2020;181:1016–1035. e1019.
   PubMed Web of Science ®Google Scholar
• Wang J, Kaperak C, Sato T, et al. Covid-19 reinfection: a rapid systematic review of case reports and case series. J Investig Med: the Official Publication of the American Federation for Clinical Research. 2021;69:1253–1255.
   Web of Science ®Google Scholar
• Zhang B, Zhou X, Zhu C, et al. Immune phenotyping based on the neutrophil-to-lymphocyte ratio and igg level predicts disease severity and outcome for patients with covid-19. Front Mol Biosci. 2020;7:157.
   PubMed Web of Science ®Google Scholar
• Zhao J, Yuan Q, Wang H, et al. Antibody responses to sars-cov-2 in patients with novel coronavirus disease 2019. Clin Infect Dis: an Official Publication of the Infectious Diseases Society of America. 2020;71:2027–2034.
   PubMed Web of Science ®Google Scholar
• WTS YL, Kishikawa J-i, Hirose M, et al. An infectivity-enhancing site on the sars-cov-2 spike protein targeted by antibodies. Cell. 2021;184(13):3452-3466 e18.
   Web of Science ®Google Scholar
• Nie J, Li Q, Wu J, et al. Establishment and validation of a pseudovirus neutralization assay for sars-cov-2. Emerg Microbes Infect. 2020;9:680–686.
   PubMed Web of Science ®Google Scholar
• Ou X, Liu Y, Lei X, et al. Characterization of spike glycoprotein of sars-cov-2 on virus entry and its immune cross-reactivity with sars-cov. Nat Commun. 2020;11:1620.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang S, Wu Y, et al. Virus-free and live-cell visualizing sars-cov-2 cell entry for studies of neutralizing antibodies and compound inhibitors. Small Meth. 2021;5:2001031.
   Web of Science ®Google Scholar
• Liu C, Zhou Q, Li Y, et al. Research and development on therapeutic agents and vaccines for covid-19 and related human coronavirus diseases. ACS Cent Sci. 2020;6:315–331.
   PubMed Web of Science ®Google Scholar
• Gao Q, Bao L, Mao H, et al. Development of an inactivated vaccine candidate for sars-cov-2. Science. 2020;369:77–81.
   PubMed Web of Science ®Google Scholar
• Yadav PD, Ella R, Kumar S, et al. Immunogenicity and protective efficacy of inactivated sars-cov-2 vaccine candidate, bbv152 in rhesus macaques. Nat Commun. 2021;12:1386.
   PubMed Web of Science ®Google Scholar
• Wang H, Zhang Y, Huang B, et al. Development of an inactivated vaccine candidate, bbibp-corv, with potent protection against sars-cov-2. Cell. 2020;182:713–721. e719.
   PubMed Web of Science ®Google Scholar
• Yang J, Wang W, Chen Z, et al. A vaccine targeting the rbd of the s protein of sars-cov-2 induces protective immunity. Nature. 2020;586:572–577.
   PubMed Web of Science ®Google Scholar
• Liang JG, Su D, Song TZ, et al. S-trimer, a covid-19 subunit vaccine candidate, induces protective immunity in nonhuman primates. Nat Commun. 2021;12:1346.
   PubMed Web of Science ®Google Scholar
• Yu J, Tostanoski LH, Peter L, et al. DNA vaccine protection against sars-cov-2 in rhesus macaques. Science. 2020;369:806–811.
   PubMed Web of Science ®Google Scholar
• Li Y, Bi Y, Xiao H, et al. A novel DNA and protein combination covid-19 vaccine formulation provides full protection against sars-cov-2 in rhesus macaques. Emerg Microbes Infect. 2021;10:342–355.
   PubMed Web of Science ®Google Scholar
• Yang R, Deng Y, Huang B, et al. A core-shell structured covid-19 mrna vaccine with favorable biodistribution pattern and promising immunity. Signal Transduct Target Ther. 2021;6:213.
   PubMed Web of Science ®Google Scholar
• Corbett KS, Flynn B, Foulds KE, et al. Evaluation of the mrna-1273 vaccine against sars-cov-2 in nonhuman primates. N Engl J Med. 2020;383:1544–1555.
   PubMed Web of Science ®Google Scholar
• Zhang NN, Li XF, Deng YQ, et al. A thermostable mrna vaccine against covid-19. Cell. 2020;182:1271–1283. e1216.
   PubMed Web of Science ®Google Scholar
• Sanchez-Felipe L, Vercruysse T, Sharma S, et al. A single-dose live-attenuated yf17d-vectored sars-cov-2 vaccine candidate. Nature. 2021;590:320–325.
   Web of Science ®Google Scholar
• Mercado NB, Zahn R, Wegmann F, et al. Single-shot ad26 vaccine protects against sars-cov-2 in rhesus macaques. Nature. 2020;586:583–588.
   PubMed Web of Science ®Google Scholar
• Feng L, Wang Q, Shan C, et al. An adenovirus-vectored covid-19 vaccine confers protection from sars-cov-2 challenge in rhesus macaques. Nat Commun. 2020;11:4207.
   PubMed Web of Science ®Google Scholar
• Wang G, Yang ML, Duan ZL, et al. Dalbavancin binds ace2 to block its interaction with sars-cov-2 spike protein and is effective in inhibiting sars-cov-2 infection in animal models. Cell Res. 2021;31:17–24.
