JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 8, 2014, Pages 3068-3073

  Lu, Ben ^a,b   Antoine, Daniel J ^c   Kwan, Kevin ^b   Lundbäck, Peter ^d   Wähämaa, Heidi ^d   Schierbeck, Hanna ^d   Robinson, Melissa ^b   Van Zoelen, Marieke A D ^b   Yang, Huan ^b   Li, Jianhua ^b   Erlandsson Harris, Helena ^d   Chavan, Sangeeta S ^b   Wang, Haichao ^e   Andersson, Ulf ^d   Tracey, Kevin J ^a,b,d  

^a Northwell Health   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d KAROLINSKA INSTITUTE   (Sweden)

^e NORTH SHORE UNIVERSITY HOSPITAL   (United States)

Author keywords

Cytokine; Damage associated molecular pattern; Innate immunity; Pathogen associated molecular pattern; Therapy

Indexed keywords

2 TERT BUTYL 9 FLUORO 3,6 DIHYDRO 7H BENZ[H]IMIDAZO[4,5 F]ISOQUINOLIN 7 ONE; BETA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P70; JANUS KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; STAT1 PROTEIN; TUMOR NECROSIS FACTOR;

ACETYLATION; ANIMAL CELL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOPLASM; DISULFIDE BOND; EXTRACELLULAR SPACE; GENE DELETION; MACROPHAGE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

CYTOKINE; DAMAGE-ASSOCIATED MOLECULAR PATTERN; INNATE IMMUNITY; PATHOGEN-ASSOCIATED MOLECULAR PATTERN; THERAPY;

ACETYLATION; ACTIVE TRANSPORT, CELL NUCLEUS; ANALYSIS OF VARIANCE; ANIMALS; BENZIMIDAZOLES; BLOTTING, WESTERN; CELL NUCLEUS; CHROMATOGRAPHY, LIQUID; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; HMGB1 PROTEIN; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE I; JANUS KINASE 1; LIPOPOLYSACCHARIDES; MICE; PYRIDONES; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TANDEM MASS SPECTROMETRY;

EID: 84896816054     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316925111     Document Type: Article

References (41)

