Significant role of host sialylated glycans in the infection and spread of severe acute respiratory syndrome coronavirus 2

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-Co...

Full description

Saved in:
Bibliographic Details
Published inPLoS pathogens Vol. 18; no. 6; p. e1010590
Main Authors Saso, Wakana, Yamasaki, Masako, Nakakita, Shin-ichi, Fukushi, Shuetsu, Tsuchimoto, Kana, Watanabe, Noriyuki, Sriwilaijaroen, Nongluk, Kanie, Osamu, Muramatsu, Masamichi, Takahashi, Yoshimasa, Matano, Tetsuro, Takeda, Makoto, Suzuki, Yasuo, Watashi, Koichi
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.06.2022
Public Library of Science (PLoS)
Subjects
ACE2
Acids
Angiotensin
Angiotensin-converting enzyme 2
Biology and life sciences
Cell surface
Coronaviruses
COVID-19
Epidemics
Infections
Medicine and health sciences
Middle East respiratory syndrome
Peptidyl-dipeptidase A
Physical Sciences
Polysaccharides
Respiratory diseases
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Sialic acids
Viral diseases
Viral infections
Online AccessGet full text

Cover

Abstract Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-CoV-2 and SARS-CoV has been poorly defined. Here we identified that host sialoglycans play a significant role in the efficient spread of SARS-CoV-2 infection, while this was not the case with SARS-CoV. SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds, but not by α2–3 analog, in VeroE6/TMPRSS2 cells. The α2-6-linked compound bound to SARS-CoV-2 spike S1 subunit to competitively inhibit SARS-CoV-2 attachment to cells. Enzymatic removal of cell surface sialic acids impaired the interaction between SARS-CoV-2 spike and angiotensin-converting enzyme 2 (ACE2), and suppressed the efficient spread of SARS-CoV-2 infection over time, in contrast to its least effect on SARS-CoV spread. Our study provides a novel molecular basis of SARS-CoV-2 infection which illustrates the distinctive characteristics from SARS-CoV.
AbstractList Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-CoV-2 and SARS-CoV has been poorly defined. Here we identified that host sialoglycans play a significant role in the efficient spread of SARS-CoV-2 infection, while this was not the case with SARS-CoV. SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds, but not by α2-3 analog, in VeroE6/TMPRSS2 cells. The α2-6-linked compound bound to SARS-CoV-2 spike S1 subunit to competitively inhibit SARS-CoV-2 attachment to cells. Enzymatic removal of cell surface sialic acids impaired the interaction between SARS-CoV-2 spike and angiotensin-converting enzyme 2 (ACE2), and suppressed the efficient spread of SARS-CoV-2 infection over time, in contrast to its least effect on SARS-CoV spread. Our study provides a novel molecular basis of SARS-CoV-2 infection which illustrates the distinctive characteristics from SARS-CoV.
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-CoV-2 and SARS-CoV has been poorly defined. Here we identified that host sialoglycans play a significant role in the efficient spread of SARS-CoV-2 infection, while this was not the case with SARS-CoV. SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds, but not by α2–3 analog, in VeroE6/TMPRSS2 cells. The α2-6-linked compound bound to SARS-CoV-2 spike S1 subunit to competitively inhibit SARS-CoV-2 attachment to cells. Enzymatic removal of cell surface sialic acids impaired the interaction between SARS-CoV-2 spike and angiotensin-converting enzyme 2 (ACE2), and suppressed the efficient spread of SARS-CoV-2 infection over time, in contrast to its least effect on SARS-CoV spread. Our study provides a novel molecular basis of SARS-CoV-2 infection which illustrates the distinctive characteristics from SARS-CoV. SARS-CoV-2, which has been highly transmissible and rapidly spreading worldwide, has caused approximately 458 million confirmed cases of COVID-19 with more than 6 million deaths by March 2022. Here we found that SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds and by depletion of cell surface sialic acid with only a minor effect on SARS-CoV infection. We identified that SARS-CoV-2 spike S1 subunit directly binds to α2-6-linked sialoglycans for efficient attachment to host cell surface. Our finding indicated that host sialoglycans play a significant role in the efficient infection of SARS-CoV-2, which provides a novel understanding of the molecular basis explaining the rapid spread of SARS-CoV-2 over SARS-CoV.
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-CoV-2 and SARS-CoV has been poorly defined. Here we identified that host sialoglycans play a significant role in the efficient spread of SARS-CoV-2 infection, while this was not the case with SARS-CoV. SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds, but not by α2-3 analog, in VeroE6/TMPRSS2 cells. The α2-6-linked compound bound to SARS-CoV-2 spike S1 subunit to competitively inhibit SARS-CoV-2 attachment to cells. Enzymatic removal of cell surface sialic acids impaired the interaction between SARS-CoV-2 spike and angiotensin-converting enzyme 2 (ACE2), and suppressed the efficient spread of SARS-CoV-2 infection over time, in contrast to its least effect on SARS-CoV spread. Our study provides a novel molecular basis of SARS-CoV-2 infection which illustrates the distinctive characteristics from SARS-CoV.Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of genetically- and virologically-related SARS-CoV. However, the molecular basis explaining the difference in the virological characteristics among SARS-CoV-2 and SARS-CoV has been poorly defined. Here we identified that host sialoglycans play a significant role in the efficient spread of SARS-CoV-2 infection, while this was not the case with SARS-CoV. SARS-CoV-2 infection was significantly inhibited by α2-6-linked sialic acid-containing compounds, but not by α2-3 analog, in VeroE6/TMPRSS2 cells. The α2-6-linked compound bound to SARS-CoV-2 spike S1 subunit to competitively inhibit SARS-CoV-2 attachment to cells. Enzymatic removal of cell surface sialic acids impaired the interaction between SARS-CoV-2 spike and angiotensin-converting enzyme 2 (ACE2), and suppressed the efficient spread of SARS-CoV-2 infection over time, in contrast to its least effect on SARS-CoV spread. Our study provides a novel molecular basis of SARS-CoV-2 infection which illustrates the distinctive characteristics from SARS-CoV.
