Platform for isolation and characterization of SARS-CoV-2 variants enables rapid characterization of Omicron in Australia.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
28
12
2021
accepted:
26
04
2022
pubmed:
1
6
2022
medline:
7
6
2022
entrez:
31
5
2022
Statut:
ppublish
Résumé
Genetically distinct variants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have emerged since the start of the COVID-19 pandemic. Over this period, we developed a rapid platform (R-20) for viral isolation and characterization using primary remnant diagnostic swabs. This, combined with quarantine testing and genomics surveillance, enabled the rapid isolation and characterization of all major SARS-CoV-2 variants circulating in Australia in 2021. Our platform facilitated viral variant isolation, rapid resolution of variant fitness using nasopharyngeal swabs and ranking of evasion of neutralizing antibodies. In late 2021, variant of concern Omicron (B1.1.529) emerged. Using our platform, we detected and characterized SARS-CoV-2 VOC Omicron. We show that Omicron effectively evades neutralization antibodies and has a different entry route that is TMPRSS2-independent. Our low-cost platform is available to all and can detect all variants of SARS-CoV-2 studied so far, with the main limitation being that our platform still requires appropriate biocontainment.
Identifiants
pubmed: 35637329
doi: 10.1038/s41564-022-01135-7
pii: 10.1038/s41564-022-01135-7
pmc: PMC9159941
doi:
Banques de données
figshare
['10.6084/m9.figshare.19530550.v1', '10.6084/m9.figshare.19523401.v1']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
896-908Informations de copyright
© 2022. The Author(s).
Références
Davies, N. G. et al. Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science https://doi.org/10.1126/science.abg3055 (2021).
Faria, N. R. et al. Genomics and epidemiology of the P.1 SARS-CoV-2 lineage in Manaus, Brazil. Science 372, 815–821 (2021).
doi: 10.1126/science.abh2644
Tegally, H. et al. Detection of a SARS-CoV-2 variant of concern in South Africa. Nature 592, 438–443 (2021).
doi: 10.1038/s41586-021-03402-9
Mlcochova, P. et al. SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion. Nature https://doi.org/10.1038/s41586-021-03944-y (2021).
Bennett, C. M. Learning to live with COVID-19 in Australia: time for a new approach. Public Health Res. Pract. https://doi.org/10.17061/phrp3132110 (2021).
Lane, C. R. et al. Genomics-informed responses in the elimination of COVID-19 in Victoria, Australia: an observational, genomic epidemiological study. Lancet Public Health 6, e547–e556 (2021).
doi: 10.1016/S2468-2667(21)00133-X
Leong, L. E. X. et al. Whole-genome sequencing of SARS-CoV-2 from quarantine hotel outbreak. Emerg. Infect. Dis. 27, 2219–2221 (2021).
doi: 10.3201/eid2708.204875
Andersson, P., Sherry, N. L. & Howden, B. P. Surveillance for SARS-CoV-2 variants of concern in the Australian context. Med. J. Aust. 214, 500–502.e1 (2021).
doi: 10.5694/mja2.51105
Seemann, T. et al. Tracking the COVID-19 pandemic in Australia using genomics. Nat. Commun. 11, 4376 (2020).
doi: 10.1038/s41467-020-18314-x
Rockett, R. J. et al. Revealing COVID-19 transmission in Australia by SARS-CoV-2 genome sequencing and agent-based modeling. Nat. Med. 26, 1398–1404 (2020).
doi: 10.1038/s41591-020-1000-7
Bull, R. A. et al. Analytical validity of nanopore sequencing for rapid SARS-CoV-2 genome analysis. Nat. Commun. 11, 6272 (2020).
doi: 10.1038/s41467-020-20075-6
Hou, Y. J. et al. SARS-CoV-2reverse genetics reveals a variable infection gradient in the respiratory tract. Cell 182, 429–446.e14 (2020).
doi: 10.1016/j.cell.2020.05.042
Matsuyama, S. et al. Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells. Proc. Natl Acad. Sci. USA 117, 7001–7003 (2020).
doi: 10.1073/pnas.2002589117
Planas, D. et al. Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies. Nat. Med. 27, 917–924 (2021).
doi: 10.1038/s41591-021-01318-5
Hoffmann, M. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181, 271–280.e8 (2020).
