Antigenic variation of SARS‐CoV‐2 in response to immune pressure

Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS‐CoV‐2 must have been subject to the selective pressure imposed by the human immune system....

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Published inMolecular ecology Vol. 30; no. 14; pp. 3548 - 3559
Main Authors Forni, Diego, Cagliani, Rachele, Pontremoli, Chiara, Mozzi, Alessandra, Pozzoli, Uberto, Clerici, Mario, Sironi, Manuela
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.07.2021
John Wiley and Sons Inc
Subjects
antigenic variation
Antigens
B cell epitope
B-lymphocytes
CD4 antigen
CD8 antigen
Chiroptera
Common cold
Conservation
Coronaviridae
Coronaviruses
COVID-19
disease severity
ecology
Epitopes
genome
Genomes
Glycoproteins
human coronavirus
Human populations
humans
humoral immunity
Immune response
Immune response (humoral)
Immune system
Immunogenicity
Lymphocytes
Lymphocytes T
nucleocapsid proteins
Nucleocapsids
Original
Proteins
sarbecovirus
SARS‐CoV‐2
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Spike glycoprotein
T cell epitope
Viral diseases
Viruses
B cell epitope
human coronavirus
T cell epitope
COVID‐19
SARS‐CoV‐2
sarbecovirus
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Abstract Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS‐CoV‐2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high‐quality SARS‐CoV‐2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS‐CoV‐2 population, epitopes for CD4+ and CD8+ T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS‐CoV‐2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
AbstractList Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS‐CoV‐2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high‐quality SARS‐CoV‐2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS‐CoV‐2 population, epitopes for CD4+ and CD8+ T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS‐CoV‐2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS‐CoV‐2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high‐quality SARS‐CoV‐2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS‐CoV‐2 population, epitopes for CD4 + and CD8 + T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS‐CoV‐2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
Analysis of the bat viruses most closely related to SARS-CoV-2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS-CoV-2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high-quality SARS-CoV-2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS-CoV-2 population, epitopes for CD4 and CD8 T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS-CoV-2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
Analysis of the bat viruses most closely related to SARS-CoV-2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS-CoV-2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high-quality SARS-CoV-2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS-CoV-2 population, epitopes for CD4+ and CD8+ T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS-CoV-2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.Analysis of the bat viruses most closely related to SARS-CoV-2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS-CoV-2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high-quality SARS-CoV-2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS-CoV-2 population, epitopes for CD4+ and CD8+ T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS-CoV-2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless, since its introduction in human populations, SARS‐CoV‐2 must have been subject to the selective pressure imposed by the human immune system. We exploited the availability of a large number of high‐quality SARS‐CoV‐2 genomes, as well as of validated epitope predictions, to show that B cell epitopes in the spike glycoprotein (S) and in the nucleocapsid protein (N) have higher diversity than nonepitope positions. Similar results were obtained for other human coronaviruses and for sarbecoviruses sampled in bats. Conversely, in the SARS‐CoV‐2 population, epitopes for CD4⁺ and CD8⁺ T cells were not more variable than nonepitope positions. A significant reduction in epitope variability was instead observed for some of the most immunogenic proteins (S, N, ORF8 and ORF3a). Analysis over longer evolutionary time frames indicated that this effect is not due to differential constraints. These data indicate that SARS‐CoV‐2 evolves to elude the host humoral immune response, whereas recognition by T cells is not actively avoided by the virus. However, we also found a trend of lower diversity of T cell epitopes for common cold coronaviruses, indicating that epitope conservation per se is not directly linked to disease severity. We suggest that conservation serves to maintain epitopes that elicit tolerizing T cell responses or induce T cells with regulatory activity.
Author Forni, Diego
Pozzoli, Uberto
Mozzi, Alessandra
Cagliani, Rachele
Pontremoli, Chiara
Clerici, Mario
Sironi, Manuela
AuthorAffiliation 1 Scientific Institute IRCCS E. MEDEA Bioinformatics Bosisio Parini Italy
2 Department of Physiopathology and Transplantation University of Milan Milan Italy
3 Don C. Gnocchi Foundation ONLUS IRCCS Milan Italy
AuthorAffiliation_xml – name: 1 Scientific Institute IRCCS E. MEDEA Bioinformatics Bosisio Parini Italy
– name: 3 Don C. Gnocchi Foundation ONLUS IRCCS Milan Italy
– name: 2 Department of Physiopathology and Transplantation University of Milan Milan Italy
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  organization: Bioinformatics
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33289207$$D View this record in MEDLINE/PubMed
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Issue 14
Keywords B cell epitope
human coronavirus
T cell epitope
COVID‐19
SARS‐CoV‐2
sarbecovirus
Language English
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This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Funding information: This work was supported by the Italian Ministry of Health (“Ricerca Corrente 2019–2020” to M.S., “Ricerca Corrente 2018–2020” to D.F.).
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Snippet Analysis of the bat viruses most closely related to SARS‐CoV‐2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless,...
Analysis of the bat viruses most closely related to SARS-CoV-2 indicated that the virus probably required limited adaptation to spread in humans. Nonetheless,...
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SubjectTerms antigenic variation
Antigens
B cell epitope
B-lymphocytes
CD4 antigen
CD8 antigen
Chiroptera
Common cold
Conservation
Coronaviridae
Coronaviruses
COVID-19
disease severity
ecology
Epitopes
genome
Genomes
Glycoproteins
human coronavirus
Human populations
humans
humoral immunity
Immune response
Immune response (humoral)
Immune system
Immunogenicity
Lymphocytes
Lymphocytes T
nucleocapsid proteins
Nucleocapsids
Original
Proteins
sarbecovirus
SARS‐CoV‐2
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Spike glycoprotein
T cell epitope
Viral diseases
Viruses
Title Antigenic variation of SARS‐CoV‐2 in response to immune pressure
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmec.15730
https://www.ncbi.nlm.nih.gov/pubmed/33289207
https://www.proquest.com/docview/2554226999
https://www.proquest.com/docview/2468333423
https://www.proquest.com/docview/2636419814
https://pubmed.ncbi.nlm.nih.gov/PMC7753431
Volume 30
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