Antiviral efficacy against and replicative fitness of an XBB.1.9.1 clinical isolate
Ryuta Uraki, Maki Kiso, ..., Mutsumi Ito, Maki Kiso, Seiya Yamayoshi, Kiyoko Iwatsuki-Horimoto, Yuko Sakai-Tagawa, Masaki Imai, Michiko Koga, Shinya Yamamoto, Eisuke Adachi, Makoto Saito, Takeya Tsutsumi, Amato Otani, Shuetsu Fukushi, Shinji Watanabe, Tadaki Suzuki, Tetsuhiro Kikuchi, Hiroshi Yotsuyanagi, Ken Maeda, Yoshihiro Kawaoka
iScience, doi:10.1016/j.isci.2023.108147
Highlights The antigenicity of XBB.1.9.1 is similar to that of XBB.1.5 XBB.1.9.1 remains susceptible to antiviral drugs The replicative ability of XBB.1.9.1 is comparable to that of XBB.1.5
SUPPLEMENTAL INFORMATION Supplemental information can be found online at https://doi.org/10.1016/j.isci.2023.108147 .
AUTHOR CONTRIBUTIONS R.U.: conceptualization, formal analysis, validation, visualization, and writing of the first draft. M. Ito, M. Kiso: data curation, formal analysis, and methodology. S. Yamayoshi: conceptualization, data curation, formal analysis, and methodology. K.I-H.: resources and validation. Y.S-T., M.
Data and code availability All data used in this paper are available in the main text, in the supplemental information, or the sources have been clearly stated. This paper does not report original code. Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.
EXPERIMENTAL MODEL AND STUDY PARTICIPANT DETAILS Animal studies were carried out in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. The protocols were approved by the Animal Experiment Committee of the Institute of Medical Science, the University of Tokyo (approval number PA19-75). Virus inoculations were performed under isoflurane, and all efforts were made to minimize animal suffering. To collect and use clinical specimens, the research protocol was approved by the Research Ethics Review Committee of the Institute of Medical Science of the University of Tokyo (approval numbers: 2019-71-0201 and 2020-740226). After informed consent was..
References
Chen, Li, Peng, Tian, Ji et al., Neutralization against XBB.1 and XBB.1.5 after omicron subvariants breakthrough infection or reinfection, Lancet Reg. Health. West. Pac,
doi:10.1016/j.lanwpc.2023.100759
Imai, Halfmann, Yamayoshi, Iwatsuki-Horimoto, Chiba et al., Characterization of a new SARS-CoV-2 variant that emerged in Brazil, Proc. Natl. Acad. Sci,
doi:10.1073/pnas.2106535118
Imai, Ito, Kiso, Yamayoshi, Uraki et al., Efficacy of Antiviral Agents against Omicron Subvariants BQ.1.1 and XBB, N. Engl. J. Med,
doi:10.1056/NEJMc2214302
Imai, None
Imai, were propagated in the presence of 1 mg/ml geneticin (G418; Invivogen) and 5 mg/ml plasmocin prophylactic (Invivogen) in DMEM containing 10% FCS. Vero E6-TMPRSS2-T2A-ACE2 and VeroE6/TMPRSS2 cells were maintained at 37 C with 5% CO 2 . Chinese hamster ovary (CHO) cells were maintained in DMEM containing 10% FCS and antibiotics at 37 C with 5% CO 2 . Expi293F cells
Matsuyama, Nao, Shirato, Kawase, Saito et al., Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells, Proc. Natl. Acad. Sci,
doi:10.1073/pnas.2002589117
Matsuyama, None
Matsuyama, None
Matsuyama, None
Muramoto, Takahashi, Halfmann, Gotoh, Noda et al., Replicative capacity of SARS-CoV-2 omicron variants BA.5 and BQ.1.1 at elevated temperatures, Lancet. Microbe,
doi:10.1016/S2666-5247(23)00100-3
Qu, Faraone, Evans, Zheng, Carlin et al., Enhanced evasion of neutralizing antibody response by Omicron XBB.1.5, CH.1.1, and CA.3.1 variants, Cell Rep,
doi:10.1016/j.celrep.2023.112443
Takashita, Kinoshita, Yamayoshi, Sakai-Tagawa, Fujisaki et al., Efficacy of Antibodies and Antiviral Drugs against Covid-19 Omicron Variant, N. Engl. J. Med,