Author Nakakita, Shin-ichi
Watashi, Koichi
Sriwilaijaroen, Nongluk
Takeda, Makoto
Suzuki, Yasuo
Yamasaki, Masako
Watanabe, Noriyuki
Takahashi, Yoshimasa
Saso, Wakana
Muramatsu, Masamichi
Matano, Tetsuro
Fukushi, Shuetsu
Kanie, Osamu
Tsuchimoto, Kana
AuthorAffiliation 4 Department of Applied Biological Sciences, Tokyo University of Science, Noda, Japan
7 Research Center for Drug and Vaccine Development, National Institute of Infectious Diseases, Tokyo, Japan
University of Wisconsin-Madison, UNITED STATES
3 AIDS Research Center, National Institute of Infectious Diseases, Tokyo, Japan
6 Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan
2 The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
10 Micro/Nano Technology Center and Department of Applied Biochemistry, Tokai University, Kanagawa, Japan
11 Department of Virology III, National Institute of Infectious Diseases, Tokyo, Japan
1 Department of Virology II, National Institute of Infectious Diseases, Tokyo, Japan
9 Department of Medical Biochemistry, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan
5 Department of Functional Glycomics, Life Science Research Center, Kagawa University, Kagawa, Japan
8 Department of Preclinical Sciences, Fa
AuthorAffiliation_xml – name: 2 The Institute of Medical Science, The University of Tokyo, Tokyo, Japan
– name: 4 Department of Applied Biological Sciences, Tokyo University of Science, Noda, Japan
– name: 7 Research Center for Drug and Vaccine Development, National Institute of Infectious Diseases, Tokyo, Japan
– name: 13 MIRAI, JST, Saitama, Japan
– name: 6 Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan
– name: University of Wisconsin-Madison, UNITED STATES
– name: 11 Department of Virology III, National Institute of Infectious Diseases, Tokyo, Japan
– name: 12 Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan
– name: 9 Department of Medical Biochemistry, School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, Japan
– name: 3 AIDS Research Center, National Institute of Infectious Diseases, Tokyo, Japan
– name: 5 Department of Functional Glycomics, Life Science Research Center, Kagawa University, Kagawa, Japan
– name: 1 Department of Virology II, National Institute of Infectious Diseases, Tokyo, Japan
– name: 10 Micro/Nano Technology Center and Department of Applied Biochemistry, Tokai University, Kanagawa, Japan
– name: 8 Department of Preclinical Sciences, Faculty of Medicine, Thammasat University, Pathumthani, Thailand
Author_xml – sequence: 1
  givenname: Wakana
  surname: Saso
  fullname: Saso, Wakana
– sequence: 2
  givenname: Masako
  surname: Yamasaki
  fullname: Yamasaki, Masako
– sequence: 3
  givenname: Shin-ichi
  surname: Nakakita
  fullname: Nakakita, Shin-ichi
– sequence: 4
  givenname: Shuetsu
  surname: Fukushi
  fullname: Fukushi, Shuetsu
– sequence: 5
  givenname: Kana
  surname: Tsuchimoto
  fullname: Tsuchimoto, Kana
– sequence: 6
  givenname: Noriyuki
  surname: Watanabe
  fullname: Watanabe, Noriyuki
– sequence: 7
  givenname: Nongluk
  surname: Sriwilaijaroen
  fullname: Sriwilaijaroen, Nongluk
– sequence: 8
  givenname: Osamu
  surname: Kanie
  fullname: Kanie, Osamu
– sequence: 9
  givenname: Masamichi
  surname: Muramatsu
  fullname: Muramatsu, Masamichi
– sequence: 10
  givenname: Yoshimasa
  surname: Takahashi
  fullname: Takahashi, Yoshimasa
– sequence: 11
  givenname: Tetsuro
  surname: Matano
  fullname: Matano, Tetsuro
– sequence: 12
  givenname: Makoto
  surname: Takeda
  fullname: Takeda, Makoto
– sequence: 13
  givenname: Yasuo
  surname: Suzuki
  fullname: Suzuki, Yasuo
– sequence: 14
  givenname: Koichi
  orcidid: 0000-0002-4536-9966
  surname: Watashi
  fullname: Watashi, Koichi
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35700214$$D View this record in MEDLINE/PubMed
BookMark eNp9kl2PEyEUhidmjfuh_8AoiTfetMIMDMWLTczGj0028UK9JgwcWhoKIzBN6q-X2tbsboxXEM77PrwczmVzFmKApnlJ8Jx0nLxbxykF5efjqMqcYIKZwE-aC8JYN-Mdp2f39ufNZc5rjCnpSP-sOe8Yx7gl9KL59c0tg7NOq1BQih5QtGgVc0HZKb_zqoBBS7-r9YxcQGUFdbGgi4sBqWBQHhMos7dl2EICpPRUACXIo0uqxLRDeRdMihtAOqYY1NalKaP2efPUKp_hxXG9an58-vj95svs7uvn25sPdzPNRFtmmgIR3UIMvDWcUGbxYAntDVArBqoY76ihBgwxHab9wOjQEqIFwdZyGPq-u2peH7ijj1ke25Zl2wvM27a2oipuDwoT1VqOyW1U2smonPxzENNSqlSc9iD7oYLxQEgvKOWEDcxaihe0FbW3SrDKuj7eNg0bMBpCSco_gD6sBLeSy7iVggiOO1EBb4-AFH9OkIvcuKzBexUgTvvcvGeM9nhRpW8eSf_9ulf3E_2NchqCKnh_EOgUc05gpXZF7T-4BnReEiz3E3eCy_3EyePEVTN9ZD7x_2v7DQws3sc
CitedBy_id crossref_primary_10_1371_journal_ppat_1012365
crossref_primary_10_1007_s12272_024_01492_3
crossref_primary_10_1021_jacs_4c05805
crossref_primary_10_1016_j_carbpol_2024_123177
crossref_primary_10_1016_j_bios_2024_116883
crossref_primary_10_1016_j_phyplu_2024_100663
crossref_primary_10_3390_v15020452
crossref_primary_10_3390_ijerph20042854
crossref_primary_10_1002_chem_202301555
crossref_primary_10_1128_jvi_00958_22
crossref_primary_10_1126_sciadv_adk4920
crossref_primary_10_1128_jvi_00601_23
crossref_primary_10_1038_s41598_023_28572_6
crossref_primary_10_29105_cienciauanl26_119_3
