The Janus face of HMGB1 in heart disease: a necessary update

Cellular and Molecular Life Sciences

Volumn 76, Issue 2, 2019, Pages 211-229

  Raucci, Angela ^a   Di Maggio, Stefania ^a   Scavello, Francesco ^a   D’Ambrosio, Alessandro ^a,d   Bianchi, Marco E ^b   Capogrossi, Maurizio C ^c,e  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c Ochsner Medical Center   (United States)

^d EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^e JOHNS HOPKINS BAYVIEW MEDICAL CENTER   (United States)

Author keywords

Alarmin; Biomarker; Inflammation; Oxidative stress; Regeneration

Indexed keywords

AMINO TERMINAL PRO BRAIN NATRIURETIC PEPTIDE; C REACTIVE PROTEIN; CHEMOKINE RECEPTOR CXCR4; GELATINASE B; HIGH MOBILITY GROUP B1 PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STROMAL CELL DERIVED FACTOR 1; TISSUE INHIBITOR OF METALLOPROTEINASE 3; ALARMIN; BIOLOGICAL MARKER;

ACETYLATION; ANGIOGENESIS; APOPTOSIS; AUTOPHAGY; AUTOPHOSPHORYLATION; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CARDIOMYOPATHY; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; EXTRACELLULAR TRAP; HEART DISEASE; HEART FAILURE; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART VENTRICLE HYPERTROPHY; HUMAN; INFLAMMATION; INFLAMMATORY CELL; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; MYOCARDITIS; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; METABOLISM; PATHOLOGY;

ALARMINS; ANIMALS; BIOMARKERS; HEART DISEASES; HMGB1 PROTEIN; HUMANS; MYOCARDIAL INFARCTION; MYOCARDITIS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 85055166071     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-018-2930-9     Document Type: Review

References (145)

1. Go AS, Mozaffarian D, Roger VL et al (2014) Heart disease and stroke statistics—2014 update: a report from the American Heart Association. Circulation 129(3):e28–e292. 10.1161/01.cir.0000441139.02102.80
2. Ahuja P, Sdek P, MacLellan WR (2007) Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 87(2):521–544. 10.1152/physrev.00032.2006
3. Bergmann O, Braun T (2016) Caught red-handed: cycling cardiomyocytes. Circ Res 118(1):3–5. 10.1161/CIRCRESAHA.115.307936
4. Frangogiannis NG (2014) The inflammatory response in myocardial injury, repair, and remodelling. Nat Rev Cardiol 11(5):255–265. 10.1038/nrcardio.2014.28
5. Bianchi ME, Agresti A (2005) HMG proteins: dynamic players in gene regulation and differentiation. Curr Opin Genet Dev 15(5):496–506. 10.1016/j.gde.2005.08.007
6. Celona B, Weiner A, Di Felice F et al (2011) Substantial histone reduction modulates genome wide nucleosomal occupancy and global transcriptional output. PLoS Biol 9(6):e1001086. 10.1371/journal.pbio.1001086
7. Liu Y, Prasad R, Wilson SH (2010) HMGB1: roles in base excision repair and related function. Biochim Biophys Acta 1799(1–2):119–130. 10.1016/j.bbagrm.2009.11.008
8. Harris HE, Raucci A (2006) Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep 7(8):774–778. 10.1038/sj.embor.7400759
9. Bianchi ME, Manfredi AA (2007) High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol Rev 220:35–46. 10.1111/j.1600-065x.2007.00574.x
10. Venereau E, Ceriotti C, Bianchi ME (2015) DAMPs from cell death to new life. Front Immunol 6:442. 10.3389/fimmu.2015.00422
11. Bonaldi T, Talamo F, Scaffidi P et al (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 22(20):5551–5560. 10.1093/emboj/cdg516
12. Tsung A, Tohme S, Billiar TR (2014) High-mobility group box-1 in sterile inflammation. J Intern Med 276(5):425–443. 10.1111/joim.12276
13. Venereau E, Casalgrandi M, Schiraldi M et al (2012) Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 209(9):1519–1528. 10.1084/jem.20120189
