Emerging concepts of type I interferons in SLE pathogenesis and therapy
Type I interferons have been suspected for decades to have a crucial role in the pathogenesis of systemic lupus erythematosus (SLE). Evidence has now overturned several long-held assumptions about how type I interferons are regulated and cause pathological conditions, providing a new view of SLE pat...
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Published in | Nature reviews. Rheumatology Vol. 18; no. 10; pp. 575 - 590 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
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Nature Publishing Group UK
01.10.2022
Nature Publishing Group |
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Abstract | Type I interferons have been suspected for decades to have a crucial role in the pathogenesis of systemic lupus erythematosus (SLE). Evidence has now overturned several long-held assumptions about how type I interferons are regulated and cause pathological conditions, providing a new view of SLE pathogenesis that resolves longstanding clinical dilemmas. This evidence includes data on interferons in relation to genetic predisposition and epigenetic regulation. Importantly, data are now available on the role of interferons in the early phases of the disease and the importance of non-haematopoietic cellular sources of type I interferons, such as keratinocytes, renal tubular cells, glial cells and synovial stromal cells, as well as local responses to type I interferons within these tissues. These local effects are found not only in inflamed target organs in established SLE, but also in histologically normal skin during asymptomatic preclinical phases, suggesting a role in disease initiation. In terms of clinical application, evidence relating to biomarkers to characterize the type I interferon system is complex, and, notably, interferon-blocking therapies are now licensed for the treatment of SLE. Collectively, the available data enable us to propose a model of disease pathogenesis that invokes the unique value of interferon-targeted therapies. Accordingly, future approaches in SLE involving disease reclassification and preventative strategies in preclinical phases should be investigated.
In this Review, Psarras, Wittmann and Vital discuss evidence of the production of type I interferons by cells and tissues other than haematopoietic cells. These interferons can have local effects, and their roles in the pathogenesis of systemic lupus erythematosus suggest the value of interferon-blocking therapies for treatment of this condition.
Key points
Type I interferon pathway variants are prominent in genetic predisposition to systemic lupus erythematosus (SLE), and epigenetic regulation affects classic interferon-stimulated genes and genes less directly related to interferon signalling.
Contrary to previous assumptions, plasmacytoid dendritic cells lose their immunogenic functions in SLE, including type I interferon production and antigen presentation.
Non-haematopoietic cells within organs affected by SLE (especially the skin) produce type I interferons, express interferon-stimulated genes, and have roles in the initiation of SLE and in established SLE.
Both the dysfunction of plasmacytoid dendritic cells and the non-haematopoietic production of type I interferons is seen in all anti-nuclear antibody-positive individuals, regardless of whether progression to organ inflammation later occurs.
Diverse biomarkers (each with advantages and disadvantages) can characterize type I interferon pathway activation, including evaluation of interferon proteins and several effects downstream of the type I interferon receptor.
Several therapies targeting the type I interferon pathway are in development (including the now licensed anifrolumab), and might have specific clinical properties relating to the model of SLE proposed herein. |
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AbstractList | Type I interferons have been suspected for decades to have a crucial role in the pathogenesis of systemic lupus erythematosus (SLE). Evidence has now overturned several long-held assumptions about how type I interferons are regulated and cause pathological conditions, providing a new view of SLE pathogenesis that resolves longstanding clinical dilemmas. This evidence includes data on interferons in relation to genetic predisposition and epigenetic regulation. Importantly, data are now available on the role of interferons in the early phases of the disease and the importance of non-haematopoietic cellular sources of type I interferons, such as keratinocytes, renal tubular cells, glial cells and synovial stromal cells, as well as local responses to type I interferons within these tissues. These local effects are found not only in inflamed target organs in established SLE, but also in histologically normal skin during asymptomatic preclinical phases, suggesting a role in disease initiation. In terms of clinical application, evidence relating to biomarkers to characterize the type I interferon system is complex, and, notably, interferon-blocking therapies are now licensed for the treatment of SLE. Collectively, the available data enable us to propose a model of disease pathogenesis that invokes the unique value of interferon-targeted therapies. Accordingly, future approaches in SLE involving disease reclassification and preventative strategies in preclinical phases should be investigated.