1. Yanai H, et al. (2009) HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462(7269):99-103.
2. Andersson U, Tracey KJ (2011) HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 29:139-162.
3. Venereau E, Schiraldi M, Uguccioni M, Bianchi ME (2013) HMGB1 and leukocyte migration during trauma and sterile inflammation. Mol Immunol 55(1):76-82.
4. Maroso M, et al. (2010) Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 16(4):413-419.
5. Urbonaviciute V, et al. (2008) Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: Implications for the pathogenesis of SLE. J Exp Med 205(13):3007-3018.
6. Lu B, et al. (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488(7413):670-674.
7. Lu B, Wang H, Andersson U, Tracey KJ (2013) Regulation of HMGB1 release by inflammasomes. Protein Cell 4(3):163-167.
8. Yang H, et al. (2010) A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc Natl Acad Sci USA 107(26):11942-11947.
9. Mittal D, et al. (2010) TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. EMBO J 29(13):2242-2252.
10. Manfredi AA, et al. (2008) Maturing dendritic cells depend on RAGE for in vivo homing to lymph nodes. J Immunol 180(4):2270-2275.
11. Venereau E, et al. (2012) Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 209(9):1519-1528.
12. Rouhiainen A, Kuja-Panula J, Tumova S, Rauvala H (2013) RAGE-mediated cell signaling. Methods Mol Biol 963:239-263.
13. Patel VS, et al. (2013) High Mobility Group Box-1 mediates hyperoxia-induced impairment of Pseudomonas aeruginosa clearance and inflammatory lung injury in mice. Am J Respir Cell Mol Biol 48(3):280-287.
14. Entezari M, et al. (2012) Inhibition of high-mobility group box 1 protein (HMGB1) enhances bacterial clearance and protects against Pseudomonas Aeruginosa pneumonia in cystic fibrosis. Mol Med 18:477-485.
15. Chavan SS, et al. (2012) HMGB1 mediates cognitive impairment in sepsis survivors. Mol Med 18:930-937.
16. Hao N, Budnik BA, Gunawardena J, O'Shea EK (2013) Tunable signal processing through modular control of transcription factor translocation. Science 339(6118): 460-464.
17. Bonaldi T, et al. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22(20):5551-5560. (Pubitemid 37279964)
18. Evankovich J, et al. (2010) High mobility group box 1 release from hepatocytes during ischemia and reperfusion injury is mediated by decreased histone deacetylase activity. J Biol Chem 285(51):39888-39897.
19. Zhang X, et al. (2008) Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages. J Immunol 181(7):5015-5023.
20. Youn JH, Shin JS (2006) Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion. J Immunol 177(11):7889-7897.
21. Kayagaki N, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479(7371):117-121.
22. Lamkanfi M, et al. (2010) Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J Immunol 185(7):4385-4392.
23. Rathinam VA, et al. (2012) TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 150(3):606-619.
24. Willingham SB, et al. (2009) NLRP3 (NALP3, Cryopyrin) facilitates in vivo caspase-1 activation, necrosis, and HMGB1 release via inflammasome-dependent and -independent pathways. J Immunol 183(3):2008-2015.
25. Hett EC, et al. (2013) Chemical genetics reveals a kinase-independent role for protein kinase R in pyroptosis. Nat Chem Biol 9(6):398-405.
26. Rendon-Mitchell B, et al. (2003) IFN-gamma induces high mobility group box 1 protein release partly through a TNF-dependent mechanism. J Immunol 170(7):3890-3897. (Pubitemid 36361997)
27. Jiang W, Pisetsky DS (2006) The role of IFN-alpha and nitric oxide in the release of HMGB1 by RAW 264.7 cells stimulated with polyinosinic-polycytidylic acid or lipopolysaccharide. J Immunol 177(5):3337-3343. (Pubitemid 44277853)
28. Kim JH, et al. (2009) Bacterial endotoxin induces the release of high mobility group box 1 via the IFN-beta signaling pathway. J Immunol 182(4):2458-2466.
29. Herzig D, et al. (2012) STAT1-deficient mice are resistant to cecal ligation and puncture-induced septic shock. Shock 38(4):395-402.
30. Sakaguchi S, et al. (2003) Essential role of IRF-3 in lipopolysaccharide-induced interferon-beta gene expression and endotoxin shock. Biochem Biophys Res Commun 306(4):860-866. (Pubitemid 36776210)
31. Tang D, et al. (2010) Endogenous HMGB1 regulates autophagy. J Cell Biol 190(5): 881-892.
32. Tang D, Kang R, Livesey KM, Zeh HJ, 3rd, Lotze MT (2011) High mobility group box 1 (HMGB1) activates an autophagic response to oxidative stress. Antioxid Redox Signal 15(8):2185-2195.
33. Ohmori Y, Hamilton TA (2001) Requirement for STAT1 in LPS-induced gene expression in macrophages. J Leukoc Biol 69(4):598-604. (Pubitemid 32294845)
34. Pan PH, Cardinal J, Li ML, Hu CP, Tsung A (2013) Interferon regulatory factor-1 mediates the release of high mobility group box-1 in endotoxemia in mice. Chin Med J (Engl) 126(5):918-924.
35. Dhupar R, et al. (2011) Interferon regulatory factor 1 mediates acetylation and release of high mobility group box 1 from hepatocytes during murine liver ischemiareperfusion injury. Shock 35(3):293-301.
36. Wang S, et al. (1998) Murine caspase-11, an ICE-interacting protease, is essential for the activation of ICE. Cell 92(4):501-509. (Pubitemid 28101113)
37. Gross O, et al. (2009) Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459(7245):433-436.
38. Hsu LC, et al. (2011) IL-1β-driven neutrophilia preserves antibacterial defense in the absence of the kinase IKKβ. Nat Immunol 12(2):144-150.
39. Li W, et al. (2011) EGCG stimulates autophagy and reduces cytoplasmic HMGB1 levels in endotoxin-stimulated macrophages. Biochem Pharmacol 81(9):1152-1163.
40. Antoine DJ, et al. (2012) Molecular forms of HMGB1 and keratin-18 as mechanistic biomarkers for mode of cell death and prognosis during clinical acetaminophen hepatotoxicity. J Hepatol 56(5):1070-1079.
41. Yang H, et al. (2012) Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol Med 18:250-259.