14. De Toma I, Rossetti G, Zambrano S et al (2014) Nucleosome loss facilitates the chemotactic response of macrophages. J Intern Med 276(5):454–469. 10.1111/joim.12286
15. Venereau E, De Leo F, Mezzapelle R et al (2016) HMGB1 as biomarker and drug target. Pharmacol Res 111:534–544. 10.1016/j.phrs.2016.06.031
16. Sessa L, Bianchi ME (2007) The evolution of High Mobility Group Box (HMGB) chromatin proteins in multicellular animals. Gene 387(1–2):133–140. 10.1016/j.gene.2006.08.034
17. Calogero S, Grassi F, Aguzzi A et al (1999) The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat Genet 22(3):276–280. 10.1038/10338
18. Lee G, Espirito Santo AI, Zwingenberger S et al (2018) Fully reduced HMGB1 accelerates the regeneration of multiple tissues by transitioning stem cells to GAlert. Proc Natl Acad Sci USA 115(19):E4463–E4472. 10.1073/pnas.1802893115
19. Bianchi ME, Falciola L, Ferrari S et al (1992) The DNA binding site of HMG1 protein is composed of two similar segments (HMG boxes), both of which have counterparts in other eukaryotic regulatory proteins. EMBO J 11(3):1055–1063
20. Rabadi MM, Xavier S, Vasko R et al (2015) High-mobility group box 1 is a novel deacetylation target of Sirtuin1. Kidney Int 87(1):95–108. 10.1038/ki.2014.217
21. Oh YJ, Youn JH, Ji Y et al (2009) HMGB1 is phosphorylated by classical protein kinase C and is secreted by a calcium-dependent mechanism. J Immunol 182(9):5800–5809. 10.4049/jimmunol.0801873
22. Zhang X, Wheeler D, Tang Y 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
23. Ito I, Fukazawa J, Yoshida M (2007) Post-translational methylation of high mobility group box 1 (HMGB1) causes its cytoplasmic localization in neutrophils. J Biol Chem 282(22):16336–16344. 10.1074/jbc.M608467200
24. Yang H, Lundback P, Ottosson L et al (2012) Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol Med 18:250. 10.2119/molmed.2011.00389
25. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81(1):1–5. 10.1189/jlb.0306164
26. Creagh EM, O’Neill LA (2006) TLRs, NLRs and RLRs: a trinity of pathogen sensors that co-operate in innate immunity. Trends Immunol 27(8):352–357. 10.1016/j.it.2006.06.003
27. Rovere-Querini P, Capobianco A, Scaffidi P et al (2004) HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 5(8):825–830. 10.1038/sj.embor.7400205
28. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418(6894):191–195. 10.1038/nature00858
29. Gardella S, Andrei C, Ferrera D et al (2002) The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 3(10):995–1001. 10.1093/embo-reports/kvf198
30. Wang H, Bloom O, Zhang M et al (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285(5425):248–251
31. Lu B, Antoine DJ, Kwan K et al (2014) JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc Natl Acad Sci USA 111(8):3068–3073. 10.1073/pnas.1316925111
32. Lu B, Nakamura T, Inouye K et al (2012) Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488(7413):670–674. 10.1038/nature11290
33. Yang S, Xu L, Yang T et al (2014) High-mobility group box-1 and its role in angiogenesis. J Leukoc Biol 95(4):563–574. 10.1189/jlb.0713412
34. Andersson U, Wang H, Palmblad K et al (2000) High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 192(4):565–570
35. Dumitriu IE, Bianchi ME, Bacci M et al (2007) The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leukoc Biol 81(1):84–91. 10.1189/jlb.0306171
36. Schiraldi M, Raucci A, Munoz LM et al (2012) HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med 209(3):551–563. 10.1084/jem.20111739
