A tug-of-war between severe acute respiratory syndrome coronavirus 2 and host antiviral defence: lessons from other pathogenic viruses

Sin-Yee Fung, Kit-San Yuen, Zi-Wei Ye, Chi-Ping Chan, Dong-Yan Jin, Sin-Yee Fung, Kit-San Yuen, Zi-Wei Ye, Chi-Ping Chan, Dong-Yan Jin

Abstract

World Health Organization has declared the ongoing outbreak of coronavirus disease 2019 (COVID-19) a Public Health Emergency of International Concern. The virus was named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) by the International Committee on Taxonomy of Viruses. Human infection with SARS-CoV-2 leads to a wide range of clinical manifestations ranging from asymptomatic, mild, moderate to severe. The severe cases present with pneumonia, which can progress to acute respiratory distress syndrome. The outbreak provides an opportunity for real-time tracking of an animal coronavirus that has just crossed species barrier to infect humans. The outcome of SARS-CoV-2 infection is largely determined by virus-host interaction. Here, we review the discovery, zoonotic origin, animal hosts, transmissibility and pathogenicity of SARS-CoV-2 in relation to its interplay with host antiviral defense. A comparison with SARS-CoV, Middle East respiratory syndrome coronavirus, community-acquired human coronaviruses and other pathogenic viruses including human immunodeficiency viruses is made. We summarize current understanding of the induction of a proinflammatory cytokine storm by other highly pathogenic human coronaviruses, their adaptation to humans and their usurpation of the cell death programmes. Important questions concerning the interaction between SARS-CoV-2 and host antiviral defence, including asymptomatic and presymptomatic virus shedding, are also discussed.

Keywords: 2019 novel coronavirus; COVID-19; Coronavirus; SARS-CoV; SARS-CoV-2; host antiviral response; type I interferon.

Figures

Figure 1.
Figure 1.
Genome organization of HCoVs. Schematic diagram of seven known HCoVs is shown (not in scale). The genes encoding structural proteins spike (S), envelope (E), membrane (M), and nucleocapsid (N) are in green. The gene encoding haemagglutinin-esterase (HE) in lineage A of betacoronaviruses is in orange. The genes encoding accessory proteins are in blue.
Figure 2.
Figure 2.
A working model of SARS-CoV-induced inflammasome activation. SARS-CoV can activate both signal 1 (priming) and signal 2 (activation). Upregulation of pro-IL-1β transcription is achieved by NF-κB activation. Two mechanisms of IL-1β maturation have been proposed. In the first model, potassium ion efflux is promoted by ORF3a and E proteins, leading to NLRP3 inflammasome assembly. Alternatively, ORF3a promotes ASC ubiquitination and consequent assembly of inflammasome. ORG8b interacts with and activates NLRP3. Activation of inflammasome leads to proteolytic cleavage of pro-caspase 1 and pro-IL-1β. ASC, apoptosis-associated speck-like protein containing a CARD. CASP1, caspase 1. IKK, IκB kinase. IL-1, interleukin-1. LPS, lipopolysaccharides. NLRP3, NACHT, LRR, and PYD domains-containing protein 3. NEMO, NF-κB essential modulator. TNF-α, tumour necrosis factor α.

