In vivo antiviral host transcriptional response to SARS-CoV-2 by viral load, sex, and age
Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across i...
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| Vydané v: | PLoS biology Ročník 18; číslo 9; s. e3000849 |
|---|---|
| Hlavní autori: | , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
United States
Public Library of Science
08.09.2020
Public Library of Science (PLoS) |
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| ISSN: | 1545-7885, 1544-9173, 1545-7885 |
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| Abstract | Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell-specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell-specific and NK cell-specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-κB) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity. |
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| AbstractList | Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell-specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell-specific and NK cell-specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-κB) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity. Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell-specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell-specific and NK cell-specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-κB) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity.Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell-specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell-specific and NK cell-specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-κB) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity. Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell-specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell-specific and NK cell-specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-[kappa]B) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity. Despite limited genomic diversity, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown a wide range of clinical manifestations in different patient populations. The mechanisms behind these host differences are still unclear. Here, we examined host response gene expression across infection status, viral load, age, and sex among shotgun RNA sequencing profiles of nasopharyngeal (NP) swabs from 430 individuals with PCR-confirmed SARS-CoV-2 and 54 negative controls. SARS-CoV-2 induced a strong antiviral response with up-regulation of antiviral factors such as OAS1-3 and IFIT1-3 and T helper type 1 (Th1) chemokines CXCL9/10/11, as well as a reduction in transcription of ribosomal proteins. SARS-CoV-2 culture in human airway epithelial (HAE) cultures replicated the in vivo antiviral host response 7 days post infection, with no induction of interferon-stimulated genes after 3 days. Patient-matched longitudinal specimens (mean elapsed time = 6.3 days) demonstrated reduction in interferon-induced transcription, recovery of transcription of ribosomal proteins, and initiation of wound healing and humoral immune responses. Expression of interferon-responsive genes, including ACE2, increased as a function of viral load, while transcripts for B cell–specific proteins and neutrophil chemokines were elevated in patients with lower viral load. Older individuals had reduced expression of the Th1 chemokines CXCL9/10/11 and their cognate receptor CXCR3, as well as CD8A and granzyme B, suggesting deficiencies in trafficking and/or function of cytotoxic T cells and natural killer (NK) cells. Relative to females, males had reduced B cell–specific and NK cell–specific transcripts and an increase in inhibitors of nuclear factor kappa-B (NF-κB) signaling, possibly inappropriately throttling antiviral responses. Collectively, our data demonstrate that host responses to SARS-CoV-2 are dependent on viral load and infection time course, with observed differences due to age and sex that may contribute to disease severity. Despite limited genomic diversity, SARS-CoV-2 has shown a wide range of clinical manifestations in different patient populations; the mechanisms behind these host differences are still unclear. This study reveals that SARS-CoV-2 infection induces inflammation by activation of interferon signaling, with differences in host response observed due to sex and age. |
| Audience | Academic |
| Author | Greninger, Alexander L. Cajimat, Maria N. Huang, Meei-Li Roychoudhury, Pavitra Bovier, Francesca Shrestha, Lasata Mears, Megan C. Lieberman, Nicole A. P. Shi, Pei-Yong Porotto, Matteo Xie, Hong Peddu, Vikas Jerome, Keith R. Moscona, Anne Bente, Dennis A. |
| AuthorAffiliation | 1 Department of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, Washington, United States of America 3 Department of Experimental Pathology, University of Texas Medical Branch, Galveston, Texas, United States of America 10 Department of Physiology & Cellular Biophysics, Columbia University Medical Center, New York, New York, United States of America 6 Center for Host–Pathogen Interaction, Columbia University Medical Center, New York, New York, United States of America 4 Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, United States of America 5 Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, United States of America 9 Department of Microbiology & Immunology, Columbia University Medical Center, New York, New York, United States of America New York University School of Medicine, UNITED STATES 11 Department of Experimental Medicine, University of Campani |
| AuthorAffiliation_xml | – name: 2 Galveston National Laboratory, University of Texas Medical Branch, Galveston, Texas, United States of America – name: 11 Department of Experimental Medicine, University of Campania “Luigi Vanvitelli,” Caserta, Italy – name: New York University School of Medicine, UNITED STATES – name: 4 Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, United States of America – name: 5 Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, United States of America – name: 8 Department of Pediatrics, Columbia University Medical Center, New York, New York, United States of America – name: 10 Department of Physiology & Cellular Biophysics, Columbia University Medical Center, New York, New York, United States of America – name: 1 Department of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, Washington, United States of America – name: 7 Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America – name: 6 Center for Host–Pathogen Interaction, Columbia University Medical Center, New York, New York, United States of America – name: 9 Department of Microbiology & Immunology, Columbia University Medical Center, New York, New York, United States of America – name: 3 Department of Experimental Pathology, University of Texas Medical Branch, Galveston, Texas, United States of America |
| Author_xml | – sequence: 1 givenname: Nicole A. P. orcidid: 0000-0001-9334-8150 surname: Lieberman fullname: Lieberman, Nicole A. P. – sequence: 2 givenname: Vikas orcidid: 0000-0002-0366-3956 surname: Peddu fullname: Peddu, Vikas – sequence: 3 givenname: Hong surname: Xie fullname: Xie, Hong – sequence: 4 givenname: Lasata orcidid: 0000-0002-9760-7348 surname: Shrestha fullname: Shrestha, Lasata – sequence: 5 givenname: Meei-Li surname: Huang fullname: Huang, Meei-Li – sequence: 6 givenname: Megan C. orcidid: 0000-0003-1293-7696 surname: Mears fullname: Mears, Megan C. – sequence: 7 givenname: Maria N. surname: Cajimat fullname: Cajimat, Maria N. – sequence: 8 givenname: Dennis A. orcidid: 0000-0002-5150-7368 surname: Bente fullname: Bente, Dennis A. – sequence: 9 givenname: Pei-Yong surname: Shi fullname: Shi, Pei-Yong – sequence: 10 givenname: Francesca surname: Bovier fullname: Bovier, Francesca – sequence: 11 givenname: Pavitra orcidid: 0000-0002-4567-8232 surname: Roychoudhury fullname: Roychoudhury, Pavitra – sequence: 12 givenname: Keith R. surname: Jerome fullname: Jerome, Keith R. – sequence: 13 givenname: Anne surname: Moscona fullname: Moscona, Anne – sequence: 14 givenname: Matteo surname: Porotto fullname: Porotto, Matteo – sequence: 15 givenname: Alexander L. orcidid: 0000-0002-7443-0527 surname: Greninger fullname: Greninger, Alexander L. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32898168$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2020 Public Library of Science 2020 Lieberman 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. 2020 Lieberman et al 2020 Lieberman et al |
| Copyright_xml | – notice: COPYRIGHT 2020 Public Library of Science – notice: 2020 Lieberman 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: 2020 Lieberman et al 2020 Lieberman et al |
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| DOI | 10.1371/journal.pbio.3000849 |
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| Title | In vivo antiviral host transcriptional response to SARS-CoV-2 by viral load, sex, and age |
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