37. Treutiger CJ, Mullins GE, Johansson AS et al (2003) High mobility group 1 B-box mediates activation of human endothelium. J Intern Med 254(4):375–385
38. Andrassy M, Volz HC, Igwe JC et al (2008) High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 117(25):3216–3226. 10.1161/CIRCULATIONAHA.108.769331
39. Tsung A, Sahai R, Tanaka H et al (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201(7):1135–1143. 10.1084/jem.20042614
40. Wang WK, Lu QH, Zhang JN et al (2014) HMGB1 mediates hyperglycaemia-induced cardiomyocyte apoptosis via ERK/Ets-1 signalling pathway. J Cell Mol Med 18(11):2311–2320. 10.1111/jcmm.12399
41. Ulloa L, Batliwalla FM, Andersson U et al (2003) High mobility group box chromosomal protein 1 as a nuclear protein, cytokine, and potential therapeutic target in arthritis. Arthritis Rheum 48(4):876–881. 10.1002/art.10854
42. Maroso M, Balosso S, Ravizza T 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. 10.1038/nm.2127
43. De Mori R, Straino S, Di Carlo A et al (2007) Multiple effects of high mobility group box protein 1 in skeletal muscle regeneration. Arterioscler Thromb Vasc Biol 27(11):2377–2383. 10.1161/ATVBAHA.107.153429
44. Limana F, Germani A, Zacheo A et al (2005) Exogenous high-mobility group box 1 protein induces myocardial regeneration after infarction via enhanced cardiac C-kit + cell proliferation and differentiation. Circ Res 97(8):e73–e83. 10.1161/01.RES.0000186276.06104.04
45. Tirone M, Tran NL, Ceriotti C et al (2018) High mobility group box 1 orchestrates tissue regeneration via CXCR4. J Exp Med 215(1):303–318. 10.1084/jem.20160217
46. Vezzoli M, Castellani P, Corna G et al (2011) High-mobility group box 1 release and redox regulation accompany regeneration and remodeling of skeletal muscle. Antioxid Redox Signal 15(8):2161–2174. 10.1089/ars.2010.3341
47. Straino S, Di Carlo A, Mangoni A et al (2008) High-mobility group box 1 protein in human and murine skin: involvement in wound healing. J Invest Dermatol 128(6):1545–1553. 10.1038/sj.jid.5701212
48. Chavakis E, Hain A, Vinci M et al (2007) High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ Res 100(2):204–212. 10.1161/01.RES.0000257774.55970.f4
49. Meng E, Guo Z, Wang H et al (2008) High mobility group box 1 protein inhibits the proliferation of human mesenchymal stem cells and promotes their migration and differentiation along osteoblastic pathway. Stem Cells Dev 17(4):805–813. 10.1089/scd.2008.027610.1089/scd.2007.0276
50. Palumbo R, Sampaolesi M, De Marchis F et al (2004) Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J Cell Biol 164(3):441–449. 10.1083/jcb.200304135
51. Yang H, Hreggvidsdottir HS, Palmblad K 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. 10.1073/pnas.1003893107
52. Zhu L, Ren L, Chen Y et al (2015) Redox status of high-mobility group box 1 performs a dual role in angiogenesis of colorectal carcinoma. J Cell Mol Med 19(9):2128–2135. 10.1111/jcmm.12577
53. Di Maggio S, Milano G, De Marchis F et al (2017) Non-oxidizable HMGB1 induces cardiac fibroblasts migration via CXCR4 in a CXCL12-independent manner and worsens tissue remodeling after myocardial infarction. Biochim Biophys Acta. 10.1016/j.bbadis.2017.07.012
54. Maugeri N, Rovere-Querini P, Baldini M et al (2014) Oxidative stress elicits platelet/leukocyte inflammatory interactions via HMGB1: a candidate for microvessel injury in systemic sclerosis. Antioxid Redox Signal 20(7):1060–1074. 10.1089/ars.2013.5298
55. Fritz G (2011) RAGE: a single receptor fits multiple ligands. Trends Biochem Sci 36(12):625–632
