Regulation of angiotensin-converting enzyme 2 isoforms by type 2 inflammation and viral infection in human airway epithelium

Hoffmann, 2020, SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor, Cell, 181, 271, 10.1016/j.cell.2020.02.052 NCBI Resource Coordinators, 2016, Database resources of the National Center for Biotechnology Information, Nucleic Acids Res., 44, D7, 10.1093/nar/gkv1290 Turner, 2015, Chapter 25. ACE2 cell biology, regulation, and physiological functions, 185 Shajahan, 2021, Comprehensive characterization of N- and O- glycosylation of SARS-CoV-2 human receptor angiotensin converting enzyme 2, Glycobiology, 31, 410, 10.1093/glycob/cwaa101 Onabajo, 2020, Interferons and viruses induce a novel truncated ACE2 isoform and not the full-length SARS-CoV-2 receptor, Nat. Genet., 52, 1283, 10.1038/s41588-020-00731-9 Blume, 2021, A novel ACE2 isoform is expressed in human respiratory epithelia and is upregulated in response to interferons and RNA respiratory virus infection, Nat. Genet., 53, 205, 10.1038/s41588-020-00759-x Ng, 2020, Tissue-specific and interferon-inducible expression of nonfunctional ACE2 through endogenous retroelement co-option, Nat. Genet., 52, 1294, 10.1038/s41588-020-00732-8 Ziegler, 2020, 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, 181, 1016, 10.1016/j.cell.2020.04.035 Sungnak, 2020, SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes, Nat. Med., 26, 681, 10.1038/s41591-020-0868-6 Radzikowska, 2020, Distribution of ACE2, CD147, CD26 and other SARS-CoV-2 associated molecules in tissues and immune cells in health and in asthma, COPD, obesity, hypertension, and COVID-19 risk factors, Allergy, 75, 2829, 10.1111/all.14429 Skevaki, 2021, SARS-CoV-2 infection and COVID-19 in asthmatics: a complex relationship, Nat. Rev. Immunol., 21, 202, 10.1038/s41577-021-00516-z Adir, 2021, Asthma and COVID-19: an update, Eur. Respir. Rev., 30, 210152, 10.1183/16000617.0152-2021 Ren, 2022, Impact of allergic rhinitis and asthma on COVID-19 infection, hospitalization, and mortality, J. Allergy Clin. Immunol. Pract., 10, 124, 10.1016/j.jaip.2021.10.049 Terry, 2021, Asthma in adult patients with COVID-19. Prevalence and risk of severe disease, Am. J. Respir. Crit. Care Med., 203, 893, 10.1164/rccm.202008-3266OC Zhu, 2020, Association of asthma and its genetic predisposition with the risk of severe COVID-19, J. Allergy Clin. Immunol., 146, 327, 10.1016/j.jaci.2020.06.001 Aveyard, 2021, Association between pre-existing respiratory disease and its treatment, and severe COVID-19: a population cohort study, Lancet Respir. Med., 9, 909, 10.1016/S2213-2600(21)00095-3 Bloom, 2022, Asthma phenotypes and COVID-19 risk: A population-based observational study, Am. J. Respir. Crit. Care Med., 205, 36, 10.1164/rccm.202107-1704OC Morrison, C.B. et al. SARS-CoV-2 infection of airway cells causes intense viral and cell shedding, two spreading mechanisms affected by IL-13. Proc. Natl Acad. Sci. U. S. A. 119, e2119680119 (2022). Bonser, 2022, The Type 2 asthma mediator IL-13 inhibits severe acute respiratory syndrome coronavirus 2 infection of bronchial epithelium, Am. J. Respir. Cell Mol. Biol., 66, 391, 10.1165/rcmb.2021-0364OC Donlan, 2021, IL-13 is a driver of COVID-19 severity, JCI Insight, 6, e150107 Sasson, 2022, Safety and efficacy of dupilumab for the treatment of hospitalized patients with moderate to severe COVID 19: a phase IIa trial, Open Forum Infect. Dis., 