Open Access

Proceedings of the National Academy of Sciences of the United States of America, volume 119, issue 1

SARS-CoV-2 spreads through cell-to-cell transmission

Cong Zeng ^{1, 2}

John P. Evans ^{1, 2, 3}

Tiffany King ^{4, 5}

Yi-Min Zheng ^{1, 2}

Eugene M. Oltz ⁶

Sean Whelan ⁷

Linda J. Saif ^{8, 9, 10}

Mark E. Peeples ^{4, 5, 10}

Shan-Lu Liu ^{1, 2, 6, 10}

Hide authors affiliations Show authors affiliations: 10 affiliations

Center for Retrovirus Research, The Ohio State University, Columbus, OH 43210; |

Department of Veterinary Biosciences, The Ohio State University, Columbus, OH 43210; |

Molecular, Cellular, and Developmental Biology Program, The Ohio State University, Columbus, OH 43210; |

⁴

Center for Vaccines and Immunity, Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH 43205; |

⁵

Department of Pediatrics, The Ohio State University College of Medicine, Columbus, OH 43205; |

⁶

Department of Microbial Infection and Immunity, The Ohio State University College of Medicine, Columbus, OH 43210; |

⁷

Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110; |

⁸

Center for Food Animal Health, Animal Sciences Department, Ohio Agricultural Research and Development Center, College of Food, Agricultural, and Environmental Sciences, The Ohio State University, Wooster, OH 44691; |

⁹

Veterinary Preventive Medicine Department, College of Veterinary Medicine, The Ohio State University, Wooster, OH 44691; |

¹⁰

Viruses and Emerging Pathogens Program, Infectious Diseases Institute, The Ohio State University, Columbus, OH 43210 |

Publication type: Journal Article

Publication date: 2021-12-22

Proceedings of the National Academy of Sciences (PNAS)

Journal: Proceedings of the National Academy of Sciences of the United States of America

Quartile SCImago

Quartile WOS

Impact factor: 11.1

ISSN: 00278424, 10916490

DOI: 10.1073/pnas.2111400119

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Multidisciplinary

Abstract

Significance

It is currently unknown if SARS-CoV-2 can spread through cell–cell contacts, and if so, the underlying mechanisms and implications. In this work, we show, by using lentiviral pseudotyped virus, that the spike protein of SARS-CoV-2 mediates the viral cell-to-cell transmission, with an efficiency higher than that of SARS-CoV. We also find that cell–cell fusion contributes to cell-to-cell transmission, yet ACE2 is not absolutely required. While the authentic variants of concern (VOCs) B.1.1.7 (alpha) and B.1.351 (beta) differ in cell-free infectivity from wild type and from each other, these VOCs have similar cell-to-cell transmission capability and exhibit differential sensitivity to neutralization by vaccinee sera. Results from our study will contribute to a better understanding of SARS-CoV-2 spread and pathogenesis.