56. Sessa L, Gatti E, Zeni F et al (2014) The receptor for advanced glycation end-products (RAGE) is only present in mammals, and belongs to a family of cell adhesion molecules (CAMs). PLoS One 9(1):e86903. 10.1371/journal.pone.0086903
57. Kierdorf K, Fritz G (2013) RAGE regulation and signaling in inflammation and beyond. J Leukoc Biol 94(1):55–68. 10.1189/jlb.1012519
58. Kang R, Chen R, Zhang Q et al (2014) HMGB1 in health and disease. Mol Aspects Med 40(1):116. 10.1016/j.mam.2014.05.001
59. Orlova VV, Choi EY, Xie C et al (2007) A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 26(4):1129–1139. 10.1038/sj.emboj.7601552
60. Penzo M, Molteni R, Suda T et al (2010) Inhibitor of NF-kappa B kinases alpha and beta are both essential for high mobility group box 1-mediated chemotaxis [corrected]. J Immunol 184(8):4497–4509. 10.4049/jimmunol.0903131
61. Raucci A, Cugusi S, Antonelli A et al (2008) A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 22(10):3716–3727. 10.1096/fj.08-109033
62. Stark K, Philippi V, Stockhausen S et al (2016) Disulfide HMGB1 derived from platelets coordinates venous thrombosis in mice. Blood 128(20):2435–2449. 10.1182/blood-2016-04-710632
63. Leifer CA, Medvedev AE (2016) Molecular mechanisms of regulation of Toll-like receptor signaling. J Leukoc Biol 100(5):927–941. 10.1189/jlb.2MR0316-117RR
64. Park JS, Svetkauskaite D, He Q et al (2004) Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279(9):7370–7377. 10.1074/jbc.M306793200
65. Conti L, Lanzardo S, Arigoni M et al (2013) The noninflammatory role of high mobility group box 1/Toll-like receptor 2 axis in the self-renewal of mammary cancer stem cells. FASEB J 27(12):4731–4744. 10.1096/fj.13-230201
66. Qiu Y, Yang J, Wang W et al (2014) HMGB1-promoted and TLR2/4-dependent NK cell maturation and activation take part in rotavirus-induced murine biliary atresia. PLoS Pathog 10(3):e1004011. 10.1371/journal.ppat.1004011
67. Urbonaviciute V, Furnrohr BG, Meister S 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. 10.1084/jem.20081165
68. Herzog C, Lorenz A, Gillmann HJ et al (2014) Thrombomodulin’s lectin-like domain reduces myocardial damage by interfering with HMGB1-mediated TLR2 signalling. Cardiovasc Res 101(3):400–410. 10.1093/cvr/cvt275
69. Mersmann J, Iskandar F, Latsch K, et al (2013) Attenuation of myocardial injury by HMGB1 blockade during ischemia/reperfusion is toll-like receptor 2-dependent. Mediators Inflamm 2013:174168. 10.1155/2013/174168
70. Mittal D, Saccheri F, Venereau E et al (2010) TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. EMBO J 29(13):2242–2252. 10.1038/emboj.2010.94
71. Yang Z, Deng Y, Su D et al (2013) TLR4 as receptor for HMGB1-mediated acute lung injury after liver ischemia/reperfusion injury. Lab Invest 93(7):792–800. 10.1038/labinvest.2013.66
72. Yao Y, Xu X, Zhang G et al (2012) Role of HMGB1 in doxorubicin-induced myocardial apoptosis and its regulation pathway. Basic Res Cardiol 107(3):267. 10.1007/s00395-012-0267-3
73. Yang H, Wang H, Ju Z et al (2015) MD-2 is required for disulfide HMGB1-dependent TLR4 signaling. J Exp Med 212(1):5–14. 10.1084/jem.20141318
74. He M, Bianchi ME, Coleman TR et al (2018) Exploring the biological functional mechanism of the HMGB1/TLR4/MD-2 complex by surface plasmon resonance. Mol Med 24(1):21. 10.1186/s10020-018-0023-8
75. Kim S, Kim SY, Pribis JP et al (2013) Signaling of high mobility group box 1 (HMGB1) through toll-like receptor 4 in macrophages requires CD14. Mol Med 19:88–98. 10.2119/molmed.2012.00306
76. Hummel S, Van Aken H, Zarbock A (2014) Inhibitors of CXC chemokine receptor type 4: putative therapeutic approaches in inflammatory diseases. Curr Opin Hematol 21(1):29–36. 10.1097/MOH.0000000000000002
