Furin cleavage is required for swine acute diarrhea syndrome coronavirus spike protein-mediated cell – cell fusion

References

• Pan Y, Tian X, Qin P, et al. Discovery of a novel swine enteric alphacoronavirus (SeACoV) in southern China. Vet Microbiol. 2017;211:15–21. doi:10.1016/j.vetmic.2017.09.020
   PubMed Web of Science ®Google Scholar
• Gong L, Li J, Zhou Q, et al. A New Bat-HKU2-like coronavirus in swine, China, 2017. Emerg Infect Dis. 2017;23(9):1607–1609. doi:10.3201/eid2309.170915
   PubMed Web of Science ®Google Scholar
• Zhou P, Fan H, Lan T, et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature. 2018;556(7700):255–258. doi:10.1038/s41586-018-0010-9
   PubMed Web of Science ®Google Scholar
• Xu Z, Zhang Y, Gong L, et al. Isolation and characterization of a highly pathogenic strain of porcine enteric alphacoronavirus causing watery diarrhoea and high mortality in newborn piglets. Transbound Emerg Dis. 2019;66(1):119–130. doi:10.1111/tbed.12992
   PubMed Web of Science ®Google Scholar
• Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol. 2019;17(3):181–192. doi:10.1038/s41579-018-0118-9
   PubMed Web of Science ®Google Scholar
• Edwards CE, Yount BL, Graham RL, et al. Swine acute diarrhea syndrome coronavirus replication in primary human cells reveals potential susceptibility to infection. Proc Natl Acad Sci USA. 2020;117(43):26915–26925. doi:10.1073/pnas.2001046117
   PubMed Web of Science ®Google Scholar
• Luo Y, Chen Y, Geng R, et al. Broad cell tropism of SADS-CoV in vitro implies its potential cross-species infection risk. Virol Sin. 2021;36(3):559–563. doi:10.1007/s12250-020-00321-3
   PubMed Web of Science ®Google Scholar
• Yang YL, Qin P, Wang B, et al. Broad cross-species infection of cultured cells by bat HKU2-related swine acute diarrhea syndrome coronavirus and identification of Its replication in murine dendritic cells in vivo highlight Its potential for diverse interspecies transmission. J Virol. 2019;93(24):e01448–19.
   PubMed Web of Science ®Google Scholar
• Wang Q, Vlasova AN, Kenney SP, et al. Emerging and re-emerging coronaviruses in pigs. Curr Opin Virol. 2019;34:39–49. doi:10.1016/j.coviro.2018.12.001
   PubMed Web of Science ®Google Scholar
• Millet JK, Whittaker GR. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 2015;202:120–134. doi:10.1016/j.virusres.2014.11.021
   PubMed Web of Science ®Google Scholar
• Guan H, Wang Y, Perculija V, et al. Cryo-electron microscopy structure of the swine acute diarrhea syndrome coronavirus spike glycoprotein provides insights into evolution of unique coronavirus spike proteins. J Virol. 2020;94(22):e01301–20. doi:10.1128/JVI.01301-20
   PubMed Web of Science ®Google Scholar
• Bosch BJ, van der Zee R, de Haan CAM, et al. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol. 2003;77(16):8801–8811. doi:10.1128/JVI.77.16.8801-8811.2003
   PubMed Web of Science ®Google Scholar
• de Haan CA, Stadler K, Godeke GJ, et al. Cleavage inhibition of the murine coronavirus spike protein by a furin-like enzyme affects cell-cell but not virus-cell fusion. J Virol. 2004;78(11):6048–6054. doi:10.1128/JVI.78.11.6048-6054.2004
   PubMed Web of Science ®Google Scholar
• Park JE, Li K, Barlan A, et al. Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci USA. 2016;113(43):12262–12267. doi:10.1073/pnas.1608147113
   PubMed Web of Science ®Google Scholar
• Matsuyama S, Nagata N, Shirato K, et al. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J Virol. 2010;84(24):12658–12664. doi:10.1128/JVI.01542-10
   PubMed Web of Science ®Google Scholar
• Simmons G, Gosalia DN, Rennekamp AJ, et al. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci USA. 2005;102(33):11876–11881. doi:10.1073/pnas.0505577102
   PubMed Web of Science ®Google Scholar
• Millet JK, Whittaker GR. Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci USA. 2014;111(42):15214–15219. doi:10.1073/pnas.1407087111
   PubMed Web of Science ®Google Scholar
• Jia Y, Cao J, Wei Z. Bioinformatics analysis of spike proteins of porcine enteric coronaviruses. Biomed Res Int. 2021;2021:6689471.
