High Mobility Group Box-1 (HMGB1): A Potential Target in Therapeutics

Author(s): Eyaldeva C. Vijayakumar, Lokesh Kumar Bhatt*, Kedar S. Prabhavalkar.

Journal Name: Current Drug Targets

Volume 20 , Issue 14 , 2019

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Graphical Abstract:


Abstract:

High mobility group box-1 (HMGB1) mainly belongs to the non-histone DNA-binding protein. It has been studied as a nuclear protein that is present in eukaryotic cells. From the HMG family, HMGB1 protein has been focused particularly for its pivotal role in several pathologies. HMGB-1 is considered as an essential facilitator in diseases such as sepsis, collagen disease, atherosclerosis, cancers, arthritis, acute lung injury, epilepsy, myocardial infarction, and local and systemic inflammation. Modulation of HMGB1 levels in the human body provides a way in the management of these diseases. Various strategies, such as HMGB1-receptor antagonists, inhibitors of its signalling pathway, antibodies, RNA inhibitors, vagus nerve stimulation etc. have been used to inhibit expression, release or activity of HMGB1. This review encompasses the role of HMGB1 in various pathologies and discusses its therapeutic potential in these pathologies.

Keywords: High mobility group box-1, cytokine mediator, inflammatory disease, cancer, sepsis, therapeutics.

[1]
Yanai H, Ban T, Taniguchi T. High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol 2012; 33(12): 633-40.
[http://dx.doi.org/10.1016/j.it.2012.10.005] [PMID: 23116548]
[2]
Ravizza T, Terrone G, Salamone A, et al. High Mobility Group Box 1 is a novel pathogenic factor and a mechanistic biomarker for epilepsy. Brain Behav Immun 2018; 72: 14-21.
[http://dx.doi.org/10.1016/j.bbi.2017.10.008] [PMID: 29031614]
[3]
Andersson U, Yang H, Harris H. High-mobility group box 1 protein (HMGB1) operates as an alarmin outside as well as inside cells. Semin Immunol 2018; 38: 40-8.
[http://dx.doi.org/10.1016/j.smim.2018.02.011] [PMID: 29530410]
[4]
Abdulahad DA, Westra J, Limburg PC, Kallenberg CGM, Bijl M. HMGB1 in systemic lupus Erythematosus: Its role in cutaneous lesions development. Autoimmun Rev 2010; 9(10): 661-5.
[http://dx.doi.org/10.1016/j.autrev.2010.05.015] [PMID: 20546955]
[5]
Ueno T, Ikeda T, Ikeda K, et al. HMGB-1 as a useful prognostic biomarker in sepsis-induced organ failure in patients undergoing PMX-DHP. J Surg Res 2011; 171(1): 183-90.
[http://dx.doi.org/10.1016/j.jss.2009.11.708] [PMID: 20338589]
[6]
Kumari T, Kumar B. High-mobility group box 1 protein (HMGB1) gene polymorphisms and cancer susceptibility: A comprehensive meta-analysis. Clin Chim Acta 2018; 483: 170-82.
[http://dx.doi.org/10.1016/j.cca.2018.04.042] [PMID: 29730397]
[7]
Shi Y, Guo X, Zhang J, Zhou H, Sun B, Feng J. DNA binding protein HMGB1 secreted by activated microglia promotes the apoptosis of hippocampal neurons in diabetes complicated with OSA. Brain Behav Immun 2018; 73: 482-92.
[http://dx.doi.org/10.1016/j.bbi.2018.06.012] [PMID: 29920330]
[8]
Wang J, Tochio N, Takeuchi A, et al. Redox-sensitive structural change in the A-domain of HMGB1 and its implication for the binding to cisplatin modified DNA. Biochem Biophys Res Commun 2013; 441(4): 701-6.
[http://dx.doi.org/10.1016/j.bbrc.2013.10.085] [PMID: 24427810]
[9]
Yang H, Antoine DJ, Andersson U, Tracey KJ. The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J Leukoc Biol 2013; 93(6): 865-73.
[http://dx.doi.org/10.1189/jlb.1212662] [PMID: 23446148]
[10]
Wang H, Bloom O, Zhang M, et al. HMG-1 as a late mediator of endotoxin lethality in mice published by: American Association for the Advancement of Science Stable URL http://www.jstor.org/stable/2898693
[11]
Hou C, Luan L, Ren C. Oxidized low-density lipoprotein promotes osteoclast differentiation from CD68 positive mononuclear cells by regulating HMGB1 release. Biochem Biophys Res Commun 2018; 495(1): 1356-62.