doi: 10.1016/j.cell.2020.02.052
Ferreira, C. B. et al. Lentiviral vector production titer is not limited in HEK293T by induced intracellular innate immunity. Mol. Ther. Methods Clin. Dev. 17, 209–219 (2020).
doi: 10.1016/j.omtm.2019.11.021
Ronco, L. V., Karpova, A. Y., Vidal, M. & Howley, P. M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12, 2061–2072 (1998).
doi: 10.1101/gad.12.13.2061
Fonseca, G. J. et al. Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host Microbe 11, 597–606 (2012).
doi: 10.1016/j.chom.2012.05.005
Bhattacharya, S. et al. Cooperation of Stat2 and p300/CBP in signalling induced by interferon-alpha. Nature 383, 344–347 (1996).
doi: 10.1038/383344a0
Juang, Y. T. et al. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc. Natl Acad. Sci. USA 95, 9837–9842 (1998).
doi: 10.1073/pnas.95.17.9837
Ramakrishnan, M. A. Determination of 50% endpoint titer using a simple formula. World J. Virol. 5, 85–86 (2016).
doi: 10.5501/wjv.v5.i2.85
Armitage, P. & Allen, I. Methods of estimating the LD 50 in quantal response data. J. Hygiene 48, 298–322 (1950).
doi: 10.1017/S0022172400015084
Tea, F. et al. SARS-CoV-2 neutralizing antibodies: longevity, breadth, and evasion by emerging viral variants. PLoS Med. 18, e1003656 (2021).
doi: 10.1371/journal.pmed.1003656
Burnett, D. L. et al. Immunizations with diverse sarbecovirus receptor-binding domains elicit SARS-CoV-2 neutralizing antibodies against a conserved site of vulnerability. Immunity 54, 2908–2921.e6 (2021).
doi: 10.1016/j.immuni.2021.10.019
Kristiansen, P. A. et al. WHO international standard for anti-SARS-CoV-2 immunoglobulin. Lancet 397, 1347–1348 (2021).
doi: 10.1016/S0140-6736(21)00527-4
Liu, J. et al. BNT162b2-elicited neutralization of B.1.617 and other SARS-CoV-2 variants. Nature 596, 273–275 (2021).
doi: 10.1038/s41586-021-03693-y
Zhou, D. et al. Evidence of escape of SARS-CoV-2 variant B.1.351 from natural and vaccine-induced sera. Cell 184, 2348–2361.e6 (2021).
doi: 10.1016/j.cell.2021.02.037
Edara, V. V. et al. Infection- and vaccine-induced antibody binding and neutralization of the B.1.351 SARS-CoV-2 variant. Cell Host Microbe 29, 516–521.e3 (2021).
doi: 10.1016/j.chom.2021.03.009
Shen, X. et al. Neutralization of SARS-CoV-2 variants B.1.429 and B.1.351. N. Engl. J. Med 384, 2352–2354 (2021).
doi: 10.1056/NEJMc2103740
Loo, S. L. et al. Human coronaviruses 229E and OC43 replicate and induce distinct antiviral responses in differentiated primary human bronchial epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 319, L926–L931 (2020).
doi: 10.1152/ajplung.00374.2020
Campbell, F. et al. Increased transmissibility and global spread of SARS-CoV-2 variants of concern as at June 2021. Euro Surveill. https://doi.org/10.2807/1560-7917.ES.2021.26.24.2100509 (2021).
Hui, K. P. Y. et al. SARS-CoV-2 Omicron variant replication in human bronchus and lung ex vivo. Nature https://doi.org/10.1038/s41586-022-04479-6 (2022).
Pinto, D. et al. Cross-neutralization of SARS-CoV-2 by a human monoclonal SARS-CoV antibody. Nature 583, 290–295 (2020).
doi: 10.1038/s41586-020-2349-y
Khoury, D. S. et al. Neutralizing antibody levels are highly predictive of immune protection from symptomatic SARS-CoV-2 infection. Nat. Med. 27, 1205–1211 (2021).
doi: 10.1038/s41591-021-01377-8
Cromer, D. et al. Neutralising antibody titres as predictors of protection against SARS-CoV-2 variants and the impact of boosting: a meta-analysis. Lancet Microbe https://doi.org/10.1016/S2666-5247(21)00267-6 (2021).