   PubMed Web of Science ®Google Scholar
• Shirato K, Kawase M, Matsuyama S. Middle East respiratory syndrome coronavirus infection mediated by the transmembrane serine protease TMPRSS2. J Virol. 2013;87(23):12552–12561. doi:10.1128/JVI.01890-13
   PubMed Web of Science ®Google Scholar
• Glowacka I, Bertram S, Muller MA, et al. Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the Humoral immune response. J Virol. 2011;85(9):4122–4134. doi:10.1128/JVI.02232-10
   PubMed Web of Science ®Google Scholar
• Yamada Y, Liu DX. Proteolytic activation of the spike protein at a novel RRRR/S motif is implicated in furin-dependent entry, syncytium formation, and infectivity of coronavirus infectious bronchitis virus in cultured cells. J Virol. 2009;83(17):8744–8758. doi:10.1128/JVI.00613-09
   PubMed Web of Science ®Google Scholar
• Seidah NG, Chretien M. Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides1Published on the world wide Web on 17 August 1999.1. Brain Res. 1999;848(1–2):45–62. doi:10.1016/S0006-8993(99)01909-5
   PubMedGoogle Scholar
• Izaguirre G. The proteolytic regulation of virus cell entry by furin and other proprotein convertases. Viruses. 2019;11(9):837. doi:10.3390/v11090837
   PubMed Web of Science ®Google Scholar
• Belouzard S, Millet JK, Licitra BN, et al. Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses. 2012;4(6):1011–1033. doi:10.3390/v4061011
   PubMed Web of Science ®Google Scholar
• Duckert P, Brunak S, Blom N. Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel. 2004;17(1):107–112. doi:10.1093/protein/gzh013
   PubMed Web of Science ®Google Scholar
• Coutard B, Valle C, de Lamballerie X, et al. The spike glycoprotein of the new coronavirus 2019-nCoV contains a furin-like cleavage site absent in CoV of the same clade. Antiviral Res. 2020;176:104742.
   PubMed Web of Science ®Google Scholar
• Licitra BN, Millet JK, Regan AD, et al. Mutation in spike protein cleavage site and pathogenesis of feline coronavirus. Emerg Infect Dis. 2013;19(7):1066–1073. doi:10.3201/eid1907.121094
   PubMed Web of Science ®Google Scholar
• Follis KE, York J, Nunberg JH. Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. Virology. 2006;350(2):358–369. doi:10.1016/j.virol.2006.02.003
   PubMed Web of Science ®Google Scholar
• Gierer S, Muller MA, Heurich A, et al. Inhibition of proprotein convertases abrogates processing of the middle eastern respiratory syndrome coronavirus spike protein in infected cells but does not reduce viral infectivity. J Infect Dis. 2015;211(6):889–897. doi:10.1093/infdis/jiu407
   PubMed Web of Science ®Google Scholar
• Wu Y, Zhao S. Furin cleavage sites naturally occur in coronaviruses. Stem Cell Res. 2020;50:102115.
   PubMed Web of Science ®Google Scholar
• Lau SY, Wang P, Mok BW, et al. Attenuated SARS-CoV-2 variants with deletions at the S1/S2 junction. Emerg Microbes Infect. 2020;9(1):837–842. doi:10.1080/22221751.2020.1756700
   PubMed Web of Science ®Google Scholar
• Liu Z, Zheng H, Lin H, et al. Identification of common deletions in the spike protein of severe acute respiratory syndrome coronavirus 2. J Virol. 2020;94(17):e00790–20.
   PubMed Web of Science ®Google Scholar
• Cheng J, Zhao Y, Xu G, et al. The S2 subunit of QX-type infectious bronchitis coronavirus spike protein is an essential determinant of neurotropism. Viruses. 2019;11(10):972. doi:10.3390/v11100972
   PubMed Web of Science ®Google Scholar
• Jin X, Xu K, Jiang P, et al. Virus strain from a mild COVID-19 patient in Hangzhou represents a new trend in SARS-CoV-2 evolution potentially related to Furin cleavage site. Emerg Microbes Infect. 2020;9(1):1474–1488. doi:10.1080/22221751.2020.1781551
   PubMed Web of Science ®Google Scholar
• Johnson BA, Xie X, Bailey AL, et al. Loss of furin cleavage site attenuates SARS-CoV-2 pathogenesis. Nature. 2021;591(7849):293-299. doi:10.1038/s41586-021-03237-4
   PubMed Web of Science ®Google Scholar
• Belouzard S, Chu VC, Whittaker GR. Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci USA. 2009;106(14):5871–5876. doi:10.1073/pnas.0809524106
   PubMed Web of Science ®Google Scholar
• Kleine-Weber H, Elzayat MT, Hoffmann M, et al. Functional analysis of potential cleavage sites in the MERS-coronavirus spike protein. Sci Rep. 2018;8(1):16597. doi:10.1038/s41598-018-34859-w
   PubMed Web of Science ®Google Scholar
• Zeng C, Evans JP, King T, et al. SARS-CoV-2 spreads through cell-to-cell transmission. Proc Natl Acad Sci USA. 2022;119(1):e2111400119. doi:10.1073/pnas.2111400119
   PubMed Web of Science ®Google Scholar
• Braga L, Ali H, Secco I, et al. Drugs that inhibit TMEM16 proteins block SARS-CoV-2 spike-induced syncytia. Nature. 2021;594(7861):88–93. doi:10.1038/s41586-021-03491-6
   PubMed Web of Science ®Google Scholar
• Zhang Z, Zheng Y, Niu Z, et al. SARS-CoV-2 spike protein dictates syncytium-mediated lymphocyte elimination. Cell Death Differ. 2021;28(9):2765–2777. doi:10.1038/s41418-021-00782-3
   PubMed Web of Science ®Google Scholar