[http://dx.doi.org/10.1016/j.bbrc.2017.11.083] [PMID: 29146189]
[12]
Kigerl KA, Lai W, Wallace LM, Yang H, Popovich PG. High mobility group box-1 (HMGB1) is increased in injured mouse spinal cord and can elicit neurotoxic inflammation. Brain Behav Immun 2018; 72: 22-33.
[http://dx.doi.org/10.1016/j.bbi.2017.11.018] [PMID: 29175543]
[13]
Yan XX, Lu L, Peng WH, et al. Increased serum HMGB1 level is associated with coronary artery disease in nondiabetic and type 2 diabetic patients. Atherosclerosis 2009; 205(2): 544-8.
[http://dx.doi.org/10.1016/j.atherosclerosis.2008.12.016] [PMID: 19150066]
[14]
Yang R, Zhu S, Pischke SE, Haugaa H, Zou X, Tonnessen TI. Bile and circulating HMGB1 contributes to systemic inflammation in obstructive jaundice. J Surg Res 2018; 228: 14-9.
[http://dx.doi.org/10.1016/j.jss.2018.02.049] [PMID: 29907203]
[15]
Shang GH, Jia CQ, Tian H, et al. Serum high mobility group box protein 1 as a clinical marker for non-small cell lung cancer. Respir Med 2009; 103(12): 1949-53.
[http://dx.doi.org/10.1016/j.rmed.2009.05.019] [PMID: 19535236]
[16]
Zhu P, Xie L, Ding HS, et al. High mobility group box 1 and kidney diseases. (Review) Int J Mol Med 2013; 31(4): 763-8.
[http://dx.doi.org/10.3892/ijmm.2013.1286] [PMID: 23440289]
[17]
Qu Y, Zhan Y, Yang S, et al. Newcastle disease virus infection triggers HMGB1 release to promote the inflammatory response. Virology 2018; 525: 19-31.
[http://dx.doi.org/10.1016/j.virol.2018.09.001] [PMID: 30216776]
[18]
Lu B, Antoine DJ, Kwan K, et al. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc Natl Acad Sci USA 2014; 111(8): 3068-73.
[http://dx.doi.org/10.1073/pnas.1316925111] [PMID: 24469805]
[19]
Manuscript A, Mechanism M. NIH Public Access 2015; 10(6): 713-27.
[20]
Kang R, Livesey KM, Zeh HJ, Loze MT, Tang D. HMGB1: a novel Beclin 1-binding protein active in autophagy. Autophagy 2010; 6(8): 1209-11.
[http://dx.doi.org/10.4161/auto.6.8.13651] [PMID: 20935509]
[21]
Yanai H, Matsuda A, An J, et al. Conditional ablation of HMGB1 in mice reveals its protective function against endotoxemia and bacterial infection. Proc Natl Acad Sci USA 2013; 110(51): 20699-704.
[http://dx.doi.org/10.1073/pnas.1320808110] [PMID: 24302768]
[22]
Kang R, Zhang Q, Hou W, et al. Intracellular Hmgb1 inhibits inflammatory nucleosome release and limits acute pancreatitis in mice. Gastroenterology 2014; 146(4): 1097-107.
[http://dx.doi.org/10.1053/j.gastro.2013.12.015] [PMID: 24361123]
[23]
Huang H, Nace GW, McDonald KA, et al. Hepatocyte-specific high-mobility group box 1 deletion worsens the injury in liver ischemia/reperfusion: a role for intracellular high-mobility group box 1 in cellular protection. Hepatology 2014; 59(5): 1984-97.
[http://dx.doi.org/10.1002/hep.26976] [PMID: 24375466]
[24]
Yan H, Zhu L, Zhang Z, et al. HMGB1-RAGE signaling pathway in pPROM. Taiwan J Obstet Gynecol 2018; 57(2): 211-6.
[http://dx.doi.org/10.1016/j.tjog.2018.02.008] [PMID: 29673663]
[25]
Zhang X, Wheeler D, Tang Y, et al. Calcium/calmodulin-dependent protein kinase (CaMK) IV mediates nucleocytoplasmic shuttling and release of HMGB1 during lipopolysaccharide stimulation of macrophages. J Immunol 2008; 181(7): 5015-23.
