Endogenous histones function as alarmins in sterile inflammatory liver injury through Toll‐like receptor 9 in mice
Sterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage‐associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high‐mobility group box 1 have been shown to be critical in s...
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| Veröffentlicht in: | Hepatology (Baltimore, Md.) Jg. 54; H. 3; S. 999 - 1008 |
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| Hauptverfasser: | , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
| Veröffentlicht: |
Hoboken
Wiley Subscription Services, Inc., A Wiley Company
02.09.2011
Wiley Wolters Kluwer Health, Inc |
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| ISSN: | 0270-9139, 1527-3350, 1527-3350 |
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| Abstract | Sterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage‐associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high‐mobility group box 1 have been shown to be critical in sterile inflammation, the role of nuclear histone proteins has not yet been investigated. We report that endogenous histones function as DAMPs after ischemic injury through the pattern recognition receptor Toll‐like receptor (TLR) 9 to initiate inflammation. Using an in vivo model of hepatic ischemia/reperfusion (I/R) injury, we show that levels of circulating histones are significantly higher after I/R, and that histone neutralization significantly protects against injury. Injection of exogenous histones exacerbates I/R injury through cytotoxic effects mediated by TLR9 and MyD88. In addition, histone administration increases TLR9 activation, whereas neither TLR9 nor MyD88 mutant mice respond to exogenous histones. Furthermore, we demonstrate in vitro that extracellular histones enhance DNA‐mediated TLR9 activation in immune cells through a direct interaction. Conclusion: These novel findings reveal that histones represent a new class of DAMP molecules and serve as a crucial link between initial damage and activation of innate immunity during sterile inflammation. (HEPATOLOGY 2011; 54:999–1008) |
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| AbstractList | Sterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage-associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high-mobility group box 1 have been shown to be critical in sterile inflammation, the role of nuclear histone proteins has not yet been investigated. We report that endogenous histones function as DAMPs after ischemic injury through the pattern recognition receptor Toll-like receptor (TLR) 9 to initiate inflammation. Using an in vivo model of hepatic ischemia/reperfusion (I/R) injury, we show that levels of circulating histones are significantly higher after I/R, and that histone neutralization significantly protects against injury. Injection of exogenous histones exacerbates I/R injury through cytotoxic effects mediated by TLR9 and MyD88. In addition, histone administration increases TLR9 activation, whereas neither TLR9 nor MyD88 mutant mice respond to exogenous histones. Furthermore, we demonstrate in vitro that extracellular histones enhance DNA-mediated TLR9 activation in immune cells through a direct interaction. Conclusion: These novel findings reveal that histones represent a new class of DAMP molecules and serve as a crucial link between initial damage and activation of innate immunity during sterile inflammation. (HEPATOLOGY 2011; 54:999-1008) Sterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage-associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high-mobility group box 1 have been shown to be critical in sterile inflammation, the role of nuclear histone proteins has not yet been investigated. We report that endogenous histones function as DAMPs after ischemic injury through the pattern recognition receptor Toll-like receptor (TLR) 9 to initiate inflammation. Using an in vivo model of hepatic ischemia/reperfusion (I/R) injury, we show that levels of circulating histones are significantly higher after I/R, and that histone neutralization significantly protects against injury. Injection of exogenous histones exacerbates I/R injury through cytotoxic effects mediated by TLR9 and MyD88. In addition, histone administration increases TLR9 activation, whereas neither TLR9 nor MyD88 mutant mice respond to exogenous histones. Furthermore, we demonstrate in vitro that extracellular histones enhance DNA-mediated TLR9 activation in immune cells through a direct interaction. These novel findings reveal that histones represent a new class of DAMP molecules and serve as a crucial link between initial damage and activation of innate immunity during sterile inflammation. Sterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage-associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high-mobility group box 1 have been shown to be critical in sterile inflammation, the role of nuclear histone proteins has not yet been investigated. We report that endogenous histones function as DAMPs after ischemic injury through the pattern recognition receptor Toll-like receptor (TLR) 9 to initiate inflammation. Using an in vivo model of hepatic ischemia/reperfusion (I/R) injury, we show that levels of circulating histones