The role of influenza-A virus and coronavirus viral glycoprotein cleavage in host adaptation

Current Opinion in Virology - Tập 58 - Trang 101303 - 2023
Miriam R Heindl1, Eva Böttcher-Friebertshäuser1
1Institute of Virology, Philipps University, Marburg, Germany

Tài liệu tham khảo

Skehel, 2000, Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin, Annu Rev Biochem, 69, 531, 10.1146/annurev.biochem.69.1.531 Hoffmann, 2018, Priming time: how cellular proteases arm coronavirus spike proteins, 71 Huang, 1980, Fusion between cell membrane and liposomes containing the glycoproteins of influenza virus, Virology, 104, 294, 10.1016/0042-6822(80)90334-7 Böttcher-Friebertshäuser, 2018, Membrane-anchored serine proteases: host cell factors in proteolytic activation of viral glycoproteins, 153 Haan, 2008, Cleavage of group 1 coronavirus spike proteins: how furin cleavage is traded off against heparan sulfate binding upon cell culture adaptation, J Virol, 82, 6078, 10.1128/JVI.00074-08 Limburg, 2019, TMPRSS2 is the major activating protease of influenza A virus in primary human airway cells and influenza B virus in human type II pneumocytes, J Virol, 93, 10.1128/JVI.00649-19 Garten, 1981, Proteolytic activation of the influenza virus hemagglutinin: the structure of the cleavage site and the enzymes involved in cleavage, Virology, 115, 361, 10.1016/0042-6822(81)90117-3 Stieneke-Gröber, 1992, Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease, EMBO J, 11, 2407, 10.1002/j.1460-2075.1992.tb05305.x Glowacka, 2011, 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, 85, 4122, 10.1128/JVI.02232-10 Simmons, 2005, Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry, Proc Natl Acad Sci USA, 102, 11876, 10.1073/pnas.0505577102 Jocher, 2022, ADAM10 and ADAM17 promote SARS-CoV-2 cell entry and spike protein-mediated lung cell fusion, EMBO Rep, 23, 10.15252/embr.202154305 Yamamoto, 2022, Metalloproteinase-dependent and TMPRSS2-independent cell surface entry pathway of SARS-CoV-2 requires the furin cleavage site and the S2 domain of spike protein, mBio, 13, 10.1128/mbio.00519-22 Harte, 2022, Metalloprotease-dependent S2'-activation promotes cell-cell fusion and syncytiation of SARS-CoV-2, Viruses, 14, 2094, 10.3390/v14102094 Benlarbi, 2022, Identification and differential usage of a host metalloproteinase entry pathway by SARS-CoV-2 Delta and Omicron, iScience, 25, 10.1016/j.isci.2022.105316 Bestle, 2021, Hemagglutinins of Avian influenza viruses are proteolytically activated by TMPRSS2 in human and murine airway cells, J Virol, 95, 10.1128/JVI.00906-21 Peitsch, 2014, Activation of influenza A viruses by host proteases from swine airway epithelium, J Virol, 88, 282, 10.1128/JVI.01635-13 Bertram, 2012, Influenza and SARS-coronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts, PLoS One, 7, 10.1371/journal.pone.0035876 Zmora, 2017, Non-human primate orthologues of TMPRSS2 cleave and activate the influenza virus hemagglutinin, PLoS One, 12, 10.1371/journal.pone.0176597 El Najjar, 2015, Analysis of cathepsin and furin proteolytic enzymes involved in viral fusion protein activation in cells of the bat reservoir host, PLoS One, 10, 10.1371/journal.pone.0115736 Bestle, 2020, TMPRSS2 and furin are both essential for proteolytic activation of SARS-CoV-2 in human airway cells, Life Sci Alliance, 3, 10.26508/lsa.202000786 Hoffmann, 2020, A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells, Mol Cell, 78, 779, 10.1016/j.molcel.2020.04.022 Iwata-Yoshikawa, 2019, TMPRSS2 contributes to virus spread and immunopathology in the airways of murine models after coronavirus infection, J Virol, 93, 10.1128/JVI.01815-18 Hatesuer, 2013, Tmprss2 is essential for influenza H1N1 virus pathogenesis in mice, PLoS