[http://dx.doi.org/10.4049/jimmunol.181.7.5015] [PMID: 18802105]
[26]
Kayagaki N, Wong MT, Stowe IB, et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013; 341(6151): 1246-9.
[http://dx.doi.org/10.1126/science.1240248] [PMID: 23887873]
[27]
Lu B, Nakamura T, Inouye K, et al. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 2012; 488(7413): 670-4.
[http://dx.doi.org/10.1038/nature11290] [PMID: 22801494]
[28]
Lu B, Wang C, Wang M, et al. Molecular mechanism and therapeutic modulation of high mobility group box 1 release and action: an updated review. Expert Rev Clin Immunol 2014; 10(6): 713-27.
[http://dx.doi.org/10.1586/1744666X.2014.909730] [PMID: 24746113]
[29]
Venereau E, De Leo F, Mezzapelle R, Careccia G, Musco G, Bianchi ME. HMGB1 as biomarker and drug target. Pharmacol Res 2016; 111: 534-44.
[http://dx.doi.org/10.1016/j.phrs.2016.06.031] [PMID: 27378565]
[30]
Gong G, Yuan LB, Hu L, et al. Glycyrrhizin attenuates rat ischemic spinal cord injury by suppressing inflammatory cytokines and HMGB1. Acta Pharmacol Sin 2012; 33(1): 11-8.
[http://dx.doi.org/10.1038/aps.2011.151] [PMID: 22158106]
[31]
Zhou RR, Liu HB, Peng JP, et al. High mobility group box chromosomal protein 1 in acute-on-chronic liver failure patients and mice with ConA-induced acute liver injury. Exp Mol Pathol 2012; 93(2): 213-9.
[http://dx.doi.org/10.1016/j.yexmp.2012.05.006] [PMID: 22609241]
[32]
Antoine DJ, Dear JW, Lewis PS, et al. Mechanistic biomarkers provide early and sensitive detection of acetaminophen-induced acute liver injury at first presentation to hospital. Hepatology 2013; 58(2): 777-87.
[http://dx.doi.org/10.1002/hep.26294] [PMID: 23390034]
[33]
Seo YS, Kwon JH, Yaqoob U, et al. HMGB1 recruits hepatic stellate cells and liver endothelial cells to sites of ethanol-induced parenchymal cell injury. Am J Physiol Gastrointest Liver Physiol 2013; 305(11): G838-48.
[http://dx.doi.org/10.1152/ajpgi.00151.2013] [PMID: 24091596]
[34]
Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011; 29(1): 139-62.
[http://dx.doi.org/10.1146/annurev-immunol-030409-101323] [PMID: 21219181]
[35]
Vincent JL, Opal SM, Marshall JC, Tracey KJ. Sepsis definitions: time for change. Lancet 2013; 381(9868): 774-5.
[http://dx.doi.org/10.1016/S0140-6736(12)61815-7] [PMID: 23472921]
[36]
Thapa RJ, Nogusa S, Chen P, et al. Interferon-induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proc Natl Acad Sci USA 2013; 110(33): E3109-18.
[http://dx.doi.org/10.1073/pnas.1301218110] [PMID: 23898178]
[37]
Whilding LM, Archibald KM, Kulbe H, Balkwill FR, Öberg D, McNeish IA. Vaccinia virus induces programmed necrosis in ovarian cancer cells. Mol Ther 2013; 21(11): 2074-86.
[http://dx.doi.org/10.1038/mt.2013.195] [PMID: 23985697]
[38]
Günther C, Martini E, Wittkopf N, et al. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 2011; 477(7364): 335-9.
[http://dx.doi.org/10.1038/nature10400] [PMID: 21921917]
[39]
Qiang X, Yang WL, Wu R, et al. Cold-inducible RNA-binding protein (CIRP) triggers inflammatory responses in hemorrhagic shock and sepsis. Nat Med 2013; 19(11): 1489-95.
[http://dx.doi.org/10.1038/nm.3368] [PMID: 24097189]
[40]
Tian J, Avalos AM, Mao SY, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007; 8(5): 487-96.
[http://dx.doi.org/10.1038/ni1457] [PMID: 17417641]
[41]
Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 2007; 81(1): 59-66.
[http://dx.doi.org/10.1189/jlb.0306180] [PMID: 16966386]
[42]
Dumitriu IE, Bianchi ME, Bacci M, Manfredi AA, Rovere-Querini P. The secretion of HMGB1 is required for the migration of maturing dendritic cells. J Leukoc Biol 2007; 81(1): 84-91.