doi:10.1056/NEJMc2119407
Takashita, Morita, Ogawa, Nakamura, Fujisaki et al., Susceptibility of Influenza Viruses to the Novel Cap-Dependent Endonuclease Inhibitor Baloxavir Marboxil, Front. Microbiol,
doi:10.3389/fmicb.2018.03026
Takashita, Yamayoshi, Simon, Van Bakel, Sordillo et al., Efficacy of Antibodies and Antiviral Drugs against Omicron BA.2.12.1, BA.4, BA.5 Subvariants. N. Engl. J. Med,
doi:10.1056/NEJMc2207519
Uraki, Ito, Kiso, Yamayoshi, Iwatsuki-Horimoto et al., Antiviral and bivalent vaccine efficacy against an omicron XBB.1.5 isolate, Lancet Infect. Dis,
doi:10.1016/S1473-3099(23)00070-1
Uraki, Ito, Kiso, Yamayoshi, Iwatsuki-Horimoto et al., Efficacy of antivirals and mRNA vaccination against an XBF clinical isolate, Lancet Reg. Health. West. Pac,
doi:10.1016/j.lanwpc.2023.100777
Uriu, Ito, Zahradnik, Fujita, Kosugi et al., Enhanced transmissibility, infectivity, and immune resistance of the SARS-CoV-2 omicron XBB.1.5 variant, Lancet Infect. Dis,
doi:10.1016/S1473-3099(23)00051-8
Vanderheiden, Edara, Floyd, Kauffman, Mantus et al., Development of a Rapid Focus Reduction Neutralization Test Assay for Measuring SARS-CoV-2 Neutralizing Antibodies, Curr. Protoc. Immunol,
doi:10.1002/cpim.116
{ 'indexed': {'date-parts': [[2024, 10, 6]], 'date-time': '2024-10-06T01:16:09Z', 'timestamp': 1728177369351},
'reference-count': 14,
'publisher': 'Elsevier BV',
'issue': '11',
'license': [ { 'start': { 'date-parts': [[2023, 11, 1]],
'date-time': '2023-11-01T00:00:00Z',
'timestamp': 1698796800000},
'content-version': 'tdm',
'delay-in-days': 0,
'URL': 'https://www.elsevier.com/tdm/userlicense/1.0/'},
{ 'start': { 'date-parts': [[2023, 11, 1]],
'date-time': '2023-11-01T00:00:00Z',
'timestamp': 1698796800000},
'content-version': 'tdm',
'delay-in-days': 0,
'URL': 'https://www.elsevier.com/legal/tdmrep-license'},
{ 'start': { 'date-parts': [[2023, 10, 2]],
'date-time': '2023-10-02T00:00:00Z',
'timestamp': 1696204800000},
'content-version': 'vor',
'delay-in-days': 0,
'URL': 'http://creativecommons.org/licenses/by-nc-nd/4.0/'}],
'content-domain': { 'domain': ['cell.com', 'elsevier.com', 'sciencedirect.com'],
'crossmark-restriction': True},
'published-print': {'date-parts': [[2023, 11]]},
'DOI': '10.1016/j.isci.2023.108147',
'type': 'journal-article',
'created': {'date-parts': [[2023, 10, 4]], 'date-time': '2023-10-04T08:42:34Z', 'timestamp': 1696408954000},
'page': '108147',
'update-policy': 'http://dx.doi.org/10.1016/elsevier_cm_policy',
'source': 'Crossref',
'is-referenced-by-count': 5,
'title': 'Antiviral efficacy against and replicative fitness of an XBB.1.9.1 clinical isolate',
'prefix': '10.1016',
'volume': '26',
'author': [ {'given': 'Ryuta', 'family': 'Uraki', 'sequence': 'first', 'affiliation': []},
{'given': 'Mutsumi', 'family': 'Ito', 'sequence': 'additional', 'affiliation': []},
{'given': 'Maki', 'family': 'Kiso', 'sequence': 'additional', 'affiliation': []},
{'given': 'Seiya', 'family': 'Yamayoshi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Kiyoko', 'family': 'Iwatsuki-Horimoto', 'sequence': 'additional', 'affiliation': []},
{'given': 'Yuko', 'family': 'Sakai-Tagawa', 'sequence': 'additional', 'affiliation': []},
{'given': 'Masaki', 'family': 'Imai', 'sequence': 'additional', 'affiliation': []},
{'given': 'Michiko', 'family': 'Koga', 'sequence': 'additional', 'affiliation': []},
{'given': 'Shinya', 'family': 'Yamamoto', 'sequence': 'additional', 'affiliation': []},
{'given': 'Eisuke', 'family': 'Adachi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Makoto', 'family': 'Saito', 'sequence': 'additional', 'affiliation': []},
