SARS-CoV-2 D614G variant exhibits efficient replication ex vivo and transmission in vivo

Pandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that emerged from China has now been largely replaced by strains containing the muta...

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Published inScience (American Association for the Advancement of Science) Vol. 370; no. 6523; pp. 1464 - 1468
Main Authors Hou, Yixuan J., Chiba, Shiho, Halfmann, Peter, Ehre, Camille, Kuroda, Makoto, Dinnon, Kenneth H., Leist, Sarah R., Schäfer, Alexandra, Nakajima, Noriko, Takahashi, Kenta, Lee, Rhianna E., Mascenik, Teresa M., Graham, Rachel, Edwards, Caitlin E., Tse, Longping V., Okuda, Kenichi, Markmann, Alena J., Bartelt, Luther, de Silva, Aravinda, Margolis, David M., Boucher, Richard C., Randell, Scott H., Suzuki, Tadaki, Gralinski, Lisa E., Kawaoka, Yoshihiro, Baric, Ralph S.
Format Journal Article
LanguageEnglish
Published United States The American Association for the Advancement of Science 18.12.2020
American Association for the Advancement of Science
Subjects
ACE2
Amino Acid Substitution
Angiotensin-converting enzyme 2
Angiotensin-Converting Enzyme 2 - genetics
Animal models
Animals
Asparagine - genetics
Aspartic acid
Coronaviridae
Coronaviruses
COVID-19
COVID-19 - transmission
COVID-19 - virology
Cricetinae
Disease transmission
Fitness
Genetic Fitness - genetics
Glycine
Glycine - genetics
Hamsters
Humans
Mesocricetus
Mice
Mice, Transgenic
Microbio
Morphology
Mutation
Neutralization
Pandemics
Pathogenesis
Pathogens
Replication
Respiratory diseases
Respiratory Mucosa - virology
Rodents
SARS-CoV-2 - genetics
SARS-CoV-2 - pathogenicity
Severe acute respiratory syndrome coronavirus 2
Substitutes
Viral diseases
Virulence
Virulence - genetics
Virus Replication - genetics
Viruses
Online AccessGet full text

