Pathogenic human coronavirus infections: causes and consequences of cytokine storm and immunopathology

Springer Science and Business Media LLC - Tập 39 Số 5 - Trang 529-539 - 2017
Rudragouda Channappanavar1, Stanley Perlman1
1Department of Microbiology, University of Iowa, BSB 3-712, Iowa City, IA, 52242, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Masters PS, Perlman, S (2013) Coronaviridae. In: Knipe DM, Howley P (eds) Fields Virology. Lippincott Williams and Wilkins, Philadelphia, PA, pp 825–858

Siddell SZJ, Snijder EJ (2005) Coronaviruses, toroviruses, and arteriviruses, vol. 1. Hodder Arnold, London

Peck KM et al (2015) Coronavirus host range expansion and Middle East respiratory syndrome coronavirus emergence: biochemical mechanisms and evolutionary perspectives. Annu Rev Virol 2(1):95–117

Su S et al (2016) Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 24(6):490–502

Weiss SR, Navas-Martin S (2005) Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 69(4):635–664

Heugel J et al (2007) Coronavirus-associated pneumonia in previously healthy children. Pediatr Infect Dis J 26(8):753–755

Kuypers J et al (2007) Clinical disease in children associated with newly described coronavirus subtypes. Pediatrics 119(1):e70–e76

Drosten C et al (2003) Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348(20):1967–1976

Kuiken T et al (2003) Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362(9380):263–270

Peiris JS et al (2003) Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361(9366):1319–1325

van Boheemen S et al (2012) Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio 3(6)

Zaki AM et al (2012) Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367(19):1814–1820

Perlman S, Netland J (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7(6):439–450

WHO Cumulative number of reported probable cases of SARS. In: 2003

http://www.who.int/csr/disease/coronavirus_infections/MERS_CoV_RA_20140613.pdf WUoM-CTfAtHaIRfA-RGLaoMAf

WHO: Middle East respiratory syndrome coronavirus (MERS-CoV). http://www.who.int/emergencies/mers-cov/en/

Adney DR et al (2014) Replication and shedding of MERS-CoV in upper respiratory tract of inoculated dromedary camels. Emerg Infect Dis 20(12):1999–2005

Alagaili AN et al (2014) Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. MBio 5(2):e00884–e00814

Ge XY et al (2013) Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503(7477):535–538

Menachery VD et al (2015) A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat Med 21(12):1508–1513

Arabi YM et al (2014) Clinical course and outcomes of critically ill patients with Middle East respiratory syndrome coronavirus infection. Ann Intern Med 160(6):389–397

Assiri A et al (2013) Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study. Lancet Infect Dis 13(9):752–761

Leong HN et al (2006) Clinical and laboratory findings of SARS in Singapore. Ann Acad Med Singap 35(5):332–339

Saad M et al (2014) Clinical aspects and outcomes of 70 patients with Middle East respiratory syndrome coronavirus infection: a single-center experience in Saudi Arabia. Int J Infect Dis 29:301–306

Al-Tawfiq JA et al (2014) Middle East respiratory syndrome coronavirus: a case-control study of hospitalized patients. Clin Infect Dis 59(2):160–165

Zumla A et al (2015) Middle East respiratory syndrome. Lancet 386(9997):995–1007

Peiris JS et al (2004) Severe acute respiratory syndrome. Nat Med 10(12 Suppl):S88–S97

Peiris JS et al (2003) Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361(9371):1767–1772

Nicholls J et al (2003) SARS: clinical virology and pathogenesis. Respirology 8(Suppl):S6–S8

van den Brand JM et al (2014) The pathology and pathogenesis of experimental severe acute respiratory syndrome and influenza in animal models. J Comp Pathol 151(1):83–112

Gu J et al (2005) Multiple organ infection and the pathogenesis of SARS. J Exp Med 202(3):415–424

Nicholls JM et al (2003) Lung pathology of fatal severe acute respiratory syndrome. Lancet 361(9371):1773–1778

van den Brand JM et al (2014) The pathology and pathogenesis of experimental severe acute respiratory syndrome and influenza in animal models. J Comp Pathol 151(1):83–112

Cui W et al (2003) Expression of lymphocytes and lymphocyte subsets in patients with severe acute respiratory syndrome. Clin Infect Dis 37(6):857–859

Li T et al (2004) Significant changes of peripheral T lymphocyte subsets in patients with severe acute respiratory syndrome. J Infect Dis 189(4):648–651

Wang YH et al (2004) A cluster of patients with severe acute respiratory syndrome in a chest ward in southern Taiwan. Intensive Care Med 30(6):1228–1231