By date By citations

Top-30

Citations by journals

	2 4 6 8 10 12
Viruses	Viruses, 11, 7.05% Viruses 11 publications, 7.05%
iScience	iScience, 6, 3.85% iScience 6 publications, 3.85%
Journal of Virology	Journal of Virology, 6, 3.85% Journal of Virology 6 publications, 3.85%
Journal of Medical Virology	Journal of Medical Virology, 5, 3.21% Journal of Medical Virology 5 publications, 3.21%
Nature Communications	Nature Communications, 4, 2.56% Nature Communications 4 publications, 2.56%
Emerging Microbes and Infections	Emerging Microbes and Infections, 4, 2.56% Emerging Microbes and Infections 4 publications, 2.56%
Proceedings of the National Academy of Sciences of the United States of America	Proceedings of the National Academy of Sciences of the United States of America, 4, 2.56% Proceedings of the National Academy of Sciences of the United States of America 4 publications, 2.56%
International Journal of Molecular Sciences	International Journal of Molecular Sciences, 3, 1.92% International Journal of Molecular Sciences 3 publications, 1.92%
mBio	mBio, 3, 1.92% mBio 3 publications, 1.92%
Frontiers in Immunology	Frontiers in Immunology, 3, 1.92% Frontiers in Immunology 3 publications, 1.92%
Vaccines	Vaccines, 2, 1.28% Vaccines 2 publications, 1.28%
Biomedicines	Biomedicines, 2, 1.28% Biomedicines 2 publications, 1.28%
Biomedicine and Pharmacotherapy	Biomedicine and Pharmacotherapy, 2, 1.28% Biomedicine and Pharmacotherapy 2 publications, 1.28%
PLoS Pathogens	PLoS Pathogens, 2, 1.28% PLoS Pathogens 2 publications, 1.28%
MedComm	MedComm, 2, 1.28% MedComm 2 publications, 1.28%
Science advances	Science advances, 2, 1.28% Science advances 2 publications, 1.28%
PLoS Computational Biology	PLoS Computational Biology, 2, 1.28% PLoS Computational Biology 2 publications, 1.28%
Virology	Virology, 2, 1.28% Virology 2 publications, 1.28%
Journal of Biomedical Science	Journal of Biomedical Science, 2, 1.28% Journal of Biomedical Science 2 publications, 1.28%
Antiviral Research	Antiviral Research, 2, 1.28% Antiviral Research 2 publications, 1.28%
Vaccine	Vaccine, 2, 1.28% Vaccine 2 publications, 1.28%
Cell Death and Disease	Cell Death and Disease, 1, 0.64% Cell Death and Disease 1 publication, 0.64%
PLoS Biology	PLoS Biology, 1, 0.64% PLoS Biology 1 publication, 0.64%
Journal of Clinical Investigation	Journal of Clinical Investigation, 1, 0.64% Journal of Clinical Investigation 1 publication, 0.64%
Archivum Immunologiae et Therapiae Experimentalis	Archivum Immunologiae et Therapiae Experimentalis, 1, 0.64% Archivum Immunologiae et Therapiae Experimentalis 1 publication, 0.64%
Cells	Cells, 1, 0.64% Cells 1 publication, 0.64%
Virulence	Virulence, 1, 0.64% Virulence 1 publication, 0.64%
Frontiers in Molecular Biosciences	Frontiers in Molecular Biosciences, 1, 0.64% Frontiers in Molecular Biosciences 1 publication, 0.64%
Nature Immunology	Nature Immunology, 1, 0.64% Nature Immunology 1 publication, 0.64%
	2 4 6 8 10 12

Citations by publishers

	5 10 15 20 25 30
Springer Nature	Springer Nature, 30, 19.23% Springer Nature 30 publications, 19.23%
Elsevier	Elsevier, 29, 18.59% Elsevier 29 publications, 18.59%
Multidisciplinary Digital Publishing Institute (MDPI)	Multidisciplinary Digital Publishing Institute (MDPI), 23, 14.74% Multidisciplinary Digital Publishing Institute (MDPI) 23 publications, 14.74%
Cold Spring Harbor Laboratory	Cold Spring Harbor Laboratory, 14, 8.97% Cold Spring Harbor Laboratory 14 publications, 8.97%
Wiley	Wiley, 13, 8.33% Wiley 13 publications, 8.33%
American Society for Microbiology	American Society for Microbiology, 10, 6.41% American Society for Microbiology 10 publications, 6.41%
Public Library of Science (PLoS)	Public Library of Science (PLoS), 6, 3.85% Public Library of Science (PLoS) 6 publications, 3.85%
Frontiers Media S.A.	Frontiers Media S.A., 6, 3.85% Frontiers Media S.A. 6 publications, 3.85%
Proceedings of the National Academy of Sciences (PNAS)	Proceedings of the National Academy of Sciences (PNAS), 4, 2.56% Proceedings of the National Academy of Sciences (PNAS) 4 publications, 2.56%
American Association for the Advancement of Science (AAAS)	American Association for the Advancement of Science (AAAS), 3, 1.92% American Association for the Advancement of Science (AAAS) 3 publications, 1.92%
American Society for Clinical Investigation	American Society for Clinical Investigation, 2, 1.28% American Society for Clinical Investigation 2 publications, 1.28%
Taylor & Francis	Taylor & Francis, 1, 0.64% Taylor & Francis 1 publication, 0.64%
American Chemical Society (ACS)	American Chemical Society (ACS), 1, 0.64% American Chemical Society (ACS) 1 publication, 0.64%
American Society for Biochemistry and Molecular Biology	American Society for Biochemistry and Molecular Biology, 1, 0.64% American Society for Biochemistry and Molecular Biology 1 publication, 0.64%
American Thoracic Society	American Thoracic Society, 1, 0.64% American Thoracic Society 1 publication, 0.64%
Royal Society of Chemistry (RSC)	Royal Society of Chemistry (RSC), 1, 0.64% Royal Society of Chemistry (RSC) 1 publication, 0.64%
Eco-Vector LLC	Eco-Vector LLC, 1, 0.64% Eco-Vector LLC 1 publication, 0.64%
EMBO press	EMBO press, 1, 0.64% EMBO press 1 publication, 0.64%
The Royal Society	The Royal Society, 1, 0.64% The Royal Society 1 publication, 0.64%
Research Square Platform LLC	Research Square Platform LLC, 1, 0.64% Research Square Platform LLC 1 publication, 0.64%
Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii	Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii, 1, 0.64% Autonomous Non-profit Organization Editorial Board of the journal Uspekhi Khimii 1 publication, 0.64%
	5 10 15 20 25 30