{'given': 'Takeya', 'family': 'Tsutsumi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Amato', 'family': 'Otani', 'sequence': 'additional', 'affiliation': []},
{'given': 'Shuetsu', 'family': 'Fukushi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Shinji', 'family': 'Watanabe', 'sequence': 'additional', 'affiliation': []},
{'given': 'Tadaki', 'family': 'Suzuki', 'sequence': 'additional', 'affiliation': []},
{'given': 'Tetsuhiro', 'family': 'Kikuchi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Hiroshi', 'family': 'Yotsuyanagi', 'sequence': 'additional', 'affiliation': []},
{'given': 'Ken', 'family': 'Maeda', 'sequence': 'additional', 'affiliation': []},
{ 'ORCID': 'http://orcid.org/0000-0001-5061-8296',
'authenticated-orcid': False,
'given': 'Yoshihiro',
'family': 'Kawaoka',
'sequence': 'additional',
'affiliation': []}],
'member': '78',
'reference': [ { 'key': '10.1016/j.isci.2023.108147_bib1',
'first-page': '100759',
'article-title': 'Neutralization against XBB.1 and XBB.1.5 after omicron subvariants '
'breakthrough infection or reinfection',
'volume': '33',
'author': 'Chen',
'year': '2023',
'journal-title': 'Lancet Reg. Health. West. Pac.'},
{ 'key': '10.1016/j.isci.2023.108147_bib2',
'doi-asserted-by': 'crossref',
'first-page': '112443',
'DOI': '10.1016/j.celrep.2023.112443',
'article-title': 'Enhanced evasion of neutralizing antibody response by Omicron XBB.1.5, '
'CH.1.1, and CA.3.1 variants',
'volume': '42',
'author': 'Qu',
'year': '2023',
'journal-title': 'Cell Rep.'},
{ 'key': '10.1016/j.isci.2023.108147_bib3',
'doi-asserted-by': 'crossref',
'first-page': '402',
'DOI': '10.1016/S1473-3099(23)00070-1',
'article-title': 'Antiviral and bivalent vaccine efficacy against an omicron XBB.1.5 '
'isolate',
'volume': '23',
'author': 'Uraki',
'year': '2023',
'journal-title': 'Lancet Infect. Dis.'},
{ 'key': '10.1016/j.isci.2023.108147_bib4',
'doi-asserted-by': 'crossref',
'first-page': '280',
'DOI': '10.1016/S1473-3099(23)00051-8',
'article-title': 'Enhanced transmissibility, infectivity, and immune resistance of the '
'SARS-CoV-2 omicron XBB.1.5 variant',
'volume': '23',
'author': 'Uriu',
'year': '2023',
'journal-title': 'Lancet Infect. Dis.'},
{ 'key': '10.1016/j.isci.2023.108147_bib5',
'doi-asserted-by': 'crossref',
'first-page': '278',
'DOI': '10.1016/S1473-3099(23)00010-5',
'article-title': 'ACE2 binding and antibody evasion in enhanced transmissibility of '
'XBB.1.5',
'volume': '23',
'author': 'Yue',
'year': '2023',
'journal-title': 'Lancet Infect. Dis.'},
{ 'key': '10.1016/j.isci.2023.108147_bib6',
'doi-asserted-by': 'crossref',
'first-page': 'e486',
'DOI': '10.1016/S2666-5247(23)00100-3',
'article-title': 'Replicative capacity of SARS-CoV-2 omicron variants BA.5 and BQ.1.1 at '
'elevated temperatures',
'volume': '4',
'author': 'Muramoto',
'year': '2023',
'journal-title': 'Lancet. Microbe'},
{ 'key': '10.1016/j.isci.2023.108147_bib7',
'doi-asserted-by': 'crossref',
'first-page': '995',
'DOI': '10.1056/NEJMc2119407',
'article-title': 'Efficacy of Antibodies and Antiviral Drugs against Covid-19 Omicron '
'Variant',
'volume': '386',
'author': 'Takashita',
'year': '2022',
'journal-title': 'N.\xa0Engl. J. Med.'},
{ 'key': '10.1016/j.isci.2023.108147_bib8',
'doi-asserted-by': 'crossref',
'first-page': '468',
'DOI': '10.1056/NEJMc2207519',
'article-title': 'Efficacy of Antibodies and Antiviral Drugs against Omicron BA.2.12.1, '
'BA.4, and BA.5 Subvariants',
'volume': '387',
'author': 'Takashita',
'year': '2022',
'journal-title': 'N.\xa0Engl. J. Med.'},
{ 'key': '10.1016/j.isci.2023.108147_bib9',