[http://dx.doi.org/10.1189/jlb.0306171] [PMID: 17035340]
[43]
Orlova VV, Choi EY, Xie C, et al. A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 2007; 26(4): 1129-39.
[http://dx.doi.org/10.1038/sj.emboj.7601552] [PMID: 17268551]
[44]
Degryse B, Bonaldi T, Scaffidi P, et al. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol 2001; 152(6): 1197-206.
[http://dx.doi.org/10.1083/jcb.152.6.1197] [PMID: 11257120]
[45]
Yu M, Wang H, Ding A, et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock [Internet] 2006; 26(2): 174-9.
[http://dx.doi.org/10.1097/01.shk.0000225404.51320.82] [PMID: 16878026]
[46]
Ivanov S, Dragoi AM, Wang X, et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007; 110(6): 1970-81.
[http://dx.doi.org/10.1182/blood-2006-09-044776] [PMID: 17548579]
[47]
Chen G-Y, Tang J, Zheng P, Liu Y. CD24 and siglec-10 selectively repress tissue damage-induced immune responses. Science 2009; 323(5922): 1722-5.
[http://dx.doi.org/10.1126/science.1168988]
[48]
Abeyama K, Stern DM, Ito Y, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 2005; 115(5): 1267-74.
[http://dx.doi.org/10.1172/JCI22782] [PMID: 15841214]
[49]
Salmivirta M, Rauvala H, Elenius K, Jalkanen M. Neurite growth-promoting protein (amphoterin, p30) binds syndecan. Exp Cell Res 1992; 200(2): 444-51.
[http://dx.doi.org/10.1016/0014-4827(92)90194-D] [PMID: 1369684]
[50]
Fiuza C, Bustin M, Talwar S, et al. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood [Internet] 2003; 101(7): 2652-60.
[http://dx.doi.org/ [http://10.1182/blood-2002-05-1300] [PMID: 12456506]
[51]
Zhu S, Ashok M, Li J, et al. Spermine protects mice against lethal sepsis partly by attenuating surrogate inflammatory markers. Mol Med 2009; 15(7-8): 275-82.
[http://dx.doi.org/10.2119/molmed.2009.00062]
[52]
Antoine DJ, Harris HE, Andersson U, Tracey KJ, Bianchi ME. A systematic nomenclature for the redox states of high mobility group box (HMGB) proteins. Mol Med 2014; Mar 24 [cited 2018 Oct 11]. 20(1): 135-7..
[53]
Schiraldi M, Raucci A, Muñoz LM, et al. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4. J Exp Med 2012; 209(3): 551-63.
[http://dx.doi.org/10.1084/jem.20111739] [PMID: 22370717]
[54]
Venereau E, Casalgrandi M, Schiraldi M, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 2012; 209(9): 1519-28.
[http://dx.doi.org/10.1084/jem.20120189] [PMID: 22869893]
[55]
Yang H, Lundbäck P, Ottosson L, et al. Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol Med 2012; 18(2): 250-9.
[http://dx.doi.org/10.2119/molmed.2011.00389] [PMID: 22105604]
[56]
Nyström S, Antoine DJ, Lundbäck P, et al. TLR activation regulates damage-associated molecular pattern isoforms released during pyroptosis. EMBO J 2013; 32(1): 86-99.
[http://dx.doi.org/10.1038/emboj.2012.328] [PMID: 23222484]
[57]
Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469(7329): 221-5.
[http://dx.doi.org/10.1038/nature09663] [PMID: 21124315]
[58]
Allen IC, Scull MA, Moore CB, et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009; 30(4): 556-65.
[http://dx.doi.org/10.1016/j.immuni.2009.02.005] [PMID: 19362020]
[59]
Miao EA, Leaf IA, Treuting PM, et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 2010; 11(12): 1136-42.
[http://dx.doi.org/10.1038/ni.1960] [PMID: 21057511]
[60]
Yamada S, Yakabe K, Ishii J, Imaizumi H, Maruyama I. New high mobility group box 1 assay system. Clin Chim Acta 2006; 372(1-2): 173-8.
[http://dx.doi.org/10.1016/j.cca.2006.04.016] [PMID: 16797518]
[61]
Ilmakunnas M, Tukiainen EM, Rouhiainen A, et al. High mobility group box 1 protein as a marker of hepatocellular injury in human liver transplantation. Liver Transpl 2008; 14(10): 1517-25.