References

    1. Woo PC, Lau SK, Lam CS, et al. . Discovery of seven novel mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol. 2012;86:3995–4008. doi: 10.1128/JVI.06540-11
    1. Kendall EJ, Bynoe ML, Tyrrell DA.. Virus isolations from common colds occurring in a residential school. Br Med J. 1962;2:82–86. doi: 10.1136/bmj.2.5297.82
    1. McIntosh K, Dees JH, Becker WB, et al. . Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc Natl Acad Sci USA. 1967;57:933–940. doi: 10.1073/pnas.57.4.933
    1. McIntosh K. Coronaviruses: a comparative review. Curr Top Microbiol Immunol. 1974;63:85–129.
    1. Pene F, Merlat A, Vabret A, et al. . Coronavirus 229E-related pneumonia in immunocompromised patients. Clin Infect Dis. 2003;37:929–932. doi: 10.1086/377612
    1. Bonavia A, Arbour N, Yong VW, et al. . Infection of primary cultures of human neural cells by human coronaviruses 229E and OC43. J Virol. 1997;71:800–806. doi: 10.1128/JVI.71.1.800-806.1997
    1. Perlman S, Netland J.. Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol. 2009;7:439–450. doi:10.1038/nrmicro2147.
    1. Stein RA. Super-spreaders in infectious diseases. Int J Infect Dis. 2011;15:e510–e513. doi: 10.1016/j.ijid.2010.06.020
    1. Peiris JS, Lai ST, Poon LL, et al. . Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet. 2003;361:1319–1325. doi: 10.1016/S0140-6736(03)13077-2
    1. Leung WK, To KF, Chan PK, et al. . Enteric involvement of severe acute respiratory syndrome-associated coronavirus infection. Gastroenterology. 2003;125:1011–1017. doi: 10.1016/j.gastro.2003.08.001
    1. Xu J, Zhong S, Liu J, et al. . Detection of severe acute respiratory syndrome coronavirus in the brain: potential role of the chemokine mig in pathogenesis. Clin Infect Dis. 2005;41:1089–1096. doi: 10.1086/444461
    1. Desmyter J, Melnick JL, Rawls WE.. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J Virol. 1968;2:955–961. doi: 10.1128/JVI.2.10.955-961.1968
    1. Zornetzer GA, Frieman MB, Rosenzweig E, et al. . Transcriptomic analysis reveals a mechanism for a prefibrotic phenotype in STAT1 knockout mice during severe acute respiratory syndrome coronavirus infection. J Virol. 2010;84:11297–11309. doi: 10.1128/JVI.01130-10
    1. van der Hoek L, Pyrc K, Jebbink MF, et al. . Identification of a new human coronavirus. Nat Med. 2004;10:368–373. doi: 10.1038/nm1024
    1. Lau SK, Woo PC, Yip CC, et al. . Coronavirus HKU1 and other coronavirus infections in Hong Kong. J Clin Microbiol. 2006;44:2063–2071. doi: 10.1128/JCM.02614-05
    1. van der Hoek L, Sure K, Ihorst G, et al. . Croup is associated with the novel coronavirus NL63. PLoS Med. 2005;2:e240. doi: 10.1371/journal.pmed.0020240
    1. Wang Y, Li X, Liu W, et al. . Discovery of a subgenotype of human coronavirus NL63 associated with severe lower respiratory tract infection in China, 2018. Emerg Microbes Infect. 2020;9:246–255. doi: 10.1080/22221751.2020.1717999
    1. Zaki AM, van Boheemen S, Bestebroer TM, et al. . Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814–1820. doi: 10.1056/NEJMoa1211721
    1. Zumla A, Hui DS, Perlman S.. Middle East respiratory syndrome. Lancet. 2015;386:995–1007. doi: 10.1016/S0140-6736(15)60454-8
    1. Zhou J, Li C, Zhao G, et al. . Human intestinal tract serves as an alternative infection route for Middle East respiratory syndrome coronavirus. Sci Adv. 2017;3:eaao4966. doi: 10.1126/sciadv.aao4966
    1. Yeung ML, Yao Y, Jia L, et al. . MERS coronavirus induces apoptosis in kidney and lung by upregulating Smad7 and FGF2. Nat Microbiol. 2016;1:16004. doi: 10.1038/nmicrobiol.2016.4