77. Campana L, Bosurgi L, Bianchi ME et al (2009) Requirement of HMGB1 for stromal cell-derived factor-1/CXCL12-dependent migration of macrophages and dendritic cells. J Leukoc Biol 86(3):609–615. 10.1189/jlb.0908576
78. Aneja RK, Alcamo AM, Cummings J, et al (2018) Lack of benefit on brain edema, blood–brain barrier permeability, or cognitive outcome in global inducible high mobility group box 1 knockout mice despite tissue sparing after experimental traumatic brain injury. J Neurotrauma. 10.1089/neu.2018.5664
79. Huebener P, Gwak GY, Pradere JP et al (2014) High-mobility group box 1 is dispensable for autophagy, mitochondrial quality control, and organ function in vivo. Cell Metab 19(3):539–547. 10.1016/j.cmet.2014.01.014
80. Kitahara T, Takeishi Y, Harada M et al (2008) High-mobility group box 1 restores cardiac function after myocardial infarction in transgenic mice. Cardiovasc Res 80(1):40–46. 10.1093/cvr/cvn163
81. Ghigo A, Franco I, Morello F et al (2014) Myocyte signalling in leucocyte recruitment to the heart. Cardiovasc Res 102(2):270–280. 10.1093/cvr/cvu030
82. Kohno T, Anzai T, Naito K et al (2009) Role of high-mobility group box 1 protein in post-infarction healing process and left ventricular remodelling. Cardiovasc Res 81(3):565–573. 10.1093/cvr/cvn291
83. Nakamura Y, Suzuki S, Shimizu T et al (2015) High mobility group box 1 promotes angiogenesis from bone marrow-derived endothelial progenitor cells after myocardial infarction. J Atheroscler Thromb 22(6):570–581. 10.5551/jat.27235
84. Foglio E, Puddighinu G, Germani A et al (2016) HMGB1 Inhibits Apoptosis Following MI and Induces Autophagy via mTORC1 Inhibition. J Cell Physiol. 10.1002/jcp.25576
85. Limana F, Esposito G, Fasanaro P et al (2013) Transcriptional profiling of HMGB1-induced myocardial repair identifies a key role for Notch signaling. Mol Ther 21(10):1841–1851. 10.1038/mt.2013.137
86. Rossini A, Zacheo A, Mocini D et al (2008) HMGB1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J Mol Cell Cardiol 44(4):683–693. 10.1016/j.yjmcc.2008.01.009
87. Takahashi K, Fukushima S, Yamahara K et al (2008) Modulated inflammation by injection of high-mobility group box 1 recovers post-infarction chronically failing heart. Circulation 118(14 Suppl):S106–S114. 10.1161/CIRCULATIONAHA.107.757443
88. Limana F, Esposito G, D’Arcangelo D et al (2011) HMGB1 attenuates cardiac remodelling in the failing heart via enhanced cardiac regeneration and miR-206-mediated inhibition of TIMP-3. PLoS One 6(6):e19845. 10.1371/journal.pone.0019845
89. van Zuylen VL, den Haan MC, Geutskens SB et al (2015) Post-myocardial infarct inflammation and the potential role of cell therapy. Cardiovasc Drugs Ther 29(1):59–73. 10.1007/s10557-014-6568-z
90. Loukili N, Rosenblatt-Velin N, Li J et al (2011) Peroxynitrite induces HMGB1 release by cardiac cells in vitro and HMGB1 upregulation in the infarcted myocardium in vivo. Cardiovasc Res 89(3):586–594. 10.1093/cvr/cvq373
91. Oozawa S, Mori S, Kanke T et al (2008) Effects of HMGB1 on ischemia-reperfusion injury in the rat heart. Circ J 72(7):1178–1184
92. Xu H, Yao Y, Su Z et al (2011) Endogenous HMGB1 contributes to ischemia-reperfusion-induced myocardial apoptosis by potentiating the effect of TNF-α/JNK. Am J Physiol Heart Circ Physiol 300(3):H913–H921. 10.1152/ajpheart.00703.2010
93. Tian Y, Pan D, Chordia MD et al (2016) The spleen contributes importantly to myocardial infarct exacerbation during post-ischemic reperfusion in mice via signaling between cardiac HMGB1 and splenic RAGE. Basic Res Cardiol 111(6):62. 10.1007/s00395-016-0583-0