[http://dx.doi.org/10.1002/lt.21573] [PMID: 18825712]
[62]
Müller S, Scaffidi P, Degryse B, et al. New EMBO members’ review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J 2001; 20(16): 4337-40.
[http://dx.doi.org/10.1093/emboj/20.16.4337] [PMID: 11500360]
[63]
Urbonaviciute V, Fürnrohr BG, Weber C, et al. Factors masking HMGB1 in human serum and plasma. J Leukoc Biol 2007; 81(1): 67-74.
[http://dx.doi.org/10.1189/jlb.0306196] [PMID: 17060363]
[64]
af Klint E, Grundtman C, Engström M, et al. Intraarticular glucocorticoid treatment reduces inflammation in synovial cell infiltrations more efficiently than in synovial blood vessels. Arthritis Rheum 2005; 52(12): 3880-9.
[http://dx.doi.org/10.1002/art.21488] [PMID: 16320336]
[65]
Barkauskaite V, Ek M, Popovic K, et al. Translocation of the novel cytokine HMGB1 to the cytoplasm and extracellular space coincides with the peak of clinical activity in experimentally UV-induced lesions of cutaneous lupus erythematosus. Lupus 2007; 16(10): 794-802.
[http://dx.doi.org/10.1177/0961203307081895] [PMID: 17895302]
[66]
Kostova N, Zlateva S, Ugrinova I, Pasheva E. The expression of HMGB1 protein and its receptor RAGE in human malignant tumors. Mol Cell Biochem 2010; 337(1-2): 251-8.
[http://dx.doi.org/10.1007/s11010-009-0305-0] [PMID: 19876719]
[67]
Ek M, Popovic K, Harris HE, Nauclér CS, Wahren-Herlenius M. Increased extracellular levels of the novel proinflammatory cytokine high mobility group box chromosomal protein 1 in minor salivary glands of patients with Sjögren’s syndrome. Arthritis Rheum 2006; 54(7): 2289-94.
[http://dx.doi.org/10.1002/art.21969] [PMID: 16802368]
[68]
Ulfgren A-K, Grundtman C, Borg K, et al. Down-regulation of the aberrant expression of the inflammation mediator high mobility group box chromosomal protein 1 in muscle tissue of patients with polymyositis and dermatomyositis treated with corticosteroids. Arthritis Rheum 2004; 50(5): 1586-94.
[http://dx.doi.org/10.1002/art.20220] [PMID: 15146429]
[69]
Abdulahad DA, Westra J, Bijzet J, et al. High mobility group box 1 (HMGB1) and anti-HMGB1 antibodies and their relation to disease characteristics in systemic lupus erythematosus. Arthritis Res Ther 2011; 13(3): R71.
[http://dx.doi.org/10.1186/ar3332] [PMID: 21548924]
[70]
Wang H, Zhu S, Zhou R, Li W, Sama AE. Therapeutic potential of HMGB1-targeting agents in sepsis. Expert Rev Mol Med 2008.10e32.
[http://dx.doi.org/10.1017/S1462399408000884] [PMID: 18980707]
[71]
Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998; 282(5396): 2085-8.
[http://dx.doi.org/10.1126/science.282.5396.2085] [PMID: 9851930]
[72]
Nagai Y, Akashi S, Nagafuku M, et al. Essential role of MD-2 in LPS responsiveness and TLR4 distribution. Nat Immunol 2002; 3(7): 667-72.
[http://dx.doi.org/10.1038/ni809] [PMID: 12055629]
[73]
Kim S, Kim SY, Pribis JP, et al. Signaling of high mobility group box 1 (HMGB1) through toll-like receptor 4 in macrophages requires CD14. Mol Med 2013; 19(1): 88-98.
[http://dx.doi.org/10.2119/molmed.2012.00306] [PMID: 23508573]
[74]
Hsu LC, Enzler T, Seita J, et al. IL-1β-driven neutrophilia preserves antibacterial defense in the absence of the kinase IKKβ. Nat Immunol 2011; 12(2): 144-50.
[http://dx.doi.org/10.1038/ni.1976] [PMID: 21170027]
[75]
Wang H, Bloom O, Zhang M, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285(5425): 248-51.
[http://dx.doi.org/10.1126/science.285.5425.248] [PMID: 10398600]
[76]
Yang H, Ochani M, Li J, et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc Natl Acad Sci USA 2004; 101(1): 296-301.