Polack, F. P. et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med. 383, 2603–2615 (2020).
doi: 10.1056/NEJMoa2034577
Hoffmann, M. et al. The Omicron variant is highly resistant against antibody-mediated neutralization: implications for control of the COVID-19 pandemic. Cell 185, 447–456.e11 (2022).
doi: 10.1016/j.cell.2021.12.032
Cameroni, E. et al. Broadly neutralizing antibodies overcome SARS-CoV-2 Omicron antigenic shift. Nature https://doi.org/10.1038/s41586-021-04386-2 (2021).
Planas, D. et al. Considerable escape of SARS-CoV-2 Omicron to antibody neutralization. Nature https://doi.org/10.1038/s41586-021-04389-z (2021).
Madhi, S. A., Ihekweazu, C., Rees, H. & Pollard, A. J. Decoupling of omicron variant infections and severe COVID-19. Lancet https://doi.org/10.1016/S0140-6736(22)00109-X (2022).
Chau, N. V. V. et al. An observational study of breakthrough SARS-CoV-2 Delta variant infections among vaccinated healthcare workers in Vietnam. EClinicalMedicine 41, 101143 (2021).
doi: 10.1016/j.eclinm.2021.101143
Pouwels, K. B. et al. Effect of Delta variant on viral burden and vaccine effectiveness against new SARS-CoV-2 infections in the UK. Nat. Med. https://doi.org/10.1038/s41591-021-01548-7 (2021).
Bergwerk, M. et al. Covid-19 breakthrough infections in vaccinated health care workers. N. Engl. J. Med. 385, 1474–1484 (2021).
doi: 10.1056/NEJMoa2109072
Diamond, M. et al. The SARS-CoV-2 B.1.1.529 Omicron virus causes attenuated infection and disease in mice and hamsters. Res. Sq. https://doi.org/10.21203/rs.3.rs-1211792/v1 (2021).
Halfmann, P. J. et al. SARS-CoV-2 Omicron virus causes attenuated disease in mice and hamsters. Nature https://doi.org/10.1038/s41586-022-04441-6 (2022).
Bleul, C. C., Wu, L., Hoxie, J. A., Springer, T. A. & Mackay, C. R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl Acad. Sci. USA 94, 1925–1930 (1997).
doi: 10.1073/pnas.94.5.1925
Workshop summary and guidelines: investigative use of bronchoscopy, lavage, and bronchial biopsies in asthma and other airway diseases. J. Allergy Clin. Immunol. 88, 808–814 (1991).
Burnett, D. L. et al. Immunizations with diverse sarbecovirus receptor-binding domains elicit SARS-CoV-2 neutralizing antibodies against a conserved site of vulnerability. Immunity https://doi.org/10.1016/j.immuni.2021.10.019 (2021).
Kober, C. et al. IgG3 and IgM identified as key to SARS-CoV-2 neutralization in convalescent plasma pools. PLoS ONE 17, e0262162 (2022).
doi: 10.1371/journal.pone.0262162
Stucki, M. et al. Investigations of prion and virus safety of a new liquid IVIG product. Biologicals 36, 239–247 (2008).
doi: 10.1016/j.biologicals.2008.01.004
Karbiener, M. et al. Plasma from post-COVID-19 and COVID-19-vaccinated donors results in highly potent SARS-CoV-2 neutralization by intravenous immunoglobulins. J. Infect. Dis. https://doi.org/10.1093/infdis/jiab482 (2021).
Follenzi, A. et al. Targeting lentiviral vector expression to hepatocytes limits transgene-specific immune response and establishes long-term expression of human antihemophilic factor IX in mice. Blood 103, 3700–3709 (2004).
doi: 10.1182/blood-2003-09-3217
Aggarwal, A. et al. Mobilization of HIV spread by diaphanous 2 dependent filopodia in infected dendritic cells. PLoS Pathog. 8, e1002762 (2012).
doi: 10.1371/journal.ppat.1002762
Cromer, D. et al. Neutralising antibody titres as predictors of protection against SARS-CoV-2 variants and the impact of boosting: a meta-analysis. Lancet Microbe https://doi.org/10.1016/S2666-5247(21)00267-6 (2021).