crossref_primary_10_3390_vaccines12111236
crossref_primary_10_1016_j_acthis_2023_152077
crossref_primary_10_1371_journal_ppat_1010905
crossref_primary_10_1016_j_antiviral_2024_105992
crossref_primary_10_1021_acschembio_3c00066
crossref_primary_10_1016_j_bbih_2024_100905
crossref_primary_10_1002_iub_2692
crossref_primary_10_1021_acsinfecdis_2c00383
crossref_primary_10_3390_foods13010145
crossref_primary_10_1016_j_ejmech_2023_115723
Cites_doi 10.1038/nature02145
10.1016/j.isci.2021.102367
10.1038/s41586-020-2180-5
10.1073/pnas.0409465102
10.1038/nbt1375
10.1016/j.cell.2020.02.052
10.1007/978-1-0716-0430-4_47
10.1093/glycob/2.1.25
10.1007/978-1-0716-0430-4_48
10.15252/msb.20209610
10.1371/journal.ppat.1003223
10.1038/s41591-020-0868-6
10.1007/BF01863914
10.1128/jvi.70.8.5634-5637.1996
10.1007/978-1-4939-3136-1_16
10.1038/s41598-020-62074-z
10.1038/nature12005
10.1038/357420a0
10.3389/fmolb.2021.690655
10.1073/pnas.85.12.4526
10.3389/fmicb.2021.651403
10.2807/1560-7917.ES.2020.25.3.2000045
10.1038/s41586-020-2577-1
10.1073/pnas.1811064116
10.1021/acscentsci.0c00855
10.1038/s41586-020-2012-7
10.1371/journal.pone.0215822
10.1073/pnas.2003138117
10.1038/s41422-020-0282-0
10.1016/j.ijantimicag.2020.105960
10.1371/journal.pbio.3001128
10.1128/JVI.00566-10
10.1126/science.abb2762
10.1016/j.bbrc.2004.05.107
10.1038/s41589-021-00924-1
10.1038/s41467-020-20457-w
10.1038/s41467-020-15562-9
10.1016/bs.accb.2018.09.004
10.1093/jac/dkv193
10.1128/JVI.02499-09
10.1073/pnas.2012939117
10.1016/j.molcel.2020.04.022
10.1074/jbc.REV120.013309
10.1128/JVI.00854-15
10.1002/(SICI)1521-3773(19980619)37:11<1524::AID-ANIE1524>3.0.CO;2-D
10.26508/lsa.202000786
10.1006/viro.1993.1360
10.1016/j.bmc.2006.11.006
10.1111/febs.14431
10.1007/978-1-0716-0430-4_49
10.1016/j.tim.2016.07.005
10.1038/s41594-019-0334-7
10.3390/v12090909
10.1073/pnas.2002589117
10.1099/vir.0.80955-0
10.1016/j.cell.2020.09.033
10.1074/jbc.M113.501122
ContentType Journal Article
Copyright 2022 Saso et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 Saso et al 2022 Saso et al
Copyright_xml – notice: 2022 Saso et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2022 Saso et al 2022 Saso et al
DBID AAYXX
CITATION
NPM
3V.
7QL
7U9
7X7
7XB
88E
8FE
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
7X8
5PM
DOA
DOI 10.1371/journal.ppat.1010590
DatabaseName CrossRef
PubMed
ProQuest Central (Corporate)
Bacteriology Abstracts (Microbiology B)
Virology and AIDS Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One
ProQuest Central
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
Medical Database
Biological Science Database
ProQuest Central Premium
ProQuest One Academic (New)
Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
PubMed
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Health & Medical Research Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList PubMed
CrossRef


Publicly Available Content Database

MEDLINE - Academic
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate Role of host sialylated glycans in SARS-CoV-2 infection and spread
EISSN 1553-7374
ExternalDocumentID 2690722357
oai_doaj_org_article_6b10f0b116944715b5ff408429413a95
PMC9197039
35700214
10_1371_journal_ppat_1010590
Genre Journal Article
GrantInformation_xml – fundername: ;
– fundername: ;
  grantid: JP21H02449
– fundername: ;
  grantid: JP20fk0310103
– fundername: ;
  grantid: JP20wm0325007
– fundername: ;
  grantid: JP20fk0310114
– fundername: ;
  grantid: JP20fk0310101
– fundername: ;
  grantid: JP20fk0108411
– fundername: ;
  grantid: JP20fk0108505
– fundername: ;
  grantid: JP20fk0108511
– fundername: ;
  grantid: JP22fk0310504
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACGFO
ACIHN
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFKRA
AFPKN
AFRAH
AHMBA
ALMA_UNASSIGNED_HOLDINGS
AOIJS
B0M
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAP
EAS
EBD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IHR
INH
INR
ISN
ISR
ITC
KQ8
LK8
M1P
M48
M7P
MM.
O5R
O5S
OK1
OVT
P2P
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
PV9
QF4
QN7
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
~8M
ADRAZ
H13
IPNFZ
NPM
RIG
WOQ
3V.
7QL
7U9
7XB
8FK
AZQEC
C1K
DWQXO
GNUQQ
H94
K9.
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQUKI
7X8
5PM
PUEGO
AAPBV
ABPTK
ACDSR
BBAFP
M~E
UMP
ID FETCH-LOGICAL-c592t-c4e19389b72d7145f0bf146de4f9b4a5734d4ded1d3046b54b211c910ff7eb663
IEDL.DBID M48
ISSN 1553-7374
1553-7366
IngestDate Sun Nov 06 00:10:34 EDT 2022
Wed Aug 27 01:30:22 EDT 2025
Thu Aug 21 17:30:33 EDT 2025
Mon Jul 21 09:37:41 EDT 2025
Fri Jul 25 11:59:51 EDT 2025
Thu Apr 03 07:04:28 EDT 2025
Thu Apr 24 22:56:13 EDT 2025
Tue Jul 01 01:51:12 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 6
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c592t-c4e19389b72d7145f0bf146de4f9b4a5734d4ded1d3046b54b211c910ff7eb663
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
The authors have declared that no competing interests exist.
