The Long Non-Coding Antisense RNA JHDM1D-AS1 Regulates Inflammatory Responses in Human Monocytes

Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune respon...

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Vydáno v:	Frontiers in cellular and infection microbiology Ročník 12; s. 934313
Hlavní autoři:	Malmström, Erik, Khan, Hina N., Veer, Cornelis van ‘t, Stunnenberg, Melissa, Meijer, Mariska T., Matsumoto, Hisatake, Otto, Natasja A., Geijtenbeek, Teunis B. H., de Vos, Alex F., Poll, Tom van der, Scicluna, Brendon P.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	Switzerland Frontiers Media SA 12.07.2022 Frontiers Media S.A
Témata:	Antisense RNA Basic Medicine Cell and Molecular Biology Cell- och molekylärbiologi Cells Cellular and Infection Microbiology Cytokines Down-regulation Enzymes Gene expression Humans Immune response Immunoregulation Inflammation Innate immunity Lipopolysaccharides Lipopolysaccharides - metabolism long non-coding RNA Macrophages Macrophages - metabolism Medical and Health Sciences Medical research Medicin och hälsovetenskap Medicinska och farmaceutiska grundvetenskaper MicroRNAs monocyte Monocytes Non-coding RNA Pathogens RNA, Antisense - metabolism RNA, Long Noncoding - metabolism Sepsis Toll-like receptors Tumor necrosis factor-TNF Amarillo Texas United Kingdom > UK United States > US Germany monocyte long non-coding RNA toll-like receptors inflammation sepsis
ISSN:	2235-2988, 2235-2988
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Abstract	Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. JHDM1D-AS1 expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of JHDM1D-AS1 expression in monocytes depended, at least in part, on nuclear factor–κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., CXCL2 , CXCL8 , IL1RN , TREM1 , TNF , and IL6 ), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., SOCS1 and IL10RA ). JHDM1D-AS1 overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify JHDM1D-AS1 as a potential anti-inflammatory mediator induced in response to inflammatory stimuli.
AbstractList	Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. JHDM1D-AS1 expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of JHDM1D-AS1 expression in monocytes depended, at least in part, on nuclear factor–κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., CXCL2, CXCL8, IL1RN, TREM1, TNF, and IL6), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., SOCS1 and IL10RA). JHDM1D-AS1 overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify JHDM1D-AS1 as a potential anti-inflammatory mediator induced in response to inflammatory stimuli. Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. JHDM1D-AS1 expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of JHDM1D-AS1 expression in monocytes depended, at least in part, on nuclear factor–κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., CXCL2 , CXCL8 , IL1RN , TREM1 , TNF , and IL6 ), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., SOCS1 and IL10RA ). JHDM1D-AS1 overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify JHDM1D-AS1 as a potential anti-inflammatory mediator induced in response to inflammatory stimuli. Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of expression in monocytes depended, at least in part, on nuclear factor-κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., , , , , , and ), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., and ). overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify as a potential anti-inflammatory mediator induced in response to inflammatory stimuli. Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. JHDM1D-AS1 expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of JHDM1D-AS1 expression in monocytes depended, at least in part, on nuclear factor-κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., CXCL2, CXCL8, IL1RN, TREM1, TNF, and IL6), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., SOCS1 and IL10RA). JHDM1D-AS1 overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify JHDM1D-AS1 as a potential anti-inflammatory mediator induced in response to inflammatory stimuli.Monocytes are key players in innate immunity, with their ability to regulate inflammatory responses and combat invading pathogens. There is a growing body of evidence indicating that long non-coding RNA (lncRNA) participate in various cellular biological processes, including the innate immune response. The immunoregulatory properties of numerous lncRNAs discovered in monocytes remain largely unexplored. Here, by RNA sequencing, we identified a lncRNA JHDM1D-AS1, which was upregulated in blood monocytes obtained from patients with sepsis relative to healthy controls. JHDM1D-AS1 expression was induced in primary human monocytes exposed to Toll-like receptor ligands, such as lipopolysaccharide (LPS), or bacteria. The inducibility of JHDM1D-AS1 expression in monocytes depended, at least in part, on nuclear factor-κB activation. JHDM1D-AS1 knockdown experiments in human monocyte-derived macrophages revealed significantly enhanced expression of inflammatory mediators, before and after exposure to LPS, relative to control cells. Specifically, genes involved in inflammatory responses were upregulated (e.g., CXCL2, CXCL8, IL1RN, TREM1, TNF, and IL6), whereas genes involved in anti-inflammatory pathways were downregulated (e.g., SOCS1 and IL10RA). JHDM1D-AS1 overexpression in a pro-monocytic cell line revealed diminished pro-inflammatory responses subsequent to LPS challenge. Collectively, these findings identify JHDM1D-AS1 as a potential anti-inflammatory mediator induced in response to inflammatory stimuli.
