Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease

Lupus-like disease is driven by NETs enriched in mitochondrial DNA. Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are generated and their roles in sterile inflammation remain unclear. Ribonucleoprotein immune complexes (RNP ICs), inducers of NETosis, require mito...

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Published in	Nature medicine Vol. 22; no. 2; pp. 146 - 153
Main Authors	Lood, Christian, Blanco, Luz P, Purmalek, Monica M, Carmona-Rivera, Carmelo, De Ravin, Suk S, Smith, Carolyne K, Malech, Harry L, Ledbetter, Jeffrey A, Elkon, Keith B, Kaplan, Mariana J
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.02.2016 Nature Publishing Group
Subjects	13/31 14/63 38 38/77 59 631/250/2504 64 64/60 692/699/249/1313/1613 Adult Animals Antigen-Antibody Complex Autoimmune diseases Biomedicine Cancer Research DNA, Mitochondrial - metabolism Extracellular Traps - immunology Extracellular Traps - metabolism Female Granulomatous Disease, Chronic - genetics Granulomatous Disease, Chronic - immunology Granulomatous Disease, Chronic - metabolism Humans Immunoprecipitation In Vitro Techniques Infectious Diseases Interferon Type I - immunology Jurkat Cells Kidney - immunology Kidney - metabolism Lupus Erythematosus, Systemic - immunology Lupus Erythematosus, Systemic - metabolism Male Metabolic Diseases Mice Microscopy, Fluorescence Mitochondria - metabolism Mitochondrial DNA Molecular Medicine NADPH Oxidases - genetics Neurons Neurosciences Neutrophils - immunology Oxidation-Reduction Oxidative stress Pathogenesis Peroxidase - metabolism Reactive Oxygen Species - metabolism Real-Time Polymerase Chain Reaction Ribonucleoproteins
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Abstract	Lupus-like disease is driven by NETs enriched in mitochondrial DNA. Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are generated and their roles in sterile inflammation remain unclear. Ribonucleoprotein immune complexes (RNP ICs), inducers of NETosis, require mitochondrial reactive oxygen species (ROS) for maximal NET stimulation. After RNP IC stimulation of neutrophils, mitochondria become hypopolarized and translocate to the cell surface. Extracellular release of oxidized mitochondrial DNA is proinflammatory in vitro , and when this DNA is injected into mice, it stimulates type I interferon (IFN) signaling through a pathway dependent on the DNA sensor STING. Mitochondrial ROS are also necessary for spontaneous NETosis of low-density granulocytes from individuals with systemic lupus erythematosus. This was also observed in individuals with chronic granulomatous disease, who lack NADPH oxidase activity but still develop autoimmunity and type I IFN signatures. Mitochondrial ROS inhibition in vivo reduces disease severity and type I IFN responses in a mouse model of lupus. Together, these findings highlight a role for mitochondria in the generation not only of NETs but also of pro-inflammatory oxidized mitochondrial DNA in autoimmune diseases.
AbstractList	Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are generated and their roles in sterile inflammation remain unclear. Ribonucleoprotein immune complexes (RNP ICs), inducers of NETosis, require mitochondrial reactive oxygen species (ROS) for maximal NET stimulation. After RNP IC stimulation of neutrophils, mitochondria become hypopolarized and translocate to the cell surface. Extracellular release of oxidized mitochondrial DNA is proinflammatory in vitro, and when this DNA is injected into mice, it stimulates type I interferon (IFN) signaling through a pathway dependent on the DNA sensor STING. Mitochondrial ROS are also necessary for spontaneous NETosis of low-density granulocytes from individuals with systemic lupus erythematosus. This was also observed in individuals with chronic granulomatous disease, who lack NADPH oxidase activity but still develop autoimmunity and type I IFN signatures. Mitochondrial ROS inhibition in vivo reduces disease severity and type I IFN responses in a mouse model of lupus. Together, these findings highlight a role for mitochondria in the generation not only of NETs but also of pro-inflammatory oxidized mitochondrial DNA in autoimmune diseases. Neutrophil extracellular traps (NETs) are implicated in autoimmunity but how they are generated and their roles in sterile inflammation remain unclear. Ribonucleoprotein immune complexes, inducers of NETosis, require mitochondrial ROS for maximal NET stimulation. During this process, mitochondria become hypopolarized and translocate to the cell surface. Extracellular release of oxidized mitochondrial DNA is proinflammatory in vitro and, when injected into mice, stimulates type-I interferon (IFN) signaling through a pathway dependent on the DNA sensor, STING. Mitochondrial ROS is also necessary for spontaneous NETosis of low-density granulocytes from individuals with systemic lupus erythematosus (SLE). This was also observed in individuals with chronic granulomatous disease (CGD), which lack NADPH-oxidase activity, but still develop autoimmunity and type I-IFN signatures. Mitochondrial ROS inhibition in vivo reduces disease severity and type-I IFN responses in a mouse model of lupus. These findings highlight a role for mitochondria in the generation not only of NETs but also of pro-inflammatory oxidized mitochondrial DNA in autoimmune diseases. Lupus-like disease is driven by NETs enriched in mitochondrial DNA. Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are generated and their roles in sterile inflammation remain unclear. Ribonucleoprotein immune complexes (RNP ICs), inducers of NETosis, require mitochondrial reactive oxygen species (ROS) for maximal NET stimulation. After RNP IC stimulation of neutrophils, mitochondria become hypopolarized and translocate to the cell surface. Extracellular release of oxidized mitochondrial DNA is proinflammatory in vitro , and when this DNA is injected into mice, it stimulates type I interferon (IFN) signaling through a pathway dependent on the DNA sensor STING. Mitochondrial ROS are also necessary for spontaneous NETosis of low-density granulocytes from individuals with systemic lupus erythematosus. This was also observed in individuals with chronic granulomatous disease, who lack NADPH oxidase activity but still develop autoimmunity and type I IFN signatures. Mitochondrial ROS inhibition in vivo reduces disease severity and type I IFN responses in a mouse model of lupus. Together, these findings highlight a role for mitochondria in the generation not only of NETs but also of pro-inflammatory oxidized mitochondrial DNA in autoimmune diseases.