    1. Ogando NS, Ferron F, Decroly E, et al. . The curious case of the nidovirus exoribonuclease: its role in RNA synthesis and replication fidelity. Front Microbiol. 2019; 10:1813. doi: 10.3389/fmicb.2019.01813
    1. Collins ND, Beck AS, Widen SG, et al. . Structural and nonstructural genes contribute to the genetic diversity of RNA viruses. mBio. 2018;9:e01871–18. doi: 10.1128/mBio.01871-18
    1. Zhao Z, Li H, Wu X, et al. . Moderate mutation rate in the SARS coronavirus genome and its implications. BMC Evol Biol. 2004;4:21. doi: 10.1186/1471-2148-4-21
    1. Jiang S, Du L, Shi Z.. An emerging coronavirus causing pneumonia outbreak in Wuhan, China: calling for developing therapeutic and prophylactic strategies. Emerg Microbes Infect. 2020;9:275–277. doi: 10.1080/22221751.2020.1723441
    1. Vijgen L, Keyaerts E, Moës E, et al. . Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J Virol. 2005;79:1595–1604. doi: 10.1128/JVI.79.3.1595-1604.2005
    1. Corman VM, Muth D, Niemeyer D, et al. . Hosts and sources of endemic human coronaviruses. Adv Virus Res. 2018;100:163–188. doi: 10.1016/bs.aivir.2018.01.001
    1. Guan Y, Zheng BJ, He YQ, et al. . Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science. 2003;302:276–278. doi: 10.1126/science.1087139
    1. Tu C, Crameri G, Kong X, et al. . Antibodies to SARS coronavirus in civets. Emerg Infect Dis. 2004;10:2244–2248. doi: 10.3201/eid1012.040520
    1. Lau SK, Woo PC, Li KS, et al. . Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA. 2005;102:14040–14045. doi: 10.1073/pnas.0506735102
    1. Li W, Shi Z, Yu M, et al. . Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391
    1. Ge XY, Li JL, Yang XL, et al. . Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature. 2013;503:535–538. doi: 10.1038/nature12711
    1. Adney DR, van Doremalen N, Brown VR, et al. . Replication and shedding of MERS-CoV in upper respiratory tract of inoculated dromedary camels. Emerg Infect Dis. 2014;20:1999–2005. doi: 10.3201/eid2012.141280
    1. Kandeil A, Gomaa M, Shehata M, et al. . Middle East respiratory syndrome coronavirus infection in non-camelid domestic mammals. Emerg Microbes Infect. 2019;8:103–108. doi: 10.1080/22221751.2018.1560235
    1. Zhou P, Yang X, Wang X, et al. . A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020. doi:10.1038/s41586-020-2012-7.
    1. 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. doi: 10.1016/S0140-6736(20)30183-5
    1. Liu P, Chen W, Chen JP.. Viral metagenomics revealed Sendai virus and coronavirus infection of Malayan pangolins (Manis javanica). Viruses. 2019;11:E979. doi: 10.3390/v11110979
    1. Calisher CH, Childs JE, Field HE, et al. . Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006;19:531–545. doi: 10.1128/CMR.00017-06
    1. Zhang G, Cowled C, Shi Z, et al. . Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science. 2013;339:456–460. doi: 10.1126/science.1230835
    1. Ahn M, Anderson DE, Zhang Q, et al. . Dampened NLRP3-mediated inflammation in bats and implications for a special viral reservoir host. Nat Microbiol. 2019;4:789–799. doi: 10.1038/s41564-019-0371-3
    1. Zhou P, Tachedjian M, Wynne JW, et al. . Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats. Proc Natl Acad Sci USA. 2016;113:2696–2701. doi: 10.1073/pnas.1518240113
    1. Xie J, Li Y, Shen X, et al. . Dampened STING-dependent interferon activation in bats. Cell Host Microbe. 2018;23:297–301. doi: 10.1016/j.chom.2018.01.006
    1. Pavlovich SS, Lovett SP, Koroleva G, et al. . The Egyptian rousette genome reveals unexpected features of bat antiviral immunity. Cell. 2018;173:1098–1110. doi: 10.1016/j.cell.2018.03.070