Ng DL et al (2016) Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal case of Middle East respiratory syndrome coronavirus infection in the United Arab Emirates, April 2014. Am J Pathol 186(3):652–658

Channappanavar R et al (2016) Dysregulated type I interferon and inflammatory monocyte-macrophage responses cause lethal pneumonia in SARS-CoV-infected mice. Cell Host Microbe 19(2):181–193

Davidson S et al (2015) Disease-promoting effects of type I interferons in viral, bacterial, and coinfections. J Interf Cytokine Res 35(4):252–264

Shaw AC et al (2013) Age-dependent dysregulation of innate immunity. Nat Rev Immunol 13(12):875–887

Cheung CY et al (2005) Cytokine responses in severe acute respiratory syndrome coronavirus-infected macrophages in vitro: possible relevance to pathogenesis. J Virol 79(12):7819–7826

Law HK et al (2005) Chemokine up-regulation in SARS-coronavirus-infected, monocyte-derived human dendritic cells. Blood 106(7):2366–2374

Yen YT et al (2006) Modeling the early events of severe acute respiratory syndrome coronavirus infection in vitro. J Virol 80(6):2684–2693

Chien JY et al (2006) Temporal changes in cytokine/chemokine profiles and pulmonary involvement in severe acute respiratory syndrome. Respirology 11(6):715–722

Wang CH et al (2005) Persistence of lung inflammation and lung cytokines with high-resolution CT abnormalities during recovery from SARS. Respir Res 6:42

Wong CK et al (2004) Plasma inflammatory cytokines and chemokines in severe acute respiratory syndrome. Clin Exp Immunol 136(1):95–103

Zhang Y et al (2004) Analysis of serum cytokines in patients with severe acute respiratory syndrome. Infect Immun 72(8):4410–4415

Cameron MJ et al (2008) Human immunopathogenesis of severe acute respiratory syndrome (SARS). Virus Res 133(1):13–19

Cameron MJRL, Xu L, Danesh A, Bermejo-Martin JF, Cameron CM, Muller MP, Gold WL, Richardson SE, Poutanen SM, Willey BM, DeVries ME, Fang Y, Seneviratne C, Bosinger SE, Persad D, Keshavjee S, Louie M, Loeb MB, Brunton J, McGeer AJ, Kelvin DJ (2007) Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J Virol 81(16):8692–8706

Huang KJ et al (2005) An interferon-gamma-related cytokine storm in SARS patients. J Med Virol 75(2):185–194

Theron M et al (2005) A probable role for IFN-gamma in the development of a lung immunopathology in SARS. Cytokine 32(1):30–38

Lau SK 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. J Gen Virol 94(Pt 12):2679–2690

Chu H et al (2015) Middle East respiratory syndrome coronavirus efficiently infects human primary T lymphocytes and activates the extrinsic and intrinsic apoptosis pathways. J Infect Dis 213(6):904–14

Tynell J et al (2016) Middle East respiratory syndrome coronavirus shows poor replication but significant induction of antiviral responses in human monocyte-derived macrophages and dendritic cells. J Gen Virol 97(2):344–355

Zhou J et al (2014) Active replication of Middle East respiratory syndrome coronavirus and aberrant induction of inflammatory cytokines and chemokines in human macrophages: implications for pathogenesis. J Infect Dis 209(9):1331–1342

Scheuplein VA et al (2015) High secretion of interferons by human plasmacytoid dendritic cells upon recognition of Middle East respiratory syndrome coronavirus. J Virol 89(7):3859–3869

Kim ES et al (2016) Clinical progression and cytokine profiles of Middle East respiratory syndrome coronavirus infection. J Korean Med Sci 31(11):1717–1725

Min CK et al (2016) Comparative and kinetic analysis of viral shedding and immunological responses in MERS patients representing a broad spectrum of disease severity. Sci Rep 6:25359

Roberts A et al (2005) Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J Virol 79(9):5833–5838

Day CW et al (2009) A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology 395(2):210–222

Nagata N et al (2008) Mouse-passaged severe acute respiratory syndrome-associated coronavirus leads to lethal pulmonary edema and diffuse alveolar damage in adult but not young mice. Am J Pathol 172(6):1625–1637

Roberts A et al (2007) A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog 3(1):e5

Frieman MB et al (2010) SARS-CoV pathogenesis is regulated by a STAT1 dependent but a type I, II and III interferon receptor independent mechanism. PLoS Pathog 6(4):e1000849

Zhao J et al (2011) Age-related increases in PGD(2) expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J Clin Invest 121(12):4921–4930

Graham RL et al (2012) A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat Med 18(12):1820–1826

Rockx B et al (2009) Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. J Virol 83(14):7062–7074