Author	Purmalek, Monica M De Ravin, Suk S Malech, Harry L Ledbetter, Jeffrey A Kaplan, Mariana J Blanco, Luz P Elkon, Keith B Lood, Christian Carmona-Rivera, Carmelo Smith, Carolyne K
AuthorAffiliation	3 Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 1 Division of Rheumatology, University of Washington, Seattle, WA 2 Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH), Bethesda, MD 4 Department of Immunology, University of Washington, Seattle, WA
AuthorAffiliation_xml	– name: 3 Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD – name: 1 Division of Rheumatology, University of Washington, Seattle, WA – name: 2 Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH), Bethesda, MD – name: 4 Department of Immunology, University of Washington, Seattle, WA
Author_xml	– sequence: 1 givenname: Christian surname: Lood fullname: Lood, Christian organization: Division of Rheumatology, University of Washington – sequence: 2 givenname: Luz P surname: Blanco fullname: Blanco, Luz P organization: Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH) – sequence: 3 givenname: Monica M surname: Purmalek fullname: Purmalek, Monica M organization: Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH) – sequence: 4 givenname: Carmelo surname: Carmona-Rivera fullname: Carmona-Rivera, Carmelo organization: Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH) – sequence: 5 givenname: Suk S surname: De Ravin fullname: De Ravin, Suk S organization: Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, NIH – sequence: 6 givenname: Carolyne K surname: Smith fullname: Smith, Carolyne K organization: Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH) – sequence: 7 givenname: Harry L orcidid: 0000-0001-5874-5775 surname: Malech fullname: Malech, Harry L organization: Laboratory of Host Defenses, National Institute of Allergy and Infectious Diseases, NIH – sequence: 8 givenname: Jeffrey A surname: Ledbetter fullname: Ledbetter, Jeffrey A organization: Department of Immunology, University of Washington – sequence: 9 givenname: Keith B orcidid: 0000-0002-7340-6146 surname: Elkon fullname: Elkon, Keith B email: elkon@uw.edu organization: Division of Rheumatology, University of Washington, Department of Immunology, University of Washington – sequence: 10 givenname: Mariana J surname: Kaplan fullname: Kaplan, Mariana J email: mariana.kaplan@nih.gov organization: Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health (NIH)
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26779811$$D View this record in MEDLINE/PubMed
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Snippet	Lupus-like disease is driven by NETs enriched in mitochondrial DNA. Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are... Neutrophil extracellular traps (NETs) are implicated in autoimmunity, but how they are generated and their roles in sterile inflammation remain unclear.... Neutrophil extracellular traps (NETs) are implicated in autoimmunity but how they are generated and their roles in sterile inflammation remain unclear....
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SubjectTerms	13/31 14/63 38 38/77 59 631/250/2504 64 64/60 692/699/249/1313/1613 Adult Animals Antigen-Antibody Complex Autoimmune diseases Biomedicine Cancer Research DNA, Mitochondrial - metabolism Extracellular Traps - immunology Extracellular Traps - metabolism Female Granulomatous Disease, Chronic - genetics Granulomatous Disease, Chronic - immunology Granulomatous Disease, Chronic - metabolism Humans Immunoprecipitation In Vitro Techniques Infectious Diseases Interferon Type I - immunology Jurkat Cells Kidney - immunology Kidney - metabolism Lupus Erythematosus, Systemic - immunology Lupus Erythematosus, Systemic - metabolism Male Metabolic Diseases Mice Microscopy, Fluorescence Mitochondria - metabolism Mitochondrial DNA Molecular Medicine NADPH Oxidases - genetics Neurons Neurosciences Neutrophils - immunology Oxidation-Reduction Oxidative stress Pathogenesis Peroxidase - metabolism Reactive Oxygen Species - metabolism Real-Time Polymerase Chain Reaction Ribonucleoproteins
Title	Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease
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