Author	de Vos, Alex F. Meijer, Mariska T. Malmström, Erik Matsumoto, Hisatake Otto, Natasja A. Geijtenbeek, Teunis B. H. Stunnenberg, Melissa Khan, Hina N. Scicluna, Brendon P. Poll, Tom van der Veer, Cornelis van ‘t
AuthorAffiliation	9 Centre for Molecular Medicine and Biobanking, University of Malta , Msida , Malta 6 Amsterdam University Medical Centers, Experimental Immunology, University of Amsterdam , Amsterdam , Netherlands 2 Division of Infection Medicine, Department of Clinical Sciences, Lund University , Lund , Sweden 1 Amsterdam University Medical Centers, Center for Experimental and Molecular Medicine, University of Amsterdam , Amsterdam , Netherlands 7 Amsterdam University Medical Centers, Division of Infectious Diseases, University of Amsterdam and Vrije Universiteit Amsterdam , Amsterdam , Netherlands 3 Emergency Medicine, Department of Clinical Sciences Lund, Lund University, Skane University Hospital , Lund , Sweden 4 Amsterdam University Medical Centers, Clinical Epidemiology and Data Science, University of Amsterdam , Amsterdam , Netherlands 5 Amsterdam Institute for Infection and Immunity , Amsterdam , Netherlands 8 Department of Applied Biomedical Science, Faculty of Health Sciences, Mater Dei hospital,
AuthorAffiliation_xml	– name: 5 Amsterdam Institute for Infection and Immunity , Amsterdam , Netherlands – name: 7 Amsterdam University Medical Centers, Division of Infectious Diseases, University of Amsterdam and Vrije Universiteit Amsterdam , Amsterdam , Netherlands – name: 4 Amsterdam University Medical Centers, Clinical Epidemiology and Data Science, University of Amsterdam , Amsterdam , Netherlands – name: 9 Centre for Molecular Medicine and Biobanking, University of Malta , Msida , Malta – name: 1 Amsterdam University Medical Centers, Center for Experimental and Molecular Medicine, University of Amsterdam , Amsterdam , Netherlands – name: 8 Department of Applied Biomedical Science, Faculty of Health Sciences, Mater Dei hospital, University of Malta , Msida , Malta – name: 2 Division of Infection Medicine, Department of Clinical Sciences, Lund University , Lund , Sweden – name: 3 Emergency Medicine, Department of Clinical Sciences Lund, Lund University, Skane University Hospital , Lund , Sweden – name: 6 Amsterdam University Medical Centers, Experimental Immunology, University of Amsterdam , Amsterdam , Netherlands
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/35903199$$D View this record in MEDLINE/PubMed
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Copyright	Copyright © 2022 Malmström, Khan, Veer, Stunnenberg, Meijer, Matsumoto, Otto, Geijtenbeek, de Vos, Poll and Scicluna. 2022. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2022 Malmström, Khan, Veer, Stunnenberg, Meijer, Matsumoto, Otto, Geijtenbeek, de Vos, Poll and Scicluna 2022 Malmström, Khan, Veer, Stunnenberg, Meijer, Matsumoto, Otto, Geijtenbeek, de Vos, Poll and Scicluna
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Keywords	monocyte long non-coding RNA toll-like receptors inflammation sepsis
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SubjectTerms	Antisense RNA Basic Medicine Cell and Molecular Biology Cell- och molekylärbiologi Cells Cellular and Infection Microbiology Cytokines Down-regulation Enzymes Gene expression Humans Immune response Immunoregulation Inflammation Innate immunity Lipopolysaccharides Lipopolysaccharides - metabolism long non-coding RNA Macrophages Macrophages - metabolism Medical and Health Sciences Medical research Medicin och hälsovetenskap Medicinska och farmaceutiska grundvetenskaper MicroRNAs monocyte Monocytes Non-coding RNA Pathogens RNA, Antisense - metabolism RNA, Long Noncoding - metabolism Sepsis Toll-like receptors Tumor necrosis factor-TNF
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Title	The Long Non-Coding Antisense RNA JHDM1D-AS1 Regulates Inflammatory Responses in Human Monocytes
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