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Abstract Pandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that emerged from China has now been largely replaced by strains containing the mutation D614G (Asp 614 -to-Gly) in the viral spike protein. Hou et al. compared the characteristics of the new variant against the ancestral form in a series of experiments in human cells and animal models. The variant is better at infecting upper-airway epithelial cells and replicates in greater numbers than the ancestral virus. Evidence indicates modest, if any, significant changes to virulence in animal models. Therefore, the virus appears to have evolved for greater transmissibility in humans rather than for greater pathogenicity. The mutation renders the new virus variant more susceptible to neutralizing antisera without altering the efficacy of vaccine candidates currently under development. Science , this issue p. 1464 The current dominant structural variant of SARS-CoV-2 appears to have evolved from the ancestral form and enhances transmissibility. The spike aspartic acid–614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
AbstractList The spike aspartic acid-614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.The spike aspartic acid-614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
Pandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that emerged from China has now been largely replaced by strains containing the mutation D614G (Asp 614 -to-Gly) in the viral spike protein. Hou et al. compared the characteristics of the new variant against the ancestral form in a series of experiments in human cells and animal models. The variant is better at infecting upper-airway epithelial cells and replicates in greater numbers than the ancestral virus. Evidence indicates modest, if any, significant changes to virulence in animal models. Therefore, the virus appears to have evolved for greater transmissibility in humans rather than for greater pathogenicity. The mutation renders the new virus variant more susceptible to neutralizing antisera without altering the efficacy of vaccine candidates currently under development. Science , this issue p. 1464 The current dominant structural variant of SARS-CoV-2 appears to have evolved from the ancestral form and enhances transmissibility. The spike aspartic acid–614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
Changing with the timesPandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that emerged from China has now been largely replaced by strains containing the mutation D614G (Asp614-to-Gly) in the viral spike protein. Hou et al. compared the characteristics of the new variant against the ancestral form in a series of experiments in human cells and animal models. The variant is better at infecting upper-airway epithelial cells and replicates in greater numbers than the ancestral virus. Evidence indicates modest, if any, significant changes to virulence in animal models. Therefore, the virus appears to have evolved for greater transmissibility in humans rather than for greater pathogenicity. The mutation renders the new virus variant more susceptible to neutralizing antisera without altering the efficacy of vaccine candidates currently under development.Science, this issue p. 1464The spike aspartic acid–614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
The spike aspartic acid-614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
Pandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that emerged from China has now been largely replaced by strains containing the mutation D614G (Asp 614 -to-Gly) in the viral spike protein. Hou et al. compared the characteristics of the new variant against the ancestral form in a series of experiments in human cells and animal models. The variant is better at infecting upper-airway epithelial cells and replicates in greater numbers than the ancestral virus. Evidence indicates modest, if any, significant changes to virulence in animal models. Therefore, the virus appears to have evolved for greater transmissibility in humans rather than for greater pathogenicity. The mutation renders the new virus variant more susceptible to neutralizing antisera without altering the efficacy of vaccine candidates currently under development. Science , this issue p. 1464 The current dominant structural variant of SARS-CoV-2 appears to have evolved from the ancestral form and enhances transmissibility. The spike aspartic acid–614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but its effects on viral pathogenesis and transmissibility remain unclear. We engineered a SARS-CoV-2 variant containing this substitution. The variant exhibits more efficient infection, replication, and competitive fitness in primary human airway epithelial cells but maintains similar morphology and in vitro neutralization properties, compared with the ancestral wild-type virus. Infection of human angiotensin-converting enzyme 2 (ACE2) transgenic mice and Syrian hamsters with both viruses resulted in similar viral titers in respiratory tissues and pulmonary disease. However, the D614G variant transmits significantly faster and displayed increased competitive fitness than the wild-type virus in hamsters. These data show that the D614G substitution enhances SARS-CoV-2 infectivity, competitive fitness, and transmission in primary human cells and animal models.
Author Markmann, Alena J.
Ehre, Camille
Nakajima, Noriko
Graham, Rachel
Bartelt, Luther
Tse, Longping V.
Takahashi, Kenta
Schäfer, Alexandra
Halfmann, Peter
de Silva, Aravinda
Okuda, Kenichi
Margolis, David M.
Boucher, Richard C.
Kuroda, Makoto
Suzuki, Tadaki
Hou, Yixuan J.
Dinnon, Kenneth H.
Randell, Scott H.
Mascenik, Teresa M.
Kawaoka, Yoshihiro
Baric, Ralph S.
Lee, Rhianna E.
Leist, Sarah R.
Edwards, Caitlin E.
Gralinski, Lisa E.
Chiba, Shiho
Author_xml – sequence: 1
  givenname: Yixuan J.
  orcidid: 0000-0002-8323-7243
  surname: Hou
  fullname: Hou, Yixuan J.
  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
– sequence: 2
  givenname: Shiho
  orcidid: 0000-0003-0415-6013
  surname: Chiba
  fullname: Chiba, Shiho
  organization: Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI, USA
– sequence: 3
  givenname: Peter
  orcidid: 0000-0002-1648-1625
  surname: Halfmann
  fullname: Halfmann, Peter
  organization: Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI, USA
– sequence: 4
  givenname: Camille
  orcidid: 0000-0002-0046-0096
  surname: Ehre
  fullname: Ehre, Camille
  organization: Marsico Lung Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
– sequence: 5
  givenname: Makoto
  surname: Kuroda
  fullname: Kuroda, Makoto
  organization: Influenza Research Institute, Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI, USA
– sequence: 6
  givenname: Kenneth H.
  orcidid: 0000-0002-8942-1551
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  fullname: Dinnon, Kenneth H.
  organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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  givenname: Sarah R.
  orcidid: 0000-0002-4989-5381
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  surname: Schäfer
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  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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  givenname: Noriko
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  surname: Nakajima
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– sequence: 10
  givenname: Kenta
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  fullname: Takahashi, Kenta
  organization: Department of Pathology, National Institute of Infectious Diseases, Tokyo, Japan
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  givenname: Rhianna E.
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  surname: Lee
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  surname: Graham
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  surname: Edwards
  fullname: Edwards, Caitlin E.
  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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  givenname: Longping V.
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  surname: Tse
  fullname: Tse, Longping V.
  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
– sequence: 16
  givenname: Kenichi
  orcidid: 0000-0001-9341-2730
  surname: Okuda
  fullname: Okuda, Kenichi
  organization: Marsico Lung Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
– sequence: 17
  givenname: Alena J.
  orcidid: 0000-0003-3656-9322
  surname: Markmann
  fullname: Markmann, Alena J.
  organization: Department of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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  surname: Bartelt
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  surname: Randell
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  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA., Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33184236$$D View this record in MEDLINE/PubMed
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These authors contributed equally to this work.
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Snippet Pandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The ancestral form of...
The spike aspartic acid-614 to glycine (D614G) substitution is prevalent in global severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains, but...
Changing with the timesPandemic spread of a virus in naïe populations can select for mutations that alter pathogenesis, virulence, and/or transmissibility. The...
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StartPage 1464
SubjectTerms ACE2
Amino Acid Substitution
Angiotensin-converting enzyme 2
Angiotensin-Converting Enzyme 2 - genetics
Animal models
Animals
Asparagine - genetics
Aspartic acid
Coronaviridae
Coronaviruses
COVID-19
COVID-19 - transmission
COVID-19 - virology
Cricetinae
Disease transmission
Fitness
Genetic Fitness - genetics
Glycine
Glycine - genetics
Hamsters
Humans
Mesocricetus
Mice
Mice, Transgenic
Microbio
Morphology
Mutation
Neutralization
Pandemics
Pathogenesis
Pathogens
Replication
Respiratory diseases
Respiratory Mucosa - virology
Rodents
SARS-CoV-2 - genetics
SARS-CoV-2 - pathogenicity
Severe acute respiratory syndrome coronavirus 2
Substitutes
Viral diseases
Virulence
Virulence - genetics
Virus Replication - genetics
Viruses
Title SARS-CoV-2 D614G variant exhibits efficient replication ex vivo and transmission in vivo
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