In this Review, Psarras, Wittmann and Vital discuss evidence of the production of type I interferons by cells and tissues other than haematopoietic cells. These interferons can have local effects, and their roles in the pathogenesis of systemic lupus erythematosus suggest the value of interferon-blocking therapies for treatment of this condition.
Key points
Type I interferon pathway variants are prominent in genetic predisposition to systemic lupus erythematosus (SLE), and epigenetic regulation affects classic interferon-stimulated genes and genes less directly related to interferon signalling.
Contrary to previous assumptions, plasmacytoid dendritic cells lose their immunogenic functions in SLE, including type I interferon production and antigen presentation.
Non-haematopoietic cells within organs affected by SLE (especially the skin) produce type I interferons, express interferon-stimulated genes, and have roles in the initiation of SLE and in established SLE.
Both the dysfunction of plasmacytoid dendritic cells and the non-haematopoietic production of type I interferons is seen in all anti-nuclear antibody-positive individuals, regardless of whether progression to organ inflammation later occurs.
Diverse biomarkers (each with advantages and disadvantages) can characterize type I interferon pathway activation, including evaluation of interferon proteins and several effects downstream of the type I interferon receptor.
Several therapies targeting the type I interferon pathway are in development (including the now licensed anifrolumab), and might have specific clinical properties relating to the model of SLE proposed herein. Type I interferons have been suspected for decades to have a crucial role in the pathogenesis of systemic lupus erythematosus (SLE). Evidence has now overturned several long-held assumptions about how type I interferons are regulated and cause pathological conditions, providing a new view of SLE pathogenesis that resolves longstanding clinical dilemmas. This evidence includes data on interferons in relation to genetic predisposition and epigenetic regulation. Importantly, data are now available on the role of interferons in the early phases of the disease and the importance of non-haematopoietic cellular sources of type I interferons, such as keratinocytes, renal tubular cells, glial cells and synovial stromal cells, as well as local responses to type I interferons within these tissues. These local effects are found not only in inflamed target organs in established SLE, but also in histologically normal skin during asymptomatic preclinical phases, suggesting a role in disease initiation. In terms of clinical application, evidence relating to biomarkers to characterize the type I interferon system is complex, and, notably, interferon-blocking therapies are now licensed for the treatment of SLE. Collectively, the available data enable us to propose a model of disease pathogenesis that invokes the unique value of interferon-targeted therapies. Accordingly, future approaches in SLE involving disease reclassification and preventative strategies in preclinical phases should be investigated.In this Review, Psarras, Wittmann and Vital discuss evidence of the production of type I interferons by cells and tissues other than haematopoietic cells. These interferons can have local effects, and their roles in the pathogenesis of systemic lupus erythematosus suggest the value of interferon-blocking therapies for treatment of this condition. |
Author | Vital, Edward M. Psarras, Antonios Wittmann, Miriam |
Author_xml | – sequence: 1 givenname: Antonios orcidid: 0000-0002-6318-0171 surname: Psarras fullname: Psarras, Antonios organization: Kennedy Institute of Rheumatology, University of Oxford, Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds – sequence: 2 givenname: Miriam surname: Wittmann fullname: Wittmann, Miriam organization: Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, Department of Dermatology, University Medical Center of the Johannes Gutenberg University – sequence: 3 givenname: Edward M. orcidid: 0000-0003-1637-4755 surname: Vital fullname: Vital, Edward M. email: E.M.J.Vital@leeds.ac.uk organization: Leeds Institute of Rheumatic and Musculoskeletal Medicine, University of Leeds, NIHR Leeds Biomedical Research Centre, Leeds Teaching Hospitals NHS Trust |
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Snippet | Type I interferons have been suspected for decades to have a crucial role in the pathogenesis of systemic lupus erythematosus (SLE). Evidence has now... |
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Title | Emerging concepts of type I interferons in SLE pathogenesis and therapy |
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