94. Ferdinandy P, Schulz R (2003) Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 138(4):532–543. 10.1038/sj.bjp.0705080
95. Diao H, Kang Z, Han F et al (2014) Astilbin protects diabetic rat heart against ischemia-reperfusion injury via blockade of HMGB1-dependent NF-kappaB signaling pathway. Food Chem Toxicol 63:104–110. 10.1016/j.fct.2013.10.045
96. Dong LY, Chen F, Xu M et al (2018) Quercetin attenuates myocardial ischemia-reperfusion injury via downregulation of the HMGB1-TLR4-NF-kappaB signaling pathway. Am J Transl Res 10(5):1273–1283
97. Hu X, Zhou X, He B et al (2010) Minocycline protects against myocardial ischemia and reperfusion injury by inhibiting high mobility group box 1 protein in rats. Eur J Pharmacol 638(1–3):84–89. 10.1016/j.ejphar.2010.03.059
98. Jiang WL, Zhang SP, Zhu HB et al (2012) Cardioprotection of Asperosaponin X on experimental myocardial ischemia injury. Int J Cardiol 155(3):430–436. 10.1016/j.ijcard.2011.06.010
99. Tong S, Zhang L, Joseph J et al (2018) Celastrol pretreatment attenuates rat myocardial ischemia/reperfusion injury by inhibiting high mobility group box 1 protein expression via the PI3 K/Akt pathway. Biochem Biophys Res Commun 497(3):843–849. 10.1016/j.bbrc.2018.02.121
100. Wang J, Hu X, Fu W et al (2014) Isoproterenolmediated heme oxygenase1 induction inhibits high mobility group box 1 protein release and protects against rat myocardial ischemia/reperfusion injury in vivo. Mol Med Rep 9(5):1863–1868. 10.3892/mmr.2014.2026
101. Wang N, Min X, Li D et al (2012) Geranylgeranylacetone protects against myocardial ischemia and reperfusion injury by inhibiting high-mobility group box 1 protein in rats. Mol Med Rep 5(2):521–524. 10.3892/mmr.2011.666
102. Wang XY, Dong WP, Bi SH et al (2013) Protective effects of osthole against myocardial ischemia/reperfusion injury in rats. Int J Mol Med 32(2):365–372. 10.3892/ijmm.2013.1386
103. Hu X, Jiang H, Cui B et al (2010) Preconditioning with high mobility group box 1 protein protects against myocardial ischemia-reperfusion injury. Int J Cardiol 145(1):111–112. 10.1016/j.ijcard.2009.05.057
104. Abeyama K, Stern DM, Ito Y et al (2005) The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 115(5):1267–1274. 10.1172/JCI22782
105. Abarbanell AM, Hartley JA, Herrmann JL et al (2011) Exogenous high-mobility group box 1 improves myocardial recovery after acute global ischemia/reperfusion injury. Surgery 149(3):329–335. 10.1016/j.surg.2010.07.002
106. van Berlo JH, Maillet M, Molkentin JD (2013) Signaling effectors underlying pathologic growth and remodeling of the heart. J Clin Invest 123(1):37–45. 10.1172/JCI62839
107. Jia Z, Xue R, Liu G, et al (2014) HMGB1 Is Involved in the Protective Effect of the PPAR alpha Agonist Fenofibrate against Cardiac Hypertrophy. PPAR Res 2014:541394. 10.1155/2014/541394
108. Lin H, Shen L, Zhang X et al (2016) HMGB1-RAGE axis makes no contribution to cardiac remodeling induced by pressure-overload. PLoS One 11(6):e0158514. 10.1371/journal.pone.0158514
109. Zhang L, Liu M, Jiang H et al (2016) Extracellular high-mobility group box 1 mediates pressure overload-induced cardiac hypertrophy and heart failure. J Cell Mol Med 20(3):459–470. 10.1111/jcmm.12743
110. Funayama A, Shishido T, Netsu S et al (2013) Cardiac nuclear high mobility group box 1 prevents the development of cardiac hypertrophy and heart failure. Cardiovasc Res 99(4):657–664. 10.1093/cvr/cvt128