ORCID 0000-0002-4536-9966
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.ppat.1010590
PMID 35700214
PQID 2690722357
PQPubID 1436335
ParticipantIDs plos_journals_2690722357
doaj_primary_oai_doaj_org_article_6b10f0b116944715b5ff408429413a95
pubmedcentral_primary_oai_pubmedcentral_nih_gov_9197039
proquest_miscellaneous_2676554608
proquest_journals_2690722357
pubmed_primary_35700214
crossref_citationtrail_10_1371_journal_ppat_1010590
crossref_primary_10_1371_journal_ppat_1010590
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2022-06-01
PublicationDateYYYYMMDD 2022-06-01
PublicationDate_xml – month: 06
  year: 2022
  text: 2022-06-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS pathogens
PublicationTitleAlternate PLoS Pathog
PublicationYear 2022
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References M Seyran (ppat.1010590.ref020) 2020
N Jia (ppat.1010590.ref042) 2020; 10
MA Langereis (ppat.1010590.ref029) 2010; 84
YJ Park (ppat.1010590.ref039) 2019; 26
L Riva (ppat.1010590.ref056) 2020; 586
VS Raj (ppat.1010590.ref009) 2013; 495
M Iwamoto (ppat.1010590.ref063) 2019; 116
W Sungnak (ppat.1010590.ref046) 2020; 26
H Chu (ppat.1010590.ref028) 2021; 12
M Awasthi (ppat.1010590.ref021) 2020; 12
ppat.1010590.ref002
N Sriwilaijaroen (ppat.1010590.ref015) 2020; 2132
N Nao (ppat.1010590.ref048) 2019; 14
S Matsuyama (ppat.1010590.ref047) 2020; 117
M Wang (ppat.1010590.ref057) 2020; 30
KS Kim (ppat.1010590.ref003) 2021; 19
A Varki (ppat.1010590.ref033) 2015
K Shionoya (ppat.1010590.ref054) 2021; 12
T Walther (ppat.1010590.ref041) 2013; 9
A Chandrasekaran (ppat.1010590.ref040) 2008; 26
J Shang (ppat.1010590.ref005) 2020; 117
BR Wasik (ppat.1010590.ref036) 2016; 24
TM Clausen (ppat.1010590.ref027) 2020; 183
M Hoffmann (ppat.1010590.ref006) 2020; 78
SI Nakakita (ppat.1010590.ref061) 2020; 2132
R Yan (ppat.1010590.ref014) 2020; 367
X Huang (ppat.1010590.ref017) 2015; 89
M Matrosovich (ppat.1010590.ref034) 2015; 367
WHO (ppat.1010590.ref001) 2022
H Ohashi (ppat.1010590.ref053) 2021; 24
D Bestle (ppat.1010590.ref007) 2020; 3
T Mizutani (ppat.1010590.ref055) 2004; 319
S Weston (ppat.1010590.ref058) 2020; 117
W Li (ppat.1010590.ref011) 2003; 426
W Li (ppat.1010590.ref018) 2017; 114
J Lan (ppat.1010590.ref004) 2020; 581
N Sriwilaijaroen (ppat.1010590.ref025) 2015; 70
H Hofmann (ppat.1010590.ref010) 2005; 102
VM Corman (ppat.1010590.ref052) 2020; 25
P Zhou (ppat.1010590.ref012) 2020; 579
H Kamitakahara (ppat.1010590.ref050) 1998; 37
N Sriwilaijaroen (ppat.1010590.ref026) 2020; 2132
BS Blaum (ppat.1010590.ref035) 2019; 76
K Watashi (ppat.1010590.ref064) 2013; 288
H Tani (ppat.1010590.ref060) 2010; 84
X Ou (ppat.1010590.ref019) 2020; 11
J Fantini (ppat.1010590.ref031) 2020; 55
AN Baker (ppat.1010590.ref023) 2020; 6
G. Kärber (ppat.1010590.ref051) 1931; 162
E Milanetti (ppat.1010590.ref022) 2021; 8
L Nguyen (ppat.1010590.ref024) 2022; 18
B Schultze (ppat.1010590.ref030) 1996; 70
S Fukushi (ppat.1010590.ref059) 2005; 86
F Hikmet (ppat.1010590.ref045) 2020; 16
F Kunkel (ppat.1010590.ref038) 1993; 195
M Ogata (ppat.1010590.ref049) 2007; 15
S Nakakita (ppat.1010590.ref062) 2016; 1368
M Hoffmann (ppat.1010590.ref013) 2020; 181
N Sriwilaijaroen (ppat.1010590.ref037) 2020; 8
N Sriwilaijaroen (ppat.1010590.ref043) 2018; 285
AJ Thompson (ppat.1010590.ref044) 2021; 296
CL Yeager (ppat.1010590.ref008) 1992; 357
R Vlasak (ppat.1010590.ref016) 1988; 85
A. Varki (ppat.1010590.ref032) 1992; 2
References_xml – volume: 426
  start-page: 450
  issue: 6965
  year: 2003
  ident: ppat.1010590.ref011
  article-title: Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus
  publication-title: Nature
  doi: 10.1038/nature02145
– volume: 24
  start-page: 102367
  issue: 4
  year: 2021
  ident: ppat.1010590.ref053
  article-title: Potential anti-COVID-19 agents, cepharanthine and nelfinavir, and their usage for combination treatment.
  publication-title: iScience
  doi: 10.1016/j.isci.2021.102367
– volume: 367
  start-page: 1
  year: 2015
  ident: ppat.1010590.ref034
  article-title: Sialic Acid Receptors of Viruses
  publication-title: Top Curr Chem
– volume: 581
  start-page: 215
  issue: 7807
  year: 2020
  ident: ppat.1010590.ref004
  article-title: Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor
  publication-title: Nature
  doi: 10.1038/s41586-020-2180-5
– volume: 8
  issue: 4
  year: 2020
  ident: ppat.1010590.ref037
  article-title: Host Receptors of Influenza Viruses and Coronaviruses-Molecular Mechanisms of Recognition.
  publication-title: Vaccines (Basel).
– volume: 102
  start-page: 7988
  issue: 22
  year: 2005
  ident: ppat.1010590.ref010
  article-title: Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.0409465102
– volume: 26
  start-page: 107
  issue: 1
  year: 2008
  ident: ppat.1010590.ref040
  article-title: Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin
  publication-title: Nat Biotechnol
  doi: 10.1038/nbt1375
– volume: 181
  start-page: 271
  issue: 2
  year: 2020
  ident: ppat.1010590.ref013
  article-title: SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor
  publication-title: Cell
  doi: 10.1016/j.cell.2020.02.052
– volume: 2132
  start-page: 483
  year: 2020
  ident: ppat.1010590.ref015
  article-title: Sialoglycovirology of Lectins: Sialyl Glycan Binding of Enveloped and Non-enveloped Viruses.