   PubMed Web of Science ®Google Scholar
• Lu S, Zhao J, Dong J, et al. Effective treatment of sars-cov-2-infected rhesus macaques by attenuating inflammation. Cell Res. 2021;31:229–232.
   Web of Science ®Google Scholar
• Baum A, Ajithdoss D, Copin R, et al. Regn-cov2 antibodies prevent and treat sars-cov-2 infection in rhesus macaques and hamsters. Science. 2020;370:1110–1115.
   PubMed Web of Science ®Google Scholar
• Shi R, Shan C, Duan X, et al. A human neutralizing antibody targets the receptor-binding site of sars-cov-2. Nature. 2020;584:120–124.
   PubMed Web of Science ®Google Scholar
• de Wit E, Feldmann F, Cronin J, et al. Prophylactic and therapeutic remdesivir (gs-5734) treatment in the rhesus macaque model of mers-cov infection. Proc Natl Acad Sci USA. 2020;117(12):6771–6776.
   PubMed Web of Science ®Google Scholar
• Lo MK, Feldmann F, Gary JM, et al. Remdesivir (gs-5734) protects African Green monkeys from nipah virus challenge. Sci Trans Med. 2019;11(494):eaau9242.
   PubMed Web of Science ®Google Scholar
• Williamson BN, Feldmann F, Schwarz B, et al. Clinical benefit of remdesivir in rhesus macaques infected with sars-cov-2. Nature. 2020;585(7824):273–276.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang D, Du G, et al. Remdesivir in adults with severe covid-19: a randomised, double-blind, placebo-controlled, multicentre trial. Lancet. 2020;395:1569–1578.
   PubMed Web of Science ®Google Scholar
• Thompson MG, Burgess JL, Naleway AL, et al. Prevention and attenuation of covid-19 with the bnt162b2 and mrna-1273 vaccines. N Engl J Med. 2021;385:320–329.
   PubMed Web of Science ®Google Scholar
• Sahin U, Muik A, Vogler I, et al. Bnt162b2 vaccine induces neutralizing antibodies and poly-specific t cells in humans. Nature. 2021;595:572–577.
   PubMed Web of Science ®Google Scholar
• Garcia-Beltran WF, Lam EC, St Denis K, et al. Multiple sars-cov-2 variants escape neutralization by vaccine-induced humoral immunity. Cell. 2021;184:2372–2383. e2379.
   PubMed Web of Science ®Google Scholar
• Kupferschmidt K. Fast-spreading U.K. virus variant raises alarms. Science. 2021;371:9–10.
   PubMed Web of Science ®Google Scholar
• Kemp SA, Collier DA, Datir RP, et al. Sars-cov-2 evolution during treatment of chronic infection. Nature. 2021;592:277–282.
   PubMed Web of Science ®Google Scholar
• Hou YJ, Chiba S, Halfmann P, et al. Sars-cov-2 d614 g variant exhibits efficient replication ex vivo and transmission in vivo. Science. 2020;370:1464–1468.
   PubMed Web of Science ®Google Scholar
• Plante JA, Liu Y, Liu J, et al. Spike mutation d614 g alters sars-cov-2 fitness. Nature. 2021;592:116–121.
   PubMed Web of Science ®Google Scholar
• Weissman D, Alameh MG, de Silva T, et al. D614 g spike mutation increases sars cov-2 susceptibility to neutralization. Cell Host Microbe. 2021;29:23–31. e24.
   PubMed Web of Science ®Google Scholar
• Wang P, Nair MS, Liu L, et al. Antibody resistance of sars-cov-2 variants b.1.351 and b.1.1.7. Nature. 2021;593:130–135.
   PubMed Web of Science ®Google Scholar
• Liu Y, Liu J, Xia H, et al. Neutralizing activity of bnt162b2-elicited serum. N Engl J Med. 2021;384:1466–1468.
   PubMed Web of Science ®Google Scholar
• Zhou D, Dejnirattisai W, Supasa P, et al. Evidence of escape of sars-cov-2 variant b.1.351 from natural and vaccine-induced sera. Cell. 2021;184:2348–2361. e2346.
   PubMed Web of Science ®Google Scholar
• Hu Z, Song C, Xu C, et al. Clinical characteristics of 24 asymptomatic infections with covid-19 screened among close contacts in Nanjing, China. Sci China Life Sci. 2020;63:706–711.
   PubMed Web of Science ®Google Scholar
• Bai Y, Yao L, Wei T, et al. Presumed asymptomatic carrier transmission of covid-19. Jama. 2020;323:1406–1407.
   PubMed Web of Science ®Google Scholar
• Xiao F, Tang M, Zheng X, et al. Evidence for gastrointestinal infection of sars-cov-2. Gastroenterology. 2020;158:1831–1833. e1833.
   PubMed Web of Science ®Google Scholar
• Gu J, Han B, Wang J. Covid-19: gastrointestinal manifestations and potential fecal-oral transmission. Gastroenterology. 2020;158:1518–1519.
   PubMed Web of Science ®Google Scholar
• Wang T, Chen R, Liu C, et al. Attention should be paid to venous thromboembolism prophylaxis in the management of covid-19. Lancet Haematol. 2020;7:e362–e363.
   PubMed Web of Science ®Google Scholar
• Liu Z, Li K, Cai Y, et al. Accelerated passage of gene-modified monkeys by hormone-induced precocious puberty. Natl Sci Rev. 2021;8(7):nwab083.
   Web of Science ®Google Scholar