Interleukin-6 Signaling Drives Fibrosis in Unresolved Inflammation
Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was s...
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| Published in: | Immunity (Cambridge, Mass.) Vol. 40; no. 1; pp. 40 - 50 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Elsevier Inc
16-01-2014
Elsevier Limited Cell Press |
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| Online Access: | Get full text |
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| Abstract | Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon-γ (IFN-γ), STAT1, or RAG-1. Here, IFN-γ and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation.
•Repeated acute resolving inflammation leads to excessive tissue damage•IL-6 regulates profibrotic IFN-γ-secreting T cells•IFN-γ increases detrimental STAT1 signaling in stromal tissue•STAT1 activity alters homeostatic control of extracellular matrix to promote fibrosis |
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| AbstractList | Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon-γ (IFN-γ), STAT1, or RAG-1. Here, IFN-γ and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation.
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Repeated acute resolving inflammation leads to excessive tissue damage
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IL-6 regulates profibrotic IFN-γ-secreting T cells
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IFN-γ increases detrimental STAT1 signaling in stromal tissue
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STAT1 activity alters homeostatic control of extracellular matrix to promote fibrosis Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon-? (IFN-?), STAT1, or RAG-1. Here, IFN-? and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation. Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon-γ (IFN-γ), STAT1, or RAG-1. Here, IFN-γ and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation. •Repeated acute resolving inflammation leads to excessive tissue damage•IL-6 regulates profibrotic IFN-γ-secreting T cells•IFN-γ increases detrimental STAT1 signaling in stromal tissue•STAT1 activity alters homeostatic control of extracellular matrix to promote fibrosis Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon-γ (IFN-γ), STAT1, or RAG-1. Here, IFN-γ and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation. Fibrosis in response to tissue damage or persistent inflammation is a pathological hallmark of many chronic degenerative diseases. By using a model of acute peritoneal inflammation, we have examined how repeated inflammatory activation promotes fibrotic tissue injury. In this context, fibrosis was strictly dependent on interleukin-6 (IL-6). Repeat inflammation induced IL-6-mediated T helper 1 (Th1) cell effector commitment and the emergence of STAT1 (signal transducer and activator of transcription-1) activity within the peritoneal membrane. Fibrosis was not observed in mice lacking interferon- gamma (IFN- gamma ), STAT1, or RAG-1. Here, IFN- gamma and STAT1 signaling disrupted the turnover of extracellular matrix by metalloproteases. Whereas IL-6-deficient mice resisted fibrosis, transfer of polarized Th1 cells or inhibition of MMP activity reversed this outcome. Thus, IL-6 causes compromised tissue repair by shifting acute inflammation into a more chronic profibrotic state through induction of Th1 cell responses as a consequence of recurrent inflammation. |
| Author | Uceda, Javier Colmont, Chantal S. Hams, Emily Jones, Simon A. Taylor, Philip R. Hammond, Victoria J. McLeod, Louise Foster, Thomas L. Jenkins, Brendan J. Greenhill, Claire J. Newton, Zarabeth O’Donnell, Valerie B. Fielding, Ceri A. McLoughlin, Rachel M. Coles, Barbara Topley, Nicholas Humphreys, Ian R. Williams, Anwen S. Rice, Christopher M. Craig, Katherine J. Lambie, Mark Williams, John D. Williams, Geraint T. Liao, Chia-Te Kift-Morgan, Ann Davies, Simon J. Jones, Gareth W. |
| Author_xml | – sequence: 1 givenname: Ceri A. surname: Fielding fullname: Fielding, Ceri A. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 2 givenname: Gareth W. surname: Jones fullname: Jones, Gareth W. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 3 givenname: Rachel M. surname: McLoughlin fullname: McLoughlin, Rachel M. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 4 givenname: Louise surname: McLeod fullname: McLeod, Louise organization: Centre for Innate Immunity and Infectious Diseases, Monash Institute for Medical Research, Monash University, Clayton, VIC 3168, Australia – sequence: 5 givenname: Victoria J. surname: Hammond fullname: Hammond, Victoria J. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 6 givenname: Javier surname: Uceda fullname: Uceda, Javier organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 7 givenname: Anwen S. surname: Williams fullname: Williams, Anwen S. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 8 givenname: Mark surname: Lambie fullname: Lambie, Mark organization: Department of Nephrology, University Hospital of North Staffordshire and Institute for Science and Technology in Medicine, Keele University, Stoke-on-Trent ST4 7QB, UK – sequence: 9 givenname: Thomas L. surname: Foster fullname: Foster, Thomas L. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 10 givenname: Chia-Te surname: Liao fullname: Liao, Chia-Te organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 11 givenname: Christopher M. surname: Rice fullname: Rice, Christopher M. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 12 givenname: Claire J. surname: Greenhill fullname: Greenhill, Claire J. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 13 givenname: Chantal S. surname: Colmont fullname: Colmont, Chantal S. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 14 givenname: Emily surname: Hams fullname: Hams, Emily organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 15 givenname: Barbara surname: Coles fullname: Coles, Barbara organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 16 givenname: Ann surname: Kift-Morgan fullname: Kift-Morgan, Ann organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 17 givenname: Zarabeth surname: Newton fullname: Newton, Zarabeth organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 18 givenname: Katherine J. surname: Craig fullname: Craig, Katherine J. organization: Institute of Nephrology, Institute of Molecular and Experimental Medicine, School of Medicine, Cardiff University, Heath Park, Cardiff CF14 4XN, UK – sequence: 19 givenname: John D. surname: Williams fullname: Williams, John D. organization: Institute of Nephrology, Institute of Molecular and Experimental Medicine, School of Medicine, Cardiff University, Heath Park, Cardiff CF14 4XN, UK – sequence: 20 givenname: Geraint T. surname: Williams fullname: Williams, Geraint T. organization: Section of Pathology, Institute of Cancer and Genetics, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 21 givenname: Simon J. surname: Davies fullname: Davies, Simon J. organization: Department of Nephrology, University Hospital of North Staffordshire and Institute for Science and Technology in Medicine, Keele University, Stoke-on-Trent ST4 7QB, UK – sequence: 22 givenname: Ian R. surname: Humphreys fullname: Humphreys, Ian R. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 23 givenname: Valerie B. surname: O’Donnell fullname: O’Donnell, Valerie B. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 24 givenname: Philip R. surname: Taylor fullname: Taylor, Philip R. organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 25 givenname: Brendan J. surname: Jenkins fullname: Jenkins, Brendan J. organization: Centre for Innate Immunity and Infectious Diseases, Monash Institute for Medical Research, Monash University, Clayton, VIC 3168, Australia – sequence: 26 givenname: Nicholas surname: Topley fullname: Topley, Nicholas email: topley@cf.ac.uk organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK – sequence: 27 givenname: Simon A. surname: Jones fullname: Jones, Simon A. email: jonessa@cf.ac.uk organization: Cardiff Institute of Infection and Immunity, Cardiff University, School of Medicine, Heath Park, Cardiff CF14 4XN, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24412616$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Article-2 ObjectType-Feature-1 Present address: School of Biochemistry & Immunology, Trinity College Dublin, Dublin, Ireland These authors contributed equally to this work These authors contributed equally to this work and are co-senior authors Present address: Institute of Molecular Medicine, Trinity College Dublin, Dublin, Ireland |
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| SubjectTerms | Acute Disease Adoptive Transfer Animals Cells, Cultured Charitable foundations Chronic Disease Cytokines Disease Models, Animal Extracellular Matrix - immunology Feedback, Physiological Fibrosis Humans Interferon-gamma - genetics Interferon-gamma - metabolism Interleukin-6 - genetics Interleukin-6 - immunology Interleukin-6 - metabolism Mice Mice, Inbred C57BL Mice, Knockout Peritoneal dialysis Peritoneum - pathology Peritonitis - genetics Peritonitis - pathology Signal Transduction STAT1 Transcription Factor - genetics STAT1 Transcription Factor - metabolism Th1 Cells - immunology Th1 Cells - transplantation Viral infections |
| Title | Interleukin-6 Signaling Drives Fibrosis in Unresolved Inflammation |
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