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-0716-0430-4_47
– volume: 2
  start-page: 25
  issue: 1
  year: 1992
  ident: ppat.1010590.ref032
  article-title: Diversity in the sialic acids
  publication-title: Glycobiology
  doi: 10.1093/glycob/2.1.25
– volume: 2132
  start-page: 547
  year: 2020
  ident: ppat.1010590.ref026
  article-title: Hemagglutinin Inhibitors are Potential Future Anti-Influenza Drugs for Mono- and Combination Therapies
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-0716-0430-4_48
– volume: 16
  start-page: e9610
  issue: 7
  year: 2020
  ident: ppat.1010590.ref045
  article-title: The protein expression profile of ACE2 in human tissues
  publication-title: Mol Syst Biol
  doi: 10.15252/msb.20209610
– volume: 9
  start-page: e1003223
  issue: 3
  year: 2013
  ident: ppat.1010590.ref041
  article-title: Glycomic analysis of human respiratory tract tissues and correlation with influenza virus infection.
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1003223
– volume: 26
  start-page: 681
  issue: 5
  year: 2020
  ident: ppat.1010590.ref046
  article-title: SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes
  publication-title: Nat Med
  doi: 10.1038/s41591-020-0868-6
– volume: 162
  start-page: 480
  year: 1931
  ident: ppat.1010590.ref051
  article-title: Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche.
  publication-title: Naunyn Schmiedebergs Arch Exp Pathol Pharmakol
  doi: 10.1007/BF01863914
– volume: 70
  start-page: 5634
  issue: 8
  year: 1996
  ident: ppat.1010590.ref030
  article-title: Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity.
  publication-title: J Virol
  doi: 10.1128/jvi.70.8.5634-5637.1996
– volume: 1368
  start-page: 225
  year: 2016
  ident: ppat.1010590.ref062
  article-title: Preparation of Glycan Arrays Using Pyridylaminated Glycans.
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-4939-3136-1_16
– volume: 10
  start-page: 5320
  issue: 1
  year: 2020
  ident: ppat.1010590.ref042
  article-title: The Human Lung Glycome Reveals Novel Glycan Ligands for Influenza A Virus.
  publication-title: Sci Rep
  doi: 10.1038/s41598-020-62074-z
– volume: 495
  start-page: 251
  issue: 7440
  year: 2013
  ident: ppat.1010590.ref009
  article-title: Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC
  publication-title: Nature
  doi: 10.1038/nature12005
– volume: 357
  start-page: 420
  issue: 6377
  year: 1992
  ident: ppat.1010590.ref008
  article-title: Human aminopeptidase N is a receptor for human coronavirus 229E.
  publication-title: Nature
  doi: 10.1038/357420a0
– volume: 8
  start-page: 690655
  year: 2021
  ident: ppat.1010590.ref022
  article-title: In-Silico Evidence for a Two Receptor Based Strategy of SARS-CoV-2.
  publication-title: Front Mol Biosci.
  doi: 10.3389/fmolb.2021.690655
– volume: 85
  start-page: 4526
  issue: 12
  year: 1988
  ident: ppat.1010590.ref016
  article-title: Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.85.12.4526
– volume: 12
  start-page: 651403
  year: 2021
  ident: ppat.1010590.ref054
  article-title: Mefloquine, a Potent Anti-severe Acute Respiratory Syndrome-Related Coronavirus 2 (SARS-CoV-2) Drug as an Entry Inhibitor in vitro.
  publication-title: Front Microbiol.
  doi: 10.3389/fmicb.2021.651403
– volume: 25
  issue: 3
  year: 2020
  ident: ppat.1010590.ref052
  article-title: Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR.
  publication-title: Euro Surveill.
  doi: 10.2807/1560-7917.ES.2020.25.3.2000045
– volume: 586
  start-page: 113
  issue: 7827
  year: 2020
  ident: ppat.1010590.ref056
  article-title: Discovery of SARS-CoV-2 antiviral drugs through large-scale compound repurposing
  publication-title: Nature
  doi: 10.1038/s41586-020-2577-1
– volume: 116
  start-page: 8487
  issue: 17
  year: 2019
  ident: ppat.1010590.ref063
  article-title: Epidermal growth factor receptor is a host-entry cofactor triggering hepatitis B virus internalization
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1811064116
– start-page: 179
  volume-title: Sialic Acids and Other Nonulosonic Acids.
  year: 2015
  ident: ppat.1010590.ref033
– volume: 6
  start-page: 2046
  issue: 11
  year: 2020
  ident: ppat.1010590.ref023
  article-title: The SARS-COV-2 Spike Protein Binds Sialic Acids and Enables Rapid Detection in a Lateral Flow Point of Care Diagnostic Device.
  publication-title: ACS Cent Sci.
  doi: 10.1021/acscentsci.0c00855
– volume: 579
  start-page: 270
  issue: 7798
  year: 2020
  ident: ppat.1010590.ref012
  article-title: A pneumonia outbreak associated with a new coronavirus of probable bat origin
  publication-title: Nature
  doi: 10.1038/s41586-020-2012-7
– volume: 14
  start-page: e0215822
  issue: 4
  year: 2019
  ident: ppat.1010590.ref048
  article-title: Consensus and variations in cell line specificity among human metapneumovirus strains
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0215822
– volume: 117
  start-page: 11727
  issue: 21
  year: 2020
  ident: ppat.1010590.ref005
  article-title: Cell entry mechanisms of SARS-CoV-2
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.2003138117
– volume: 30
  start-page: 269
  issue: 3
  year: 2020
  ident: ppat.1010590.ref057
  article-title: Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro.
  publication-title: Cell Res
  doi: 10.1038/s41422-020-0282-0
– volume: 55
  start-page: 105960
  issue: 5
  year: 2020
  ident: ppat.1010590.ref031
  article-title: Structural and molecular modelling studies reveal a new mechanism of action of chloroquine and hydroxychloroquine against SARS-CoV-2 infection.