are significantly higher after I/R, and that histone neutralization significantly protects against injury. Injection of exogenous histones exacerbates I/R injury through cytotoxic effects mediated by TLR9 and MyD88. In addition, histone administration increases TLR9 activation, whereas neither TLR9 nor MyD88 mutant mice respond to exogenous histones. Furthermore, we demonstrate in vitro that extracellular histones enhance DNA-mediated TLR9 activation in immune cells through a direct interaction.UNLABELLEDSterile inflammatory insults are known to activate innate immunity and propagate organ damage through the recognition of extracellular damage-associated molecular pattern (DAMP) molecules. Although DAMPs such as endogenous DNA and nuclear high-mobility group box 1 have been shown to be critical in sterile inflammation, the role of nuclear histone proteins has not yet been investigated. We report that endogenous histones function as DAMPs after ischemic injury through the pattern recognition receptor Toll-like receptor (TLR) 9 to initiate inflammation. Using an in vivo model of hepatic ischemia/reperfusion (I/R) injury, we show that levels of circulating histones are significantly higher after I/R, and that histone neutralization significantly protects against injury. Injection of exogenous histones exacerbates I/R injury through cytotoxic effects mediated by TLR9 and MyD88. In addition, histone administration increases TLR9 activation, whereas neither TLR9 nor MyD88 mutant mice respond to exogenous histones. Furthermore, we demonstrate in vitro that extracellular histones enhance DNA-mediated TLR9 activation in immune cells through a direct interaction.These novel findings reveal that histones represent a new class of DAMP molecules and serve as a crucial link between initial damage and activation of innate immunity during sterile inflammation.CONCLUSIONThese novel findings reveal that histones represent a new class of DAMP molecules and serve as a crucial link between initial damage and activation of innate immunity during sterile inflammation. |
| Author | Tsung, Allan Liao, Xinghua Zhang, Lemeng Huang, Hai Xu, Jun Yan, Wei Esmon, Charles T. Nace, Gary Billiar, Timothy Ross, Mark Evankovich, John |
| Author_xml | – sequence: 1 givenname: Hai surname: Huang fullname: Huang, Hai – sequence: 2 givenname: John surname: Evankovich fullname: Evankovich, John – sequence: 3 givenname: Wei surname: Yan fullname: Yan, Wei – sequence: 4 givenname: Gary surname: Nace fullname: Nace, Gary – sequence: 5 givenname: Lemeng surname: Zhang fullname: Zhang, Lemeng – sequence: 6 givenname: Mark surname: Ross fullname: Ross, Mark – sequence: 7 givenname: Xinghua surname: Liao fullname: Liao, Xinghua – sequence: 8 givenname: Timothy surname: Billiar fullname: Billiar, Timothy – sequence: 9 givenname: Jun surname: Xu fullname: Xu, Jun – sequence: 10 givenname: Charles T. surname: Esmon fullname: Esmon, Charles T. – sequence: 11 givenname: Allan surname: Tsung fullname: Tsung, Allan email: tsunga@upmc.edu |
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| ContentType | Journal Article |
| Copyright | Copyright © 2011 American Association for the Study of Liver Diseases 2015 INIST-CNRS Copyright © 2011 American Association for the Study of Liver Diseases. Copyright © 2011 American Association for the Study of Liver Diseases 2011 |
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| Issue | 3 |
| Keywords | Vertebrata Mammalia Mouse Animal Liver Rodentia Gastroenterology Toll like receptor |
| Language | English |
| License | CC BY 4.0 Copyright © 2011 American Association for the Study of Liver Diseases. Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation. |
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| Notes | These authors contributed equally to this work. fax: 412‐692‐2002 Potential conflict of interest: Nothing to report. Supported by a Howard Hughes Medical Institute Physician‐Scientist Award (A. T.), an American College of Surgeons Research Fellowship (A. T.), and a Howard Hughes Medical Institute Research Training for Medical Student Fellowship (J. E.) ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Supported by a Howard Hughes Medical Institute Physician-Scientist Award (A. T.), an American College of Surgeons Research Fellowship (A. T.), and a Howard Hughes Medical Institute Research Training for Medical Student Fellowship (J. E.) |
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| PublicationTitle | Hepatology (Baltimore, Md.) |
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| SubjectTerms | Animals Biological and medical sciences Cells, Cultured Gastroenterology. Liver. Pancreas. Abdomen Hepatology Histones - physiology HMGB1 Protein - physiology Immunity, Innate Inflammation Inflammation - etiology Liver - blood supply Liver Injury/Regeneration Liver. Biliary tract. Portal circulation. Exocrine pancreas Male Medical sciences Mice Mice, Inbred C57BL Myeloid Differentiation Factor 88 - physiology Reperfusion Injury - prevention & control Rodents Signal Transduction Toll-Like Receptor 9 - physiology |
| Title | Endogenous histones function as alarmins in sterile inflammatory liver injury through Toll‐like receptor 9 in mice |
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