Pathog, 9, 10.1371/journal.ppat.1003774 Tarnow, 2014, TMPRSS2 is a host factor that is essential for pneumotropism and pathogenicity of H7N9 influenza A virus in mice, J Virol, 88, 4744, 10.1128/JVI.03799-13 Li, 2021, Distinct mechanisms for TMPRSS2 expression explain organ-specific inhibition of SARS-CoV-2 infection by enzalutamide, Nat Commun, 12 Keller, 2022, TMPRSS2, a novel host-directed drug target against SARS-CoV-2, Signal Transduct Target Ther, 7, 251, 10.1038/s41392-022-01084-x Menachery, 2020, Trypsin treatment unlocks barrier for zoonotic bat coronavirus infection, J Virol, 94, 10.1128/JVI.01774-19 Harbig, 2020, Transcriptome profiling and protease inhibition experiments identify proteases that activate H3N2 influenza A and influenza B viruses in murine airways, J Biol Chem, 295, 11388, 10.1074/jbc.RA120.012635 Quesada, 2010, Comparative genomic analysis of the zebra finch degradome provides new insights into evolution of proteases in birds and mammals, BMC Genom, 11, 10.1186/1471-2164-11-220 Magnen, 2018, Kallikrein-related peptidase 5 and seasonal influenza viruses, limitations of the experimental models for activating proteases, Biol Chem, 399, 1053, 10.1515/hsz-2017-0340 Baron, 2013, Matriptase, HAT, and TMPRSS2 activate the hemagglutinin of H9N2 influenza A viruses, J Virol, 87, 1811, 10.1128/JVI.02320-12 Oberst, 2003, Characterization of matriptase expression in normal human tissues, J Histochem Cytochem, 51, 1017, 10.1177/002215540305100805 Böttcher-Friebertshäuser, 2010, Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors, J Virol, 84, 5605, 10.1128/JVI.00140-10 Park, 2016, Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism, Proc Natl Acad Sci USA, 113, 12262, 10.1073/pnas.1608147113 Koch, 2021, TMPRSS2 expression dictates the entry route used by SARS-CoV-2 to infect host cells, EMBO J, 40, 10.15252/embj.2021107821 Li, 2013, IFITM proteins restrict viral membrane hemifusion, PLoS Pathog, 9, 10.1371/journal.ppat.1003124 Wrensch, 2014, IFITM proteins inhibit entry driven by the MERS-coronavirus spike protein: evidence for cholesterol-independent mechanisms, Viruses, 6, 3683, 10.3390/v6093683 Zhao, 2020, The potential intermediate hosts for SARS-CoV-2, Front Microbiol, 11, 10.3389/fmicb.2020.580137 Prelli Bozzo, 2021, IFITM proteins promote SARS-CoV-2 infection and are targets for virus inhibition in vitro, Nat Commun, 12, 4584, 10.1038/s41467-021-24817-y Shi, 2021, Opposing activities of IFITM proteins in SARS-CoV-2 infection, EMBO J, 40, 10.15252/embj.2020106501 Meng, 2022, Altered TMPRSS2 usage by SARS-CoV-2 Omicron impacts infectivity and fusogenicity, Nature, 603, 706, 10.1038/s41586-022-04474-x Zhao, 2022, SARS-CoV-2 Omicron variant shows less efficient replication and fusion activity when compared with Delta variant in TMPRSS2-expressed cells, Emerg Microbes Infect, 11, 277, 10.1080/22221751.2021.2023329 Willett, 2022, SARS-CoV-2 Omicron is an immune escape variant with an altered cell entry pathway, Nat Microbiol, 7, 1161, 10.1038/s41564-022-01143-7 Iwata-Yoshikawa, 2022, Essential role of TMPRSS2 in SARS-CoV-2 infection in murine airways, Nat Commun, 13, 10.1038/s41467-022-33911-8 Aggarwal, 2022, SARS-CoV-2 Omicron BA.5: evolving tropism and evasion of potent humoral responses and resistance to clinical immunotherapeutics relative to viral variants of concern, EBioMedicine, 84, 10.1016/j.ebiom.2022.104270 Licitra, 2013, Mutation in spike protein cleavage site and pathogenesis of feline coronavirus, Emerg Infect Dis, 19, 1066, 10.3201/eid1907.121094 Jackwood, 2020, Infectious bronchitis, 167 Stout, 2021, Furin cleavage sites in the spike proteins of bat and rodent coronaviruses: implications for virus evolution and zoonotic transfer from