  publication-title: Int J Antimicrob Agents
  doi: 10.1016/j.ijantimicag.2020.105960
– volume: 19
  start-page: e3001128
  issue: 3
  year: 2021
  ident: ppat.1010590.ref003
  article-title: A quantitative model used to compare within-host SARS-CoV-2, MERS-CoV, and SARS-CoV dynamics provides insights into the pathogenesis and treatment of SARS-CoV-2
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.3001128
– volume: 84
  start-page: 8970
  issue: 17
  year: 2010
  ident: ppat.1010590.ref029
  article-title: Attachment of mouse hepatitis virus to O-acetylated sialic acid is mediated by hemagglutinin-esterase and not by the spike protein
  publication-title: J Virol
  doi: 10.1128/JVI.00566-10
– volume: 367
  start-page: 1444
  issue: 6485
  year: 2020
  ident: ppat.1010590.ref014
  article-title: Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2
  publication-title: Science
  doi: 10.1126/science.abb2762
– volume: 319
  start-page: 1228
  issue: 4
  year: 2004
  ident: ppat.1010590.ref055
  article-title: Phosphorylation of p38 MAPK and its downstream targets in SARS coronavirus-infected cells
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/j.bbrc.2004.05.107
– volume: 18
  start-page: 81
  issue: 1
  year: 2022
  ident: ppat.1010590.ref024
  article-title: Sialic acid-containing glycolipids mediate binding and viral entry of SARS-CoV-2
  publication-title: Nat Chem Biol
  doi: 10.1038/s41589-021-00924-1
– volume: 12
  start-page: 134
  issue: 1
  year: 2021
  ident: ppat.1010590.ref028
  article-title: Host and viral determinants for efficient SARS-CoV-2 infection of the human lung
  publication-title: Nat Commun
  doi: 10.1038/s41467-020-20457-w
– volume: 11
  start-page: 1620
  issue: 1
  year: 2020
  ident: ppat.1010590.ref019
  article-title: Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV.
  publication-title: Nat Commun.
  doi: 10.1038/s41467-020-15562-9
– volume: 76
  start-page: 65
  year: 2019
  ident: ppat.1010590.ref035
  article-title: Sialic Acids in Nonenveloped Virus Infections
  publication-title: Adv Carbohydr Chem Biochem
  doi: 10.1016/bs.accb.2018.09.004
– volume: 70
  start-page: 2797
  issue: 10
  year: 2015
  ident: ppat.1010590.ref025
  article-title: 6SLN-lipo PGA specifically catches (coats) human influenza virus and synergizes neuraminidase-targeting drugs for human influenza therapeutic potential.
  publication-title: J Antimicrob Chemother
  doi: 10.1093/jac/dkv193
– volume: 84
  start-page: 2798
  issue: 6
  year: 2010
  ident: ppat.1010590.ref060
  article-title: Involvement of ceramide in the propagation of Japanese encephalitis virus
  publication-title: J Virol
  doi: 10.1128/JVI.02499-09
– volume: 117
  start-page: 30687
  issue: 48
  year: 2020
  ident: ppat.1010590.ref058
  article-title: The SKI complex is a broad-spectrum, host-directed antiviral drug target for coronaviruses, influenza, and filoviruses
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.2012939117
– volume: 78
  start-page: 779
  issue: 4
  year: 2020
  ident: ppat.1010590.ref006
  article-title: A Multibasic Cleavage Site in the Spike Protein of SARS-CoV-2 Is Essential for Infection of Human Lung Cells
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2020.04.022
– volume: 296
  start-page: 100017
  year: 2021
  ident: ppat.1010590.ref044
  article-title: Adaptation of influenza viruses to human airway receptors
  publication-title: J Biol Chem
  doi: 10.1074/jbc.REV120.013309
– volume: 89
  start-page: 7202
  issue: 14
  year: 2015
  ident: ppat.1010590.ref017
  article-title: Human Coronavirus HKU1 Spike Protein Uses O-Acetylated Sialic Acid as an Attachment Receptor Determinant and Employs Hemagglutinin-Esterase Protein as a Receptor-Destroying Enzyme
  publication-title: J Virol
  doi: 10.1128/JVI.00854-15
– volume: 37
  start-page: 1524
  issue: 11
  year: 1998
  ident: ppat.1010590.ref050
  article-title: A Lysoganglioside/Poly-L-glutamic Acid Conjugate as a Picomolar Inhibitor of Influenza Hemagglutinin
  publication-title: Angew Chem Int Ed Engl
  doi: 10.1002/(SICI)1521-3773(19980619)37:11<1524::AID-ANIE1524>3.0.CO;2-D
– ident: ppat.1010590.ref002
– volume: 3
  issue: 9
  year: 2020
  ident: ppat.1010590.ref007
  article-title: TMPRSS2 and furin are both essential for proteolytic activation of SARS-CoV-2 in human airway cells
  publication-title: Life Sci Alliance
  doi: 10.26508/lsa.202000786
– volume: 195
  start-page: 195
  issue: 1
  year: 1993
  ident: ppat.1010590.ref038
  article-title: Structural and functional analysis of the surface protein of human coronavirus OC43
  publication-title: Virology
  doi: 10.1006/viro.1993.1360
– volume: 15
  start-page: 1383
  issue: 3
  year: 2007
  ident: ppat.1010590.ref049
  article-title: Chemoenzymatic synthesis of artificial glycopolypeptides containing multivalent sialyloligosaccharides with a gamma-polyglutamic acid backbone and their effect on inhibition of infection by influenza viruses
  publication-title: Bioorg Med Chem
  doi: 10.1016/j.bmc.2006.11.006
– volume: 285
  start-page: 1611
  issue: 9
  year: 2018
  ident: ppat.1010590.ref043
  article-title: N-glycan structures of human alveoli provide insight into influenza A virus infection and pathogenesis.
  publication-title: FEBS J
  doi: 10.1111/febs.14431
– volume: 2132
  start-page: 567
  year: 2020
  ident: ppat.1010590.ref061
  article-title: Preparation and Detection of Glycan-Binding Activity of Influenza Virus.
  publication-title: Methods Mol Biol
  doi: 10.1007/978-1-0716-0430-4_49
– volume: 24
  start-page: 991
  issue: 12
  year: 2016
  ident: ppat.1010590.ref036
  article-title: Effects of Sialic Acid Modifications on Virus Binding and Infection
  publication-title: Trends Microbiol
  doi: 10.1016/j.tim.2016.07.005
– volume: 26
  start-page: 1151
  issue: 12
  year: 2019
  ident: ppat.1010590.ref039
  article-title: Structures of MERS-CoV spike glycoprotein in complex with sialoside attachment receptors
  publication-title: Nat Struct Mol Biol
  doi: 10.1038/s41594-019-0334-7
– year: 2020
  ident: ppat.1010590.ref020
  article-title: The structural basis of accelerated host cell entry by SARS-CoV-2dagger.
  publication-title: FEBS J.