    1. Sharp PM, Hahn BH.. Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med. 2011;1:a006841. doi: 10.1101/cshperspect.a006841
    1. Buffalo CZ, Stürzel CM, Heusinger E, et al. . Structural basis for tetherin antagonism as a barrier to zoonotic lentiviral transmission. Cell Host Microbe. 2019;26:359–368. doi: 10.1016/j.chom.2019.08.002
    1. Chan CP, Kok KH, Jin DY.. Human T-cell leukemia virus type 1 infection and adult T-cell leukemia. Adv Exp Med Biol. 2017;1018:147–166. doi: 10.1007/978-981-10-5765-6_9
    1. Mahieux R, Gessain A.. HTLV-3/STLV-3 and HTLV-4 viruses: discovery, epidemiology, serology and molecular aspects. Viruses. 2011;3:10740–10790. doi: 10.3390/v3071074
    1. Chan JF, Kok KH, Zhu Z, et al. . Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect. 2020;9:221–236. doi: 10.1080/22221751.2020.1719902
    1. Wong LY, Lui PY, Jin DY.. A molecular arms race between host innate antiviral response and emerging human coronaviruses. Virol Sin. 2016;31:12–23. doi: 10.1007/s12250-015-3683-3
    1. Shi CS, Nabar NR, Huang NN, et al. . SARS-Coronavirus open reading frame-8b triggers intracellular stress pathways and activates NLRP3 inflammasomes. Cell Death Discov. 2019;5:101. doi: 10.1038/s41420-019-0181-7
    1. Chan JF, Yuan S, Kok KH, et al. . A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020;395:513–524. doi: 10.1016/S0140-6736(20)30154-9
    1. Shen Z, Ning F, Zhou W, et al. . Superspreading SARS events, Beijing, 2003. Emerg Infect Dis. 2004;10:256–260. doi: 10.3201/eid1002.030732
    1. Holshue ML, DeBolt C, Lindquist S, et al. . First case of 2019 novel coronavirus in the United States. N Engl J Med. 2020. doi:10.1056/NEJMoa2001191.
    1. Bai Y, Yao L, Wei T, et al. . Presumed asymptomatic carrier transmission of COVID-19. JAMA. 2020. doi:10.1001/jama.2020.1585.
    1. Heimdal I, Moe N, Krokstad S, et al. . Human coronavirus in hospitalized children with respiratory tract infections: a 9-year population-based study from Norway. J Infect Dis. 2019;219:1198–1206. doi: 10.1093/infdis/jiy646
    1. Lau SK, Feng Y, Chen H, et al. . Severe acute respiratory syndrome (SARS) coronavirus ORF8 protein is acquired from SARS-related coronavirus from greater horseshoe bats through recombination. J Virol. 2015;89:10532–10547. doi: 10.1128/JVI.01048-15
    1. Huynh J, Li S, Yount B, et al. . Evidence supporting a zoonotic origin of human coronavirus strain NL63. J Virol. 2012;86:12816–12825. doi: 10.1128/JVI.00906-12
    1. Higgins PG, Phillpotts RJ, Scott GM, et al. . Intranasal interferon as protection against experimental respiratory coronavirus infection in volunteers. Antimicrob Agents Chemother. 1983;24:713–715. doi: 10.1128/AAC.24.5.713
    1. Mesel-Lemoine M, Millet J, Vidalain PO, et al. . A human coronavirus responsible for the common cold massively kills dendritic cells but not monocytes. J Virol. 2012;86:7577–7587. doi: 10.1128/JVI.00269-12
    1. Siu KL, Yeung ML, Kok KH, et al. . Middle East respiratory syndrome coronavirus 4a protein is a double-stranded RNA-binding protein that suppresses PACT-induced activation of RIG-I and MDA5 in the innate antiviral response. J Virol. 2014;88:4866–4876. doi: 10.1128/JVI.03649-13
    1. Siu KL, Kok KH, Ng MH, et al. . Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3.TANK.TBK1/IKKε complex. J Biol Chem. 2009;284:16202–16209. doi: 10.1074/jbc.M109.008227
    1. Lui PY, Wong LY, Fung CL, et al. . Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3. Emerg Microbes Infect. 2016;5:e39. doi: 10.1038/emi.2016.33