111. Su FF, Shi MQ, Guo WG et al (2012) High-mobility group box 1 induces calcineurin-mediated cell hypertrophy in neonatal rat ventricular myocytes. Mediators Inflamm 2012:805149. 10.1155/2012/805149
112. Vejpongsa P, Yeh ET (2014) Prevention of anthracycline-induced cardiotoxicity: challenges and opportunities. J Am Coll Cardiol 64(9):938–945. 10.1016/j.jacc.2014.06.1167
113. Luo P, Zhu Y, Chen M et al (2018) HMGB1 contributes to adriamycin-induced cardiotoxicity via up-regulating autophagy. Toxicol Lett 292:115–122. 10.1016/j.toxlet.2018.04.034
114. Narumi T, Shishido T, Otaki Y et al (2015) High-mobility group box 1-mediated heat shock protein beta 1 expression attenuates mitochondrial dysfunction and apoptosis. J Mol Cell Cardiol 82:1–12. 10.1016/j.yjmcc.2015.02.018
115. Williams LJ, Nye BG, Wende AR (2017) Diabetes-related cardiac dysfunction. Endocrinol Metab (Seoul) 32(2):171–179. 10.3803/EnM.2017.32.2.171
116. Volz HC, Seidel C, Laohachewin D et al (2010) HMGB1: the missing link between diabetes mellitus and heart failure. Basic Res Cardiol 105(6):805–820. 10.1007/s00395-010-0114-3
117. Wang WK, Wang B, Lu QH et al (2014) Inhibition of high-mobility group box 1 improves myocardial fibrosis and dysfunction in diabetic cardiomyopathy. Int J Cardiol 172(1):202–212. 10.1016/j.ijcard.2014.01.011
118. Song J, Liu Q, Tang H et al (2016) Activation of PI3Kgamma/Akt pathway increases cardiomyocyte HMGB1 expression in diabetic environment. Oncotarget 7(49):80803–80810. 10.18632/oncotarget.13096
119. Tao A, Song J, Lan T et al (2015) Cardiomyocyte-fibroblast interaction contributes to diabetic cardiomyopathy in mice: Role of HMGB1/TLR4/IL-33 axis. Biochim Biophys Acta 1852(10 Pt A):2075–85. 10.1016/j.bbadis.2015.07.015
120. Wu H, Sheng ZQ, Xie J et al (2016) Reduced HMGB 1-mediated pathway and oxidative stress in resveratrol-treated diabetic mice: a possible mechanism of cardioprotection of resveratrol in diabetes mellitus. Oxid Med Cell Longev 2016:9836860. 10.1155/2016/9836860
121. Sanada S, Hakuno D, Higgins LJ et al (2007) IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J Clin Invest 117(6):1538–1549. 10.1172/JCI30634
122. Wu RN, Yu TY, Zhou JC et al (2018) Targeting HMGB1 ameliorates cardiac fibrosis through restoring TLR2-mediated autophagy suppression in myocardial fibroblasts. Int J Cardiol 267:156–162. 10.1016/j.ijcard.2018.04.103
123. Sagar S, Liu PP, Cooper LT Jr (2012) Myocarditis. Lancet 379(9817):738–747. 10.1016/S0140-6736(11)60648-X
124. Comarmond C, Cacoub P (2017) Myocarditis in auto-immune or auto-inflammatory diseases. Autoimmun Rev. 10.1016/j.autrev.2017.05.021
125. Su Z, Sun C, Zhou C et al (2011) HMGB1 blockade attenuates experimental autoimmune myocarditis and suppresses Th17-cell expansion. Eur J Immunol 41(12):3586–3595. 10.1002/eji.201141879
126. Su Z, Yin J, Wang T et al (2014) Up-regulated HMGB1 in EAM directly led to collagen deposition by a PKCbeta/Erk1/2-dependent pathway: cardiac fibroblast/myofibroblast might be another source of HMGB1. J Cell Mol Med 18(9):1740–1751. 10.1111/jcmm.12324
127. Bangert A, Andrassy M, Muller AM et al (2016) Critical role of RAGE and HMGB1 in inflammatory heart disease. Proc Natl Acad Sci USA 113(2):E155–E164. 10.1073/pnas.1522288113
128. Merx MW, Weber C (2007) Sepsis and the heart. Circulation 116(7):793–802. 10.1161/CIRCULATIONAHA.106.678359
129. Hagiwara S, Iwasaka H, Uchino T et al (2008) High mobility group box 1 induces a negative inotropic effect on the left ventricle in an isolated rat heart model of septic shock: a pilot study. Circ J 72(6):1012–1017