– volume: 12
  issue: 9
  year: 2020
  ident: ppat.1010590.ref021
  article-title: The Sialoside-Binding Pocket of SARS-CoV-2 Spike Glycoprotein Structurally Resembles MERS-CoV.
  publication-title: Viruses
  doi: 10.3390/v12090909
– volume: 117
  start-page: 7001
  issue: 13
  year: 2020
  ident: ppat.1010590.ref047
  article-title: Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.2002589117
– volume: 114
  start-page: E8508
  issue: 40
  year: 2017
  ident: ppat.1010590.ref018
  article-title: Identification of sialic acid-binding function for the Middle East respiratory syndrome coronavirus spike glycoprotein
  publication-title: Proc Natl Acad Sci U S A
– year: 2022
  ident: ppat.1010590.ref001
  publication-title: WHO Coronavirus (COVID-19) Dashboard.
– volume: 86
  start-page: 2269
  issue: Pt 8
  year: 2005
  ident: ppat.1010590.ref059
  article-title: Vesicular stomatitis virus pseudotyped with severe acute respiratory syndrome coronavirus spike protein
  publication-title: J Gen Virol
  doi: 10.1099/vir.0.80955-0
– volume: 183
  start-page: 1043
  issue: 4
  year: 2020
  ident: ppat.1010590.ref027
  article-title: SARS-CoV-2 Infection Depends on Cellular Heparan Sulfate and ACE2
  publication-title: Cell
  doi: 10.1016/j.cell.2020.09.033
– volume: 288
  start-page: 31715
  issue: 44
  year: 2013
  ident: ppat.1010590.ref064
  article-title: Interleukin-1 and tumor necrosis factor-alpha trigger restriction of hepatitis B virus infection via a cytidine deaminase activation-induced cytidine deaminase (AID).
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M113.501122
SSID ssj0041316
Score 2.5003362
Snippet Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has been transmitted across all over the world, in contrast to the limited epidemic of...
SourceID plos
doaj
pubmedcentral
proquest
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1010590
SubjectTerms ACE2
Acids
Angiotensin
Angiotensin-converting enzyme 2
Biology and life sciences
Cell surface
Coronaviruses
COVID-19
Epidemics
Infections
Medicine and health sciences
Middle East respiratory syndrome
Peptidyl-dipeptidase A
Physical Sciences
Polysaccharides
Respiratory diseases
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Sialic acids
Viral diseases
Viral infections
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Ra9swEBalMOjLWLd29dqVG_RVbSzLlvW4jZUy2F62Qt-MZEldICghTgbZr9-dbGfNKPSlrz4ZW3fnu0_W6TvGLrRutSvbwJ3LHZdeBm4xkXEtnRPBIsJPBKbfvlc3t_LrXXn3oNUX1YT19MC94q4qm0_CxOZ5pSUG0tKWIchJjWEUw6_Rib0Uc964mOpjMIpS01NqisNVUVXDoblC5VeDjS4XC5Poo-n05U5SStz9xHU6m3eP4c7_yycf5KPrV-zlACThYz-BQ7bn42v2om8tuXnD_vyY3kcqA0LNAZUQwjwAneiADj1uM0OI6eB-tkF5B9MIiANhLMyKYKKDboF40tFtmDz90oNp1ysPy3978zDSHUBLPAjm93S57kAcsdvrLz8_3_ChzwJvSy1WvJUeYVytrRJO5bJEdQcMoA4Np600pSqkk86jMWkb1ZbS4qqxRZwRAnVUqYpjth_n0Z8wEMIXBlVqyVy1t0ZVxhrjnamlsa7OWDEqumkHEnLqhTFr0s6awsVIr76GzNMM5skY39616Ek4nhj_iWy4HUsU2ukCOlYzOFbzlGNl7IQ8YHxA1wj6kSCIHihjZ6NXPC7-sBXjx0o7MCb6-ZrGqIrKAieoiLe9E21fsqBOAyKXGVM77rUzi11JnP5KhOA61xi49bvnmPYpOxB0wiP9aDpj-6vl2r9H3LWy5-kT-wufgiwM
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV3di9QwEA96Ivgifl_1lAi-xtumadM8iYrHIeiLHuxbSZpkXVjaXrsr7P31N5OmPVcOfW0SmsxMZiaZyW8IeadUrWxee2ZtaplwwjMDhowpYS33Bjz8AGD67XtxfiG-LvNlvHAbYlrlpBODorZtjXfkpxyPcRzBWT50lwyrRmF0NZbQuEvuIXQZSrVczgcu0M-h9CmWxmEyK4r4dC6T6Wnk1Puu0wFEGt9gHpimgOCPiKebdrjN-_w7ifIPq3T2iDyM7iT9OPL_Mbnjmifk_lhgcv-UXP1YrxpMBgL6UUwkpK2n-K6DDiB3-w04mpauNntoH-i6oeAN0ik9q6G6sXTowKu0OAxMqOsd1fVu62h_E6GnE-gBrRENQf9e97uB8mfk4uzLz8_nLFZbYHWu-JbVwoEzVyojuZWpyP3CeFCjFtinjNC5zIQV1gFLMZhqcmHg7FiDt-E91lUpsufkqGkbd0wo5y7TQFKTFkqUzmhZaKO1s7oU2tgyIdlE6KqOUORYEWNThfiahCPJSL4K2VNF9iSEzaO6EYrjP_0_IQ_nvgikHT60_aqK-7IqDCxgYVKcKdjp3OTei0UJVhqkR6s8IccoAdMPhupGDhNyMknF7c1v52bYshiH0Y1rd9hHFpgcuABCvBiFaJ5khvUGeCoSIg_E62AVhy3N-leABVepAvWtXv57Wq_IA44vOMJF0gk52vY79xr8qq15EzbPNUEsJWY