    1. Shen Z, Wang G, Yang Y, et al. . A conserved region of nonstructural protein 1 from alphacoronaviruses inhibits host gene expression and is critical for viral virulence. J Biol Chem. 2019;294:13606–13618. doi: 10.1074/jbc.RA119.009713
    1. Tohya Y, Narayanan K, Kamitani W, et al. . Suppression of host gene expression by nsp1 proteins of group 2 bat coronaviruses. J Virol. 2009;83:5282–5288. doi: 10.1128/JVI.02485-08
    1. Drappier M, Michiels T.. Inhibition of the OAS/RNase L pathway by viruses. Curr Opin Virol. 2015;15:19–26. doi: 10.1016/j.coviro.2015.07.002
    1. Forni D, Cagliani R, Clerici M, et al. . Molecular evolution of human coronavirus genomes. Trends Microbiol. 2017;25:35–48. doi: 10.1016/j.tim.2016.09.001
    1. Thornbrough JM, Jha BK, Yount B, et al. . Middle East respiratory syndrome coronavirus NS4b protein inhibits host RNase L activation. mBio. 2016;7:e00258. doi: 10.1128/mBio.00258-16
    1. Danthi P. Viruses and the diversity of cell death. Annu Rev Virol. 2016;3:533–553. doi: 10.1146/annurev-virology-110615-042435
    1. Upton JW, Chan FK.. Staying alive: cell death in antiviral immunity. Mol Cell. 2014;54:273–280. doi: 10.1016/j.molcel.2014.01.027
    1. Richard A, Tulasne D.. Caspase cleavage of viral proteins, another way for viruses to make the best of apoptosis. Cell Death Dis. 2012;3:e277. doi: 10.1038/cddis.2012.18
    1. He L, Ding Y, Zhang Q, et al. . Expression of elevated levels of pro-inflammatory cytokines in SARS-CoV-infected ACE2+ cells in SARS patients: relation to the acute lung injury and pathogenesis of SARS. J Pathol. 2006;210:288–297. doi: 10.1002/path.2067
    1. Tang BS, Chan KH, Cheng VC, et al. . Comparative host gene transcription by microarray analysis early after infection of the Huh7 cell line by severe acute respiratory syndrome coronavirus and human coronavirus 229E. J Virol. 2005;79:6180–6193. doi: 10.1128/JVI.79.10.6180-6193.2005
    1. Siu KL, Yuen KS, Castaño-Rodriguez C, et al. . Severe acute respiratory syndrome coronavirus ORF3a protein activates the NLRP3 inflammasome by promoting TRAF3-dependent ubiquitination of ASC. FASEB J. 2019;33:8865–8877. doi: 10.1096/fj.201802418R
    1. Nieto-Torres JL, DeDiego ML, Verdiá-Báguena C, et al. . Severe acute respiratory syndrome coronavirus envelope protein ion channel activity promotes virus fitness and pathogenesis. PLoS Pathog. 2014;10:e1004077. doi: 10.1371/journal.ppat.1004077
    1. DeDiego ML, Nieto-Torres JL, Regla-Nava JA, et al. . Inhibition of NF-κB-mediated inflammation in severe acute respiratory syndrome coronavirus-infected mice increases survival. J Virol. 2014;88:913–924. doi: 10.1128/JVI.02576-13
    1. Nieto-Torres JL, Verdiá-Báguena C, Jimenez-Guardeño JM, et al. . Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology. 2015;485:330–339. doi: 10.1016/j.virol.2015.08.010
    1. Chen IY, Moriyama M, Chang MF, et al. . Severe acute respiratory syndrome coronavirus viroporin 3a activates the NLRP3 inflammasome. Front Microbiol. 2019;10:50. doi: 10.3389/fmicb.2019.00050
    1. Chau TN, Lee KC, Yao H, et al. . SARS-associated viral hepatitis caused by a novel coronavirus: report of three cases. Hepatology. 2004;39:302–310. doi: 10.1002/hep.20111
    1. Tan YX, Tan TH, Lee MJ, et al. . Induction of apoptosis by the severe acute respiratory syndrome coronavirus 7a protein is dependent on its interaction with the Bcl-XL protein. J Virol. 2007;81:6346–6355. doi: 10.1128/JVI.00090-07
    1. Yue Y, Nabar NR, Shi CS, et al. . SARS-coronavirus open reading frame-3a drives multimodal necrotic cell death. Cell Death Dis. 2018;9:904. doi: 10.1038/s41419-018-0917-y

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다