Interferon Regulatory Factors IRF1 and IRF7 Directly Regulate Gene Expression in Bats in Response to Viral Infection

Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show Interferon Regulatory Factor 1 (IRF1), 3, and 7 levels are elevated in most bat tissues and that, basally, IRFs contribute to the expression of type...

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Published inCell reports (Cambridge) Vol. 33; no. 5; p. 108345
Main Authors Irving, Aaron T., Zhang, Qian, Kong, Pui-San, Luko, Katarina, Rozario, Pritisha, Wen, Ming, Zhu, Feng, Zhou, Peng, Ng, Justin H.J., Sobota, Radoslaw M., Wang, Lin-Fa
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Published United States Elsevier Inc 03.11.2020
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Abstract Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show Interferon Regulatory Factor 1 (IRF1), 3, and 7 levels are elevated in most bat tissues and that, basally, IRFs contribute to the expression of type I IFN ligands and high expression of interferon regulated genes (IRGs). CRISPR knockout (KO) of IRF 1/3/7 in cells reveals distinct subsets of genes affected by each IRF in an IFN-ligand signaling-dependent and largely independent manner. As the master regulators of innate immunity, the IRFs control the kinetics and maintenance of the IRG response and play essential roles in response to influenza A virus (IAV), herpes simplex virus 1 (HSV-1), Melaka virus/Pteropine orthoreovirus 3 Melaka (PRV3M), and Middle East respiratory syndrome-related coronavirus (MERS-CoV) infection. With its differential expression in bats compared to that in humans, this highlights a critical role for basal IRF expression in viral responses and potentially immune cell development in bats with relevance for IRF function in human biology. [Display omitted] •IRF1, 3, and 7 are highly expressed in multiple bat tissues and control gene expression•Antiviral IRG expression in bat cells is largely IFN independent•IRF1 and 7 regulate distinct subsets and alter the kinetics/maintenance of IRGs•IRF1, 3, and 7 regulate antiviral responses to IAV/MERS/HSV-1/PRV3M in bat cells Bats express high levels of antiviral genes in response to synthetic dsRNA, IFN, or virus by the transcription factors IRF1/3/7. Irving et al. show that this induction largely bypasses IFNα/β production and that this may be a method for limiting the inflammation induced by IFN signaling while still restricting virus infection.
AbstractList Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show Interferon Regulatory Factor 1 (IRF1), 3, and 7 levels are elevated in most bat tissues and that, basally, IRFs contribute to the expression of type I IFN ligands and high expression of interferon regulated genes (IRGs). CRISPR knockout (KO) of IRF 1/3/7 in cells reveals distinct subsets of genes affected by each IRF in an IFN-ligand signaling-dependent and largely independent manner. As the master regulators of innate immunity, the IRFs control the kinetics and maintenance of the IRG response and play essential roles in response to influenza A virus (IAV), herpes simplex virus 1 (HSV-1), Melaka virus/Pteropine orthoreovirus 3 Melaka (PRV3M), and Middle East respiratory syndrome-related coronavirus (MERS-CoV) infection. With its differential expression in bats compared to that in humans, this highlights a critical role for basal IRF expression in viral responses and potentially immune cell development in bats with relevance for IRF function in human biology. Bats express high levels of antiviral genes in response to synthetic dsRNA, IFN, or virus by the transcription factors IRF1/3/7. Irving et al. show that this induction largely bypasses IFNα/β production and that this may be a method for limiting the inflammation induced by IFN signaling while still restricting virus infection.
Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show Interferon Regulatory Factor 1 (IRF1), 3, and 7 levels are elevated in most bat tissues and that, basally, IRFs contribute to the expression of type I IFN ligands and high expression of interferon regulated genes (IRGs). CRISPR knockout (KO) of IRF 1/3/7 in cells reveals distinct subsets of genes affected by each IRF in an IFN-ligand signaling-dependent and largely independent manner. As the master regulators of innate immunity, the IRFs control the kinetics and maintenance of the IRG response and play essential roles in response to influenza A virus (IAV), herpes simplex virus 1 (HSV-1), Melaka virus/Pteropine orthoreovirus 3 Melaka (PRV3M), and Middle East respiratory syndrome-related coronavirus (MERS-CoV) infection. With its differential expression in bats compared to that in humans, this highlights a critical role for basal IRF expression in viral responses and potentially immune cell development in bats with relevance for IRF function in human biology. [Display omitted] •IRF1, 3, and 7 are highly expressed in multiple bat tissues and control gene expression•Antiviral IRG expression in bat cells is largely IFN independent•IRF1 and 7 regulate distinct subsets and alter the kinetics/maintenance of IRGs•IRF1, 3, and 7 regulate antiviral responses to IAV/MERS/HSV-1/PRV3M in bat cells Bats express high levels of antiviral genes in response to synthetic dsRNA, IFN, or virus by the transcription factors IRF1/3/7. Irving et al. show that this induction largely bypasses IFNα/β production and that this may be a method for limiting the inflammation induced by IFN signaling while still restricting virus infection.
Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show Interferon Regulatory Factor 1 (IRF1), 3, and 7 levels are elevated in most bat tissues and that, basally, IRFs contribute to the expression of type I IFN ligands and high expression of interferon regulated genes (IRGs). CRISPR knockout (KO) of IRF 1/3/7 in cells reveals distinct subsets of genes affected by each IRF in an IFN-ligand signaling-dependent and largely independent manner. As the master regulators of innate immunity, the IRFs control the kinetics and maintenance of the IRG response and play essential roles in response to influenza A virus (IAV), herpes simplex virus 1 (HSV-1), Melaka virus/Pteropine orthoreovirus 3 Melaka (PRV3M), and Middle East respiratory syndrome-related coronavirus (MERS-CoV) infection. With its differential expression in bats compared to that in humans, this highlights a critical role for basal IRF expression in viral responses and potentially immune cell development in bats with relevance for IRF function in human biology.
ArticleNumber 108345
Author Sobota, Radoslaw M.
Ng, Justin H.J.
Zhu, Feng
Zhang, Qian
Wen, Ming
Kong, Pui-San
Rozario, Pritisha
Luko, Katarina
Wang, Lin-Fa
Irving, Aaron T.
Zhou, Peng
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  orcidid: 0000-0002-0196-1570
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  organization: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore
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  surname: Zhang
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  surname: Kong
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  organization: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore
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  surname: Zhu
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  organization: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore
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  surname: Zhou
  fullname: Zhou, Peng
  organization: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore
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  surname: Ng
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  organization: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33147460$$D View this record in MEDLINE/PubMed
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Issue 5
Keywords Interferon Regulatory Factor
PRV3M
bat
innate immunity
IRF
interferon
MERS
virus
IAV
IRG
Language English
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Snippet Bat cells and tissue have elevated basal expression levels of antiviral genes commonly associated with interferon alpha (IFNα) signaling. Here, we show...
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StartPage 108345
SubjectTerms Animals
bat
Chiroptera - immunology
Gene Expression Regulation - immunology
Herpesvirus 1, Human - immunology
IAV
Influenza A virus - immunology
innate immunity
interferon
Interferon Regulatory Factor
Interferon Regulatory Factor-1 - immunology
Interferon Regulatory Factor-7 - immunology
IRF
IRG
MERS
Middle East Respiratory Syndrome Coronavirus - immunology
Orthoreovirus - immunology
PRV3M
virus
Virus Diseases - immunology
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Title Interferon Regulatory Factors IRF1 and IRF7 Directly Regulate Gene Expression in Bats in Response to Viral Infection
URI https://dx.doi.org/10.1016/j.celrep.2020.108345
https://www.ncbi.nlm.nih.gov/pubmed/33147460
https://pubmed.ncbi.nlm.nih.gov/PMC8755441
https://doaj.org/article/1a481bd494ec45cba71a7d42d304574a
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