9, ofac343, 10.1093/ofid/ofac343 Vanderwall, 2022, Airway epithelial interferon response to SARS-CoV-2 is inferior to rhinovirus and heterologous rhinovirus infection suppresses SARS-CoV-2 replication, Sci. Rep., 12, 6972, 10.1038/s41598-022-10763-2 Essaidi-Laziosi, 2022, Sequential infections with rhinovirus and influenza modulate the replicative capacity of SARS-CoV-2 in the upper respiratory tract, Emerg Microbes. Infect., 11, 412, 10.1080/22221751.2021.2021806 Dee, 2021, Human rhinovirus infection blocks severe acute respiratory syndrome coronavirus 2 replication within the respiratory epithelium: implications for COVID-19 epidemiology, J. Infect. Dis., 224, 31, 10.1093/infdis/jiab147 Radzikowska, 2022, Rhinovirus-induced epithelial RIG-I inflammasome activation suppresses antiviral immunity and promotes inflammatory responses in virus-induced asthma exacerbations and COVID-19, medRxiv Le Glass, 2021, Incidence and outcome of coinfections with SARS-CoV-2 and rhinovirus, Viruses, 13, 2528, 10.3390/v13122528 Gilles, 2020, Pollen exposure weakens innate defense against respiratory viruses, Allergy, 75, 576, 10.1111/all.14047 Damialis, A. et al. Higher airborne pollen concentrations correlated with increased SARS-CoV-2 infection rates, as evidenced from 31 countries across the globe. Proc. Natl Acad. Sci. U. S. A. 118, e2019034118 (2021). Kimura, 2020, Type 2 inflammation modulates ACE2 and TMPRSS2 in airway epithelial cells, J. Allergy Clin. Immunol., 146, 80, 10.1016/j.jaci.2020.05.004 Herrera-Esposito, 2022, Age-specific rate of severe and critical SARS-CoV-2 infections estimated with multi-country seroprevalence studies, BMC Infect. Dis., 22, 311, 10.1186/s12879-022-07262-0 Allen, 2021, Subtle influence of ACE2 glycan processing on SARS-CoV-2 recognition, J. Mol. Biol., 433, 166762, 10.1016/j.jmb.2020.166762 Yang, 2020, Inhibition of SARS-CoV-2 viral entry upon blocking N- and O-glycan elaboration, eLife, 9, e61552, 10.7554/eLife.61552 Rowland, 2021, Analysis of the role of N-linked glycosylation in cell surface expression, function, and binding properties of SARS-CoV-2 receptor ACE2, Microbiol. Spectr., 9, e0119921, 10.1128/Spectrum.01199-21 Liu, 2008, Control of protein synthesis and mRNA degradation by microRNAs, Curr. Opin. Cell Biol., 20, 214, 10.1016/j.ceb.2008.01.006 Yamada, 2019, Contributions of regulated transcription and mRNA decay to the dynamics of gene expression, Wiley Interdiscip. Rev. RNA, 10, e1508, 10.1002/wrna.1508 Eden, 2011, Proteome half-life dynamics in living human cells, Science, 331, 764, 10.1126/science.1199784 Williams, 2021, Differential expression in humans of the viral entry receptor ACE2 compared with the short deltaACE2 isoform lacking SARS-CoV-2 binding sites, Sci. Rep., 11, 24336, 10.1038/s41598-021-03731-9 Della Bella, 2022, Translation and emerging functions of non-coding RNAs in inflammation and immunity, Allergy, 77, 2025, 10.1111/all.15234 Lee, 2020, ACE2 localizes to the respiratory cilia and is not increased by ACE inhibitors or ARBs, Nat. Commun., 11, 5453, 10.1038/s41467-020-19145-6 Osan, 2022, Goblet cell hyperplasia increases SARS-CoV-2 infection in chronic obstructive pulmonary disease, Microbiol. Spectr., 10, e0045922, 10.1128/spectrum.00459-22 Lukassen, 2020, SARS-CoV-2 receptor ACE2 and TMPRSS2 are primarily expressed in bronchial transient secretory cells, EMBO J., 39, e105114, 10.15252/embj.20105114 Pinto, 2022, Ultrastructural