130. Xu H, Su Z, Wu J et al (2010) The alarmin cytokine, high mobility group box 1, is produced by viable cardiomyocytes and mediates the lipopolysaccharide-induced myocardial dysfunction via a TLR4/phosphatidylinositol 3-kinase gamma pathway. J Immunol 184(3):1492–1498. 10.4049/jimmunol.0902660
131. An R, Zhao L, Xi C et al (2016) Melatonin attenuates sepsis-induced cardiac dysfunction via a PI3 K/Akt-dependent mechanism. Basic Res Cardiol 111(1):8. 10.1007/s00395-015-0526-1
132. Li C, Hua F, Ha T et al (2012) Activation of myocardial phosphoinositide-3-kinase p110alpha ameliorates cardiac dysfunction and improves survival in polymicrobial sepsis. PLoS One 7(9):e44712. 10.1371/journal.pone.0044712
133. Andrassy M, Volz HC, Riedle N et al (2011) HMGB1 as a predictor of infarct transmurality and functional recovery in patients with myocardial infarction. J Intern Med 270(3):245–253. 10.1111/j.1365-2796.2011.02369.x
134. Cirillo P, Giallauria F, Pacileo M et al (2009) Increased high mobility group box-1 protein levels are associated with impaired cardiopulmonary and echocardiographic findings after acute myocardial infarction. J Card Fail 15(4):362–367. 10.1016/j.cardfail.2008.11.010
135. Giallauria F, Cirillo P, Lucci R et al (2010) Autonomic dysfunction is associated with high mobility group box-1 levels in patients after acute myocardial infarction. Atherosclerosis 208(1):280–284. 10.1016/j.atherosclerosis.2009.07.025
136. Goldstein RS, Gallowitsch-Puerta M, Yang L et al (2006) Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock 25(6):571–574. 10.1097/01.shk.0000209540.99176.72
137. Hashimoto T, Ishii J, Kitagawa F et al (2012) Circulating high-mobility group box 1 and cardiovascular mortality in unstable angina and non-ST-segment elevation myocardial infarction. Atherosclerosis 221(2):490–495. 10.1016/j.atherosclerosis.2012.01.040
138. Sorensen MV, Pedersen S, Mogelvang R et al (2011) Plasma high-mobility group box 1 levels predict mortality after ST-segment elevation myocardial infarction. JACC Cardiovasc Interv 4(3):281–286. 10.1016/j.jcin.2010.10.015
139. Wang LJ, Lu L, Zhang FR et al (2011) Increased serum high-mobility group box-1 and cleaved receptor for advanced glycation endproducts levels and decreased endogenous secretory receptor for advanced glycation endproducts levels in diabetic and non-diabetic patients with heart failure. Eur J Heart Fail 13(4):440–449. 10.1093/eurjhf/hfq231
140. Volz HC, Laohachewin D, Schellberg D et al (2012) HMGB1 is an independent predictor of death and heart transplantation in heart failure. Clin Res Cardiol 101(6):427–435. 10.1007/s00392-011-0409-x
141. Liu T, Zhang DY, Zhou YH et al (2015) Increased serum HMGB1 level may predict the fatal outcomes in patients with chronic heart failure. Int J Cardiol 184:318–320. 10.1016/j.ijcard.2015.02.088
142. Vandervelde S, van Amerongen MJ, Tio RA et al (2006) Increased inflammatory response and neovascularization in reperfused vs. non-reperfused murine myocardial infarction. Cardiovasc Pathol 15(2):83–90. 10.1016/j.carpath.2005.10.006
143. Zandarashvili L, Sahu D, Lee K et al (2013) Real-time kinetics of high-mobility group box 1 (HMGB1) oxidation in extracellular fluids studied by in situ protein NMR spectroscopy. J Biol Chem 288(17):11621–11627. 10.1074/jbc.M113.449942
144. Walker LE, Frigerio F, Ravizza T et al (2017) Molecular isoforms of high-mobility group box 1 are mechanistic biomarkers for epilepsy. J Clin Invest 127(6):2118–2132. 10.1172/JCI92001
145. Higo T, Naito AT, Sumida T, et al (2017) DNA single-strand break-induced DNA damage response causes heart failure. Nat Commun 8:15104. 10.1038/ncomms15104