We do not take into account publications without a DOI.
Statistics recalculated only for publications connected to researchers, organizations and labs registered on the platform.
Statistics recalculated weekly.

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GOST |

Cite this

GOST Copy

Zeng C. et al. SARS-CoV-2 spreads through cell-to-cell transmission // Proceedings of the National Academy of Sciences of the United States of America. 2021. Vol. 119. No. 1.

GOST all authors (up to 50) Copy

Zeng C., Evans J. P., King T., Zheng Y., Oltz E. M., Whelan S., Saif L. J., Peeples M. E., Liu S. SARS-CoV-2 spreads through cell-to-cell transmission // Proceedings of the National Academy of Sciences of the United States of America. 2021. Vol. 119. No. 1.

RIS |

Cite this

RIS Copy

TY - JOUR

DO - 10.1073/pnas.2111400119

UR - https://doi.org/10.1073/pnas.2111400119

TI - SARS-CoV-2 spreads through cell-to-cell transmission

T2 - Proceedings of the National Academy of Sciences of the United States of America

AU - Zeng, Cong

AU - Evans, John P.

AU - King, Tiffany

AU - Zheng, Yi-Min

AU - Oltz, Eugene M.

AU - Whelan, Sean

AU - Saif, Linda J.

AU - Peeples, Mark E.

AU - Liu, Shan-Lu

PY - 2021

DA - 2021/12/22 00:00:00

PB - Proceedings of the National Academy of Sciences (PNAS)

IS - 1

VL - 119

SN - 0027-8424

SN - 1091-6490

ER -

BibTex

Cite this

BibTex Copy

@article{2021_Zeng,

author = {Cong Zeng and John P. Evans and Tiffany King and Yi-Min Zheng and Eugene M. Oltz and Sean Whelan and Linda J. Saif and Mark E. Peeples and Shan-Lu Liu},

title = {SARS-CoV-2 spreads through cell-to-cell transmission},

journal = {Proceedings of the National Academy of Sciences of the United States of America},

year = {2021},

volume = {119},

publisher = {Proceedings of the National Academy of Sciences (PNAS)},

month = {dec},

url = {https://doi.org/10.1073/pnas.2111400119},

number = {1},

doi = {10.1073/pnas.2111400119}

}

Found error?

Publisher

Proceedings of the National Academy of Sciences (PNAS)

Journal

Proceedings of the National Academy of Sciences of the United States of America

Quartile SCImago

Quartile WOS

Impact factor

11.1

ISSN

00278424 (Print)
10916490 (Electronic)