insight into SARS-CoV-2 entry and budding in human airway epithelium, Nat. Commun., 13, 1609, 10.1038/s41467-022-29255-y Jia, 2005, ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia, J. Virol., 79, 14614, 10.1128/JVI.79.23.14614-14621.2005 Buchrieser, 2020, Syncytia formation by SARS-CoV-2-infected cells, EMBO J., 39, e106267, 10.15252/embj.2020106267 Hewitt, 2021, Regulation of immune responses by the airway epithelial cell landscape, Nat. Rev. Immunol., 21, 347, 10.1038/s41577-020-00477-9 Jakiela, 2021, Remodeling of bronchial epithelium caused by asthmatic inflammation affects its response to rhinovirus infection, Sci. Rep., 11, 12821, 10.1038/s41598-021-92252-6 Wawrzyniak, 2017, Regulation of bronchial epithelial barrier integrity by type 2 cytokines and histone deacetylases in asthmatic patients, J. Allergy Clin. Immunol., 139, 93, 10.1016/j.jaci.2016.03.050 Akdis, 2021, Does the epithelial barrier hypothesis explain the increase in allergy, autoimmunity and other chronic conditions?, Nat. Rev. Immunol., 21, 739, 10.1038/s41577-021-00538-7 Sugita, 2018, Type 2 innate lymphoid cells disrupt bronchial epithelial barrier integrity by targeting tight junctions through IL-13 in asthmatic patients, J. Allergy Clin. Immunol., 141, 300, 10.1016/j.jaci.2017.02.038 Huang, 2021, Identification of oligosaccharyltransferase as a host target for inhibition of SARS-CoV-2 and its variants, Cell Discov., 7, 116, 10.1038/s41421-021-00354-2 Yu, 2017, TUSC3: A novel tumour suppressor gene and its functional implications, J. Cell Mol. Med., 21, 1711, 10.1111/jcmm.13128 Lee, 2021, Longitudinal proteomic profiling provides insights into host response and proteome dynamics in COVID-19 progression, Proteomics, 21, e2000278, 10.1002/pmic.202000278 Baggen, 2021, Cellular host factors for SARS-CoV-2 infection, Nat. Microbiol., 6, 1219, 10.1038/s41564-021-00958-0 Cantuti-Castelvetri, 2020, Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity, Science, 370, 856, 10.1126/science.abd2985 Daly, 2020, Neuropilin-1 is a host factor for SARS-CoV-2 infection, Science, 370, 861, 10.1126/science.abd3072 Hudák, 2021, Contribution of syndecans to the cellular entry of SARS-CoV-2, Int. J. Mol. Sci., 22, 5336, 10.3390/ijms22105336 Chen, 2016, Mechanism and inhibition of human UDP-GlcNAc 2-epimerase, the key enzyme in sialic acid biosynthesis, Sci. Rep., 6, 23274, 10.1038/srep23274 Sun, 2021, The role of cell surface sialic acids for SARS-CoV-2 infection, Glycobiology, 31, 1245, 10.1093/glycob/cwab032 Zhang, 2015, The roles of dipeptidyl peptidase 4 (DPP4) and DPP4 inhibitors in different lung diseases: new evidence, Front. Pharmacol., 12, 731453, 10.3389/fphar.2021.731453 Bai, 2015, Phenotypic responses of differentiated asthmatic human airway epithelial cultures to rhinovirus, PLoS One, 10, e0118286, 10.1371/journal.pone.0118286 Yin, 2021, MDA5 governs the innate immune response to SARS-CoV-2 in lung epithelial cells, Cell Rep., 34, 108628, 10.1016/j.celrep.2020.108628 Lester, 2014, Toll-like receptors in antiviral innate immunity, J. Mol. Biol., 426, 1246, 10.1016/j.jmb.2013.11.024 Kast, 2017, Respiratory syncytial virus infection influences tight junction integrity, Clin. Exp. Immunol., 190, 351, 10.1111/cei.13042 Tan, 2019, Tight junction, mucin, and inflammasome-related molecules are differentially expressed in eosinophilic, mixed, and neutrophilic experimental asthma in mice, Allergy, 74, 294, 10.1111/all.13619