An interferon-stimulated long non-coding RNA USP30-AS1 as an immune modulator in influenza A virus infection

Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-r...

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Published inPLoS pathogens Vol. 21; no. 1; p. e1012854
Main Authors Cao, Yi, Chin, Alex W. H., Gu, Haogao, Li, Mengting, Gu, Yuner, Lau, Sylvia P. N., Hui, Kenrie P. Y., Chan, Michael C. W., Poon, Leo L. M.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 08.01.2025
Public Library of Science (PLoS)
Subjects
Animals
Biological response modifiers
Biology and life sciences
Control systems
Gene expression
Genes
Genetic aspects
Health aspects
Humans
Immune response
Immune system
Immunity, Innate
Immunotherapy
Influenza
Influenza A virus - immunology
Influenza, Human - genetics
Influenza, Human - immunology
Influenza, Human - virology
Interferon
Interferons - immunology
Medical research
Medicine and health sciences
Medicine, Experimental
Mice
Mice, Inbred C57BL
Orthomyxoviridae Infections - genetics
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - virology
Physiological aspects
Protein biosynthesis
Research and Analysis Methods
RNA
RNA, Long Noncoding - genetics
RNA, Long Noncoding - immunology
Signal Transduction
Viral proteins
China
Puerto Rico
California
Online AccessGet full text
ISSN1553-7374
1553-7366
1553-7374
DOI10.1371/journal.ppat.1012854

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Abstract Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30 . In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation.
AbstractList Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30. In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation.Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30. In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation.
Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30. In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation.
Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30 . In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation. Influenza A virus (IAV) infection can induce differential expression of long non-coding RNAs (lncRNAs). However, the understanding of IAV induced lncRNAs that involve in host immune responses is limited. Here we identified that lncRNA USP30-AS1 was induced by multiple subtypes of IAV infection, serving as a critical regulator regarding IAV induced immune responses. Deletion of USP30-AS1 led to enhanced viral protein synthesis and elevated viral growth in IAV infection. JAK-STAT signaling activation can drive the transcription of USP30-AS1 . USP30-AS1 does not exert function through the nearby partner protein-coding gene USP30 . Deficiency of USP30-AS1 triggers unbalanced, elevated pro-inflammatory responses in IAV infected cells, indicating the role of USP30-AS1 as a modulator regarding immune response during IAV infection. We also provide a user-friendly database that allows access to well-annotated host gene expression profiles in influenza virus infection or interferon stimulation.
Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection. However, how lncRNAs engage immune responses during influenza A virus (IAV) infection remains unclear. Here, we show that lncRNA USP30-AS1 is up-regulated by infection of multiple different IAV subtypes and is required for tuning inflammatory and antiviral response in IAV infection. Genetically inactivation of USP30-AS1 enhances viral protein synthesis and viral growth. USP30-AS1 is an interferon-stimulated gene, and the induction of USP30-AS1 can be achieved by JAK-STAT mediated signaling activation. The immune regulation of USP30-AS1 is independent of its proximal protein-coding gene USP30 . In IAV infection, deletion of USP30-AS1 unleashes high systemic inflammatory responses involving a broad range of pro-inflammatory factors, suggesting USP30-AS1 as a critical modulator of immune responses in IAV infection. Furthermore, we established a database providing well-annotated host gene expression profiles IAV infection or immune stimulation.
Audience Academic
Author Gu, Yuner
Hui, Kenrie P. Y.
Chan, Michael C. W.
Gu, Haogao
Poon, Leo L. M.
Cao, Yi
Chin, Alex W. H.
Li, Mengting
Lau, Sylvia P. N.
AuthorAffiliation 3 HKU-Pasteur Research Pole, The University of Hong Kong, Hong Kong SAR, China
2 Centre for Immunology & Infection, Hong Kong Science Park, Hong Kong SAR, China
University of Georgia, UNITED STATES OF AMERICA
1 School of Public Health, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China
4 HKJC Global Health Institute, The University of Hong Kong, Hong Kong SAR, China
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Snippet Long non-coding RNAs (lncRNAs) are essential components of innate immunity, maintaining the functionality of immune systems that control virus infection....
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StartPage e1012854
SubjectTerms Animals
Biological response modifiers
Biology and life sciences
Control systems
Gene expression
Genes
Genetic aspects
Health aspects
Humans
Immune response
Immune system
Immunity, Innate
Immunotherapy
Influenza
Influenza A virus - immunology
Influenza, Human - genetics
Influenza, Human - immunology
Influenza, Human - virology
Interferon
Interferons - immunology
Medical research
Medicine and health sciences
Medicine, Experimental
Mice
Mice, Inbred C57BL
Orthomyxoviridae Infections - genetics
Orthomyxoviridae Infections - immunology
Orthomyxoviridae Infections - virology
Physiological aspects
Protein biosynthesis
Research and Analysis Methods
RNA
RNA, Long Noncoding - genetics
RNA, Long Noncoding - immunology
Signal Transduction
Viral proteins
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Title An interferon-stimulated long non-coding RNA USP30-AS1 as an immune modulator in influenza A virus infection
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