rodent species, One Health, 13, 10.1016/j.onehlt.2021.100282 Zhou, 2020, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, 579, 270, 10.1038/s41586-020-2012-7 Peacock, 2021, The furin cleavage site in the SARS-CoV-2 spike protein is required for transmission in ferrets, Nat Microbiol, 6, 899, 10.1038/s41564-021-00908-w Wrobel, 2020, SARS-CoV-2 and bat RaTG13 spike glycoprotein structures inform on virus evolution and furin-cleavage effects, Nat Struct Mol Biol, 27, 763, 10.1038/s41594-020-0468-7 Yu, 2022, SARS-CoV-2 spike engagement of ACE2 primes S2' site cleavage and fusion initiation, Proc Natl Acad Sci USA, 119 Lubinski, 2022, Functional evaluation of the P681H mutation on the proteolytic activation of the SARS-CoV-2 variant B.1.1.7 (Alpha) spike, iScience, 25, 10.1016/j.isci.2021.103589 Sasaki, 2021, SARS-CoV-2 variants with mutations at the S1/S2 cleavage site are generated in vitro during propagation in TMPRSS2-deficient cells, PLoS Pathog, 17, 10.1371/journal.ppat.1009233 Chaudhry, 2022, Rapid SARS-CoV-2 adaptation to available cellular proteases, J Virol, 96, 10.1128/jvi.02186-21 Chandran, 2005, Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection, Science, 308, 1643, 10.1126/science.1110656 Pager, 2005, Cathepsin L is involved in proteolytic processing of the Hendra virus fusion protein, J Virol, 79, 12714, 10.1128/JVI.79.20.12714-12720.2005 Balistreri, 2021, A widespread viral entry mechanism: the C-end Rule motif-neuropilin receptor interaction, Proc Natl Acad Sci USA, 118, 10.1073/pnas.2112457118 Guo, 2015, Neuropilin functions as an essential cell surface receptor, J Biol Chem, 290, 29120, 10.1074/jbc.R115.687327 Mayi, 2021, The role of neuropilin-1 in COVID-19, PLoS Pathog, 17, 10.1371/journal.ppat.1009153 Teesalu, 2009, C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration, Proc Natl Acad Sci USA, 106, 16157, 10.1073/pnas.0908201106 Pang, 2014, An endocytosis pathway initiated through neuropilin-1 and regulated by nutrient availability, Nat Commun, 5, 4904, 10.1038/ncomms5904 Daly, 2020, Neuropilin-1 is a host factor for SARS-CoV-2 infection, Science, 370, 861, 10.1126/science.abd3072 Cantuti-Castelvetri, 2020, Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity, Science, 370, 856, 10.1126/science.abd2985 Kong, 2022, Neuropilin-1 mediates SARS-CoV-2 infection of astrocytes in brain organoids, inducing inflammation leading to dysfunction and death of neurons, mBio, 13, 10.1128/mbio.02308-22 Hikmet, 2020, The protein expression profile of ACE2 in human tissues, Mol Syst Biol, 16, 10.15252/msb.20209610 Li, 2021, Neuropilin-1 assists SARS-CoV-2 infection by stimulating the separation of Spike protein S1 and S2, Biophys J, 120, 2828, 10.1016/j.bpj.2021.05.026 Baindara, 2022, Conservation and enhanced binding of SARS-CoV-2 Omicron spike protein to coreceptor neuropilin-1 predicted by docking analysis, Infect Dis Rep, 14, 243, 10.3390/idr14020029 Abdelwhab, 2013, Genetic changes that accompanied shifts of low pathogenic avian influenza viruses toward higher pathogenicity in poultry, Virulence, 4, 441, 10.4161/viru.25710 Alexander, 2007, An overview of the epidemiology of avian influenza, Vaccine, 25, 5637, 10.1016/j.vaccine.2006.10.051 Short, 2014, Influenza virus and endothelial cells: a species specific relationship, Front Microbiol, 5, 10.3389/fmicb.2014.00653 Vijaykrishna, 2008, Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses, PLoS Pathog, 4, 10.1371/journal.ppat.1000161 Reperant, 2009, Avian influenza viruses in mammals, Rev Sci Tech, 28, 137, 10.20506/rst.28.1.1876 Garten, 1982, The cleavage site of the hemagglutinin of fowl plague virus, Virology, 122, 186, 10.1016/0042-6822(82)90387-7 Woo, 2012, J Virol, 86, 3995, 10.1128/JVI.06540-11