Smits SL et al (2010) Exacerbated innate host response to SARS-CoV in aged non-human primates. PLoS Pathog 6(2):e1000756

Totura AL et al (2015) Toll-like receptor 3 signaling via TRIF contributes to a protective innate immune response to severe acute respiratory syndrome coronavirus infection. MBio 6(3):e00638–e00615

Jimenez-Guardeno JM et al (2014) The PDZ-binding motif of severe acute respiratory syndrome coronavirus envelope protein is a determinant of viral pathogenesis. PLoS Pathog 10(8):e1004320

Nieto-Torres JL et al (2014) Severe acute respiratory syndrome coronavirus envelope protein ion channel activity promotes virus fitness and pathogenesis. PLoS Pathog 10(5):e1004077

Nieto-Torres JL et al (2015) Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology 485:330–339

de Wit E et al (2013) Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. Proc Natl Acad Sci U S A 110(41):16598–16603

Haagmans BL et al (2015) Asymptomatic Middle East respiratory syndrome coronavirus infection in rabbits. J Virol 89(11):6131–6135

Houser KV et al (2016) Prophylaxis with a Middle East respiratory syndrome coronavirus (MERS-CoV)-specific human monoclonal antibody protects rabbits from MERS-CoV infection. J Infect Dis 213(10):1557–1561

Falzarano D et al (2014) Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog 10(8):e1004250

Johnson RF et al (2015) Intratracheal exposure of common marmosets to MERS-CoV Jordan-n3/2012 or MERS-CoV EMC/2012 isolates does not result in lethal disease. Virology 485:422–430

Barlan A et al (2014) Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J Virol 88(9):4953–4961

Zhao J et al (2014) Rapid generation of a mouse model for Middle East respiratory syndrome. Proc Natl Acad Sci U S A 111(13):4970–4975

Gretebeck LM, Subbarao K (2015) Animal models for SARS and MERS coronaviruses. Curr Opin Virol 13:123–129

van Doremalen N, Munster VJ (2015) Animal models of Middle East respiratory syndrome coronavirus infection. Antivir Res 122:28–38

Pascal KE et al (2015) Pre- and postexposure efficacy of fully human antibodies against Spike protein in a novel humanized mouse model of MERS-CoV infection. Proc Natl Acad Sci U S A 112(28):8738–8743

Cockrell A et al (2016) A mouse model for MERS coronavirus-induced acute respiratory distress syndrome. Nature Microbiology 2:16226

Li K et al (2017) Mouse-adapted MERS coronavirus causes lethal lung disease in human DPP4 knockin mice. Proceedings of the National Academy of Sciences 114(15):E3119–E3128

Frieman M et al (2007) Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J Virol 81(18):9812–9824

Kindler E et al (2016) Interaction of SARS and MERS coronaviruses with the antiviral interferon response. Adv Virus Res 96:219–243

Narayanan K et al (2008) Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J Virol 82(9):4471–4479

Sun L et al (2012) Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PLoS One 7(2):e30802

Thiel V, Weber F (2008) Interferon and cytokine responses to SARS-coronavirus infection. Cytokine Growth Factor Rev 19(2):121–132

Totura AL, Baric RS (2012) SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon. Current Opinion in Virology 2(3):264–275

Wathelet MG et al (2007) Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81(21):11620–11633

Fehr AR et al (2016) The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection. mBio 7(6):e01721–16

Frieman M et al (2009) Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J Virol 83(13):6689–6705

Kopecky-Bromberg SA et al (2007) Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J Virol 81(2):548–557

Lu XL et al (2011) SARS-CoV nucleocapsid protein antagonizes IFN-beta response by targeting initial step of IFN-beta induction pathway, and its C-terminal region is critical for the antagonism. Virus Genes 42(1):37–45

Siu KL et al (2014) Suppression of innate antiviral response by severe acute respiratory syndrome coronavirus M protein is mediated through the first transmembrane domain. Cell Mol Immunol 11(2):141–149

Lui PY et al (2016) Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3. Emerg Microbes Infect 5:e39

Yang Y et al (2013) The structural and accessory proteins M, ORF 4a, ORF 4b, and ORF 5 of Middle East respiratory syndrome coronavirus (MERS-CoV) are potent interferon antagonists. Protein Cell 4(12):951–961

Chu CM et al (2004) Initial viral load and the outcomes of SARS. CMAJ 171(11):1349–1352

Ng ML et al (2003) Proliferative growth of SARS coronavirus in Vero E6 cells. J Gen Virol 84(Pt 12):3291–3303

Oh MD et al (2016) Viral load kinetics of MERS coronavirus infection. N Engl J Med 375(13):1303–1305