'doi-asserted-by': 'crossref',
'first-page': '89',
'DOI': '10.1056/NEJMc2214302',
'article-title': 'Efficacy of Antiviral Agents against Omicron Subvariants BQ.1.1 and XBB',
'volume': '388',
'author': 'Imai',
'year': '2023',
'journal-title': 'N.\xa0Engl. J. Med.'},
{ 'key': '10.1016/j.isci.2023.108147_bib10',
'first-page': '100777',
'article-title': 'Efficacy of antivirals and mRNA vaccination against an XBF clinical '
'isolate',
'volume': '34',
'author': 'Uraki',
'year': '2023',
'journal-title': 'Lancet Reg. Health. West. Pac.'},
{ 'key': '10.1016/j.isci.2023.108147_bib11',
'doi-asserted-by': 'crossref',
'first-page': '7001',
'DOI': '10.1073/pnas.2002589117',
'article-title': 'Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells',
'volume': '117',
'author': 'Matsuyama',
'year': '2020',
'journal-title': 'Proc. Natl. Acad. Sci. USA'},
{ 'key': '10.1016/j.isci.2023.108147_bib12',
'doi-asserted-by': 'crossref',
'DOI': '10.1073/pnas.2106535118',
'article-title': 'Characterization of a new SARS-CoV-2 variant that emerged in Brazil',
'volume': '118',
'author': 'Imai',
'year': '2021',
'journal-title': 'Proc. Natl. Acad. Sci. USA'},
{ 'key': '10.1016/j.isci.2023.108147_bib13',
'doi-asserted-by': 'crossref',
'first-page': 'e116',
'DOI': '10.1002/cpim.116',
'article-title': 'Development of a Rapid Focus Reduction Neutralization Test Assay for '
'Measuring SARS-CoV-2 Neutralizing Antibodies',
'volume': '131',
'author': 'Vanderheiden',
'year': '2020',
'journal-title': 'Curr. Protoc. Immunol.'},
{ 'key': '10.1016/j.isci.2023.108147_bib14',
'doi-asserted-by': 'crossref',
'first-page': '3026',
'DOI': '10.3389/fmicb.2018.03026',
'article-title': 'Susceptibility of Influenza Viruses to the Novel Cap-Dependent '
'Endonuclease Inhibitor Baloxavir Marboxil',
'volume': '9',
'author': 'Takashita',
'year': '2018',
'journal-title': 'Front. Microbiol.'}],
'container-title': 'iScience',
'original-title': [],
'language': 'en',
'link': [ { 'URL': 'https://api.elsevier.com/content/article/PII:S2589004223022241?httpAccept=text/xml',
'content-type': 'text/xml',
'content-version': 'vor',
'intended-application': 'text-mining'},
{ 'URL': 'https://api.elsevier.com/content/article/PII:S2589004223022241?httpAccept=text/plain',
'content-type': 'text/plain',
'content-version': 'vor',
'intended-application': 'text-mining'}],
'deposited': { 'date-parts': [[2024, 8, 5]],
'date-time': '2024-08-05T06:56:12Z',
'timestamp': 1722840972000},
'score': 1,
'resource': {'primary': {'URL': 'https://linkinghub.elsevier.com/retrieve/pii/S2589004223022241'}},
'subtitle': [],
'short-title': [],
'issued': {'date-parts': [[2023, 11]]},
'references-count': 14,
'journal-issue': {'issue': '11', 'published-print': {'date-parts': [[2023, 11]]}},
'alternative-id': ['S2589004223022241'],
'URL': 'http://dx.doi.org/10.1016/j.isci.2023.108147',
'relation': {},
'ISSN': ['2589-0042'],
'subject': [],
'container-title-short': 'iScience',
'published': {'date-parts': [[2023, 11]]},
'assertion': [ {'value': 'Elsevier', 'name': 'publisher', 'label': 'This article is maintained by'},
{ 'value': 'Antiviral efficacy against and replicative fitness of an XBB.1.9.1 clinical '
'isolate',
'name': 'articletitle',
'label': 'Article Title'},
{'value': 'iScience', 'name': 'journaltitle', 'label': 'Journal Title'},
{ 'value': 'https://doi.org/10.1016/j.isci.2023.108147',
'name': 'articlelink',
'label': 'CrossRef DOI link to publisher maintained version'},
{'value': 'article', 'name': 'content_type', 'label': 'Content Type'},
{'value': '© 2023 The Author(s).', 'name': 'copyright', 'label': 'Copyright'}],
'article-number': '108147'}