  priority: 102
  providerName: ProQuest
Title Significant role of host sialylated glycans in the infection and spread of severe acute respiratory syndrome coronavirus 2
URI https://www.ncbi.nlm.nih.gov/pubmed/35700214
https://www.proquest.com/docview/2690722357
https://www.proquest.com/docview/2676554608
https://pubmed.ncbi.nlm.nih.gov/PMC9197039
https://doaj.org/article/6b10f0b116944715b5ff408429413a95
http://dx.doi.org/10.1371/journal.ppat.1010590
Volume 18
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3di9QwEB_uA-VexO-rnksEX3ts27RpHkQ8ueMQ7hB1Yd9K0qTrQmnXdldc_3pn0g9dWRF83STddmaSmWQmvx_AKylzaeK88I0JjM8tL3yNjsyX3Jiw0BjhOwDTm9vkesbfz-P5AQycrb0A271bO-KTmjXl-fev2zc44V871gYRDIPOVyvlAKHpPuUhHKNvEsRpcMPHvAKu2I4MlchyfBElSX-Z7m9POYG7EQHAhwHf8VsO3p_gUMu63Rea_llh-ZvLuroP9_pYk73tjOMBHNjqIdzp2Ce3j-DHp-WiokohFC6jKkNWF4wufbAWjXJbYhRq2KLcYnvLlhXDUJENtVsVU5Vh7QpDTkPD0L_axjKVb9aWNb_S92xARGA5QSWob8tm07LwMcyuLj-_u_Z7KgY_j2W49nNuMdJLpRahEQGPi6kucI01qFupuYpFxA03FvVNmVYdc40byxxDkaIg0pUkegJHVV3ZU2BhaCOF0tVBInlqtRKJ0kpZo1KutEk9iAZBZ3mPU050GWXmkm8C9yud-DLSVNZrygN_HLXqcDr-0f-CdDj2JZRt90PdLLJ-0maJxg-Y6oDeFJ14rOOi4NMUXTgakpKxB6dkAcMftFlIZw0hIQh5cDZYxf7ml2MzzmdK0qjK1hvqIxKqHJyiIJ52RjS-5GCLHogd89r5it2WavnFYYbLQOLaLp_998jncBLSzQ93AHUGR-tmY19gPLbWEzgUczGB44vL2w8fJ-5UY-Km3U_ElTvy
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Lb9QwELZKEYIL4tkGChgJjqaJ4zx8QIhXtaWPC620t2DH9rLSKgnJLmj5UfxGZvIqiyo49bp2so5nMvNNPDMfIS-kzKWJcseMCQwTVjimwZExKYzhTgPCbxuYnpzGk3PxaRpNt8ivoRYG0yoHm9gaalPm-I18n2MYx7E5y5vqG0PWKDxdHSg0OrU4susfELI1rw8_gHxfcn7w8ez9hPWsAiyPJF-yXFgALanUCTdJICLnawfmwsAypRYqSkJhhLGwdDw01JHQECPl4FWdQ_6QOIT7XiPXwfH6GOwl0zHAA3_QUq0iFQ9LwjjuS_XCJNjvNeNVVam2aTXWfG64wpYxADusLsrmMrT7d9LmH17w4A653cNX-rbTt7tkyxb3yI2O0HJ9n_z8PJ8VmHwE8qKYuEhLR7GOhDag5-sFAFtDZ4s1jDd0XlBAn3RIByuoKgxtKkCxBi8Dl21rS1W-WlpaX2QE0KHJAs2x-4L6Pq9XDeUPyPmVyOEh2S7Kwu4SyrkNFWypDmIpUqtVEiutlDUqFUqb1CPhsNFZ3rc-RwaORdae5yUQAnXbl6F4sl48HmHjVVXX-uM_89-hDMe52Li7_aGsZ1lvB7JYwwP4OsCVAi6IdOSc8FNABaA9SkYe2UUNGP6gyS703iN7g1ZcPvx8HAYTgec-qrDlCuckMSYj-rARO50SjYsMkd-AB8IjyYZ6bTzF5kgx_9q2IZeBBHchH_17Wc_IzcnZyXF2fHh69Jjc4lg90n7E2iPby3plnwCmW-qn7YtEyZerfnN_A7JGYgs
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9MwED-NTiBeEN8LDDASPIY2jvPhB4QYW7UxqCZg0t4yO7ZLpSopTQsqfxp_HXf56Cia4GmvtZPavrPvd_Hd7wBeSJlLE-XONyYwvrDC-RoNmS-FMdxpRPg1genHUXx4Kt6fRWdb8KvLhaGwyu5MrA9qU-b0jbzPyY3jRM7Sd21YxMn-8M3sm08VpOimtSun0ajIsV39QPeten20j7J-yfnw4Mu7Q7-tMODnkeQLPxcWAUwqdcJNEojIDbTDo8PgkKUWKkpCYYSxOA26QNSR0Ogv5WhhnaNaInGI770G2wl5RT3Y3jsYnXzq7ABah7rwKhXm8ZMwjtvEvTAJ-q2evJrNVE1hTRmgG4axrh9AfKvTsroM-_4dwvmHTRzehlstmGVvG-27A1u2uAvXm_KWq3vw8_NkXFAoEkqPURgjKx2jrBJWodavpghzDRtPV9hesUnBEIuyLjisYKowrJohpjX0GBpwO7dM5cuFZfOL-ADWUS6wnLgY1PfJfFkxfh9Or0QSD6BXlIXdAca5DRUuqQ5iKVKrVRIrrZQ1KhVKm9SDsFvoLG-J0KkexzSrb_cSdIia5ctIPFkrHg_89VOzhgjkP_33SIbrvkTjXf9QzsdZeypkscYJDHRAI0WUEOnIOTFIESOg9igZebBDGtD9QZVd7AIPdjutuLz5-boZDwy6BVKFLZfUJ4kpNHGAC_GwUaL1IEOqdsAD4UGyoV4bs9hsKSZfa1JyGUg0HvLRv4f1DG7grs0-HI2OH8NNTqkk9RetXegt5kv7BAHeQj9tdxKD86vevL8BD-5npg
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Significant+role+of+host+sialylated+glycans+in+the+infection+and+spread+of+severe+acute+respiratory+syndrome+coronavirus+2&rft.jtitle=PLoS+pathogens&rft.au=Saso%2C+Wakana&rft.au=Yamasaki%2C+Masako&rft.au=Nakakita%2C+Shin-ichi&rft.au=Fukushi%2C+Shuetsu&rft.date=2022-06-01&rft.pub=Public+Library+of+Science&rft.issn=1553-7366&rft.eissn=1553-7374&rft.volume=18&rft.issue=6&rft_id=info:doi/10.1371%2Fjournal.ppat.1010590&rft_id=info%3Apmid%2F35700214&rft.externalDocID=PMC9197039
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7374&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7374&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7374&client=summon