Herold S et al (2008) Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 205(13):3065–3077

Hogner K et al (2013) Macrophage-expressed IFN-beta contributes to apoptotic alveolar epithelial cell injury in severe influenza virus pneumonia. PLoS Pathog 9(2):e1003188

Rodrigue-Gervais IG et al (2014) Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival. Cell Host Microbe 15(1):23–35

Zhao J et al (2010) T cell responses are required for protection from clinical disease and for virus clearance in severe acute respiratory syndrome coronavirus-infected mice. J Virol 84(18):9318–9325

Kim KD et al (2007) Adaptive immune cells temper initial innate responses. Nat Med 13(10):1248–1252

Palm NW, Medzhitov R (2007) Not so fast: adaptive suppression of innate immunity. Nat Med 13(10):1142–1144

Zornetzer GA et al (2010) Transcriptomic analysis reveals a mechanism for a prefibrotic phenotype in STAT1 knockout mice during severe acute respiratory syndrome coronavirus infection. J Virol 84(21):11297–11309

Page C et al (2012) Induction of alternatively activated macrophages enhances pathogenesis during severe acute respiratory syndrome coronavirus infection. J Virol 86(24):13334–13349

Gralinski LE et al (2015) Genome wide identification of SARS-CoV susceptibility loci using the collaborative cross. PLoS Genet 11(10):e1005504

Drosten C et al (2013) Clinical features and virological analysis of a case of Middle East respiratory syndrome coronavirus infection. Lancet Infect Dis 13(9):745–751

Lew TW et al (2003) Acute respiratory distress syndrome in critically ill patients with severe acute respiratory syndrome. JAMA 290(3):374–380

Jiang Y et al (2005) Characterization of cytokine/chemokine profiles of severe acute respiratory syndrome. Am J Respir Crit Care Med 171(8):850–857

Reghunathan R et al (2005) Expression profile of immune response genes in patients with Severe Acute Respiratory Syndrome. BMC Immunology 6:2

Stockman LJ et al (2006) SARS: systematic review of treatment effects. PLoS Med 3(9):e343

Al-Tawfiq JA et al (2014) Ribavirin and interferon therapy in patients infected with the Middle East respiratory syndrome coronavirus: an observational study. Int J Infect Dis 20:42–46

Falzarano D et al (2013) Treatment with interferon-alpha2b and ribavirin improves outcome in MERS-CoV-infected rhesus macaques. Nat Med 19(10):1313–1317

Omrani AS et al (2014) Ribavirin and interferon alfa-2a for severe Middle East respiratory syndrome coronavirus infection: a retrospective cohort study. Lancet Infect Dis 14(11):1090–1095

Auyeung TW et al (2005) The use of corticosteroid as treatment in SARS was associated with adverse outcomes: a retrospective cohort study. J Infect 51(2):98–102

Ho JC et al (2003) High-dose pulse versus nonpulse corticosteroid regimens in severe acute respiratory syndrome. Am J Respir Crit Care Med 168(12):1449–1456

Yam LY et al (2007) Corticosteroid treatment of severe acute respiratory syndrome in Hong Kong. J Infect 54(1):28–39

Haagmans BL et al (2004) Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. Nat Med 10(3):290–293

Zumla A et al (2016) Coronaviruses—drug discovery and therapeutic options. Nat Rev Drug Discov 15(5):327–47

Davidson S et al (2016) IFNlambda is a potent anti-influenza therapeutic without the inflammatory side effects of IFNalpha treatment. EMBO Mol Med 8(9):1099–1112

Blazek K et al (2015) IFN-lambda resolves inflammation via suppression of neutrophil infiltration and IL-1beta production. J Exp Med 212(6):845–853

Imai Y et al (2008) Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133(2):235–249

Shirey KA et al (2013) The TLR4 antagonist Eritoran protects mice from lethal influenza infection. Nature 497(7450):498–502

Teijaro JR et al (2011) Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146(6):980–991

Walsh KB et al (2011) Suppression of cytokine storm with a sphingosine analog provides protection against pathogenic influenza virus. Proc Natl Acad Sci U S A 108(29):12018–12023

Leuschner F et al (2015) Silencing of CCR2 in myocarditis. Eur Heart J 36(23):1478–1488

Leuschner F et al (2011) Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat Biotechnol 29(11):1005–1010

Darwish I et al (2011) Immunomodulatory therapy for severe influenza. Expert Rev Anti-Infect Ther 9(7):807–822

McDermott JE et al (2016) The effect of inhibition of PP1 and TNFalpha signaling on pathogenesis of SARS coronavirus. BMC Syst Biol 10(1):93