[http://dx.doi.org/10.1073/pnas.2434651100] [PMID: 14695889]
[77]
Yang H, Wang H, Czura CJ, Tracey KJ. The cytokine activity of HMGB1. J Leukoc Biol 2005; 78(1): 1-8.
[http://dx.doi.org/10.1189/jlb.1104648] [PMID: 15734795]
[78]
Wang H, Yang H, Czura CJ, Sama AE, Tracey KJ. HMGB1 as a late mediator of lethal systemic inflammation. Am J Respir Crit Care Med 2001; 164(10 Pt 1): 1768-73.
[http://dx.doi.org/10.1164/ajrccm.164.10.2106117] [PMID: 11734424]
[79]
Ye C, Choi J-G, Abraham S, et al. Human macrophage and dendritic cell-specific silencing of high-mobility group protein B1 ameliorates sepsis in a humanized mouse model. Proc Natl Acad Sci USA 2012; 109(51): 21052-7.
[http://dx.doi.org/10.1073/pnas.1216195109] [PMID: 23213216]
[80]
Taniguchi N, Kawahara K, Yone K, et al. High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum 2003; 48(4): 971-81.
[http://dx.doi.org/10.1002/art.10859] [PMID: 12687539]
[81]
Kokkola R, Sundberg E, Ulfgren AK, et al. High mobility group box chromosomal protein 1: a novel proinflammatory mediator in synovitis. Arthritis Rheum 2002; 46(10): 2598-603.
[http://dx.doi.org/10.1002/art.10540] [PMID: 12384917]
[82]
Pullerits R, Jonsson I-M, Verdrengh M, et al. High mobility group box chromosomal protein 1, a DNA binding cytokine, induces arthritis. Arthritis Rheum 2003; 48(6): 1693-700.
[http://dx.doi.org/10.1002/art.11028] [PMID: 12794838]
[83]
Wen Z, Xu L, Chen X, et al. Autoantibody induction by DNA-containing immune complexes requires HMGB1 with the TLR2/microRNA-155 pathway. J Immunol 2013; 190(11): 5411-22.
[http://dx.doi.org/10.4049/jimmunol.1203301] [PMID: 23616573]
[84]
Ohnishi M, Katsuki H, Fukutomi C, et al. HMGB1 inhibitor glycyrrhizin attenuates intracerebral hemorrhage-induced injury in rats. Neuropharmacology 2011; 61(5-6): 975-80.
[http://dx.doi.org/10.1016/j.neuropharm.2011.06.026] [PMID: 21752338]
[85]
Lu M, Yu S, Xu W, Gao B, Xiong S. HMGB1 Promotes Systemic Lupus Erythematosus by Enhancing Macrophage Inflammatory Response. J Immunol Res 2015; 2015946748
[http://dx.doi.org/10.1155/2015/946748] [PMID: 26078984]
[86]
Lamkanfi M, Sarkar A, Vande Walle L, et al. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J Immunol 2010; 185(7): 4385-92.
[http://dx.doi.org/10.4049/jimmunol.1000803] [PMID: 20802146]
[87]
Singh V, Roth S, Veltkamp R, Liesz A. HMGB1 as a Key Mediator of Immune Mechanisms in Ischemic Stroke. Antioxid Redox Signal 2016; 24(12): 635-51.
[http://dx.doi.org/10.1089/ars.2015.6397] [PMID: 26493086]
[88]
Yang QW, Lu FL, Zhou Y, et al. HMBG1 mediates ischemia-reperfusion injury by TRIF-adaptor independent Toll-like receptor 4 signaling. J Cereb Blood Flow Metab 2011; 31(2): 593-605.
[http://dx.doi.org/10.1038/jcbfm.2010.129] [PMID: 20700129]
[89]
Liesz A, Dalpke A, Mracsko E, et al. DAMP signaling is a key pathway inducing immune modulation after brain injury. J Neurosci 2015; 35(2): 583-98.
[http://dx.doi.org/10.1523/JNEUROSCI.2439-14.2015] [PMID: 25589753]
[90]
Muhammad S, Barakat W, Stoyanov S, et al. The HMGB1 receptor RAGE mediates ischemic brain damage. J Neurosci 2008; 28(46): 12023-31.
[http://dx.doi.org/10.1523/JNEUROSCI.2435-08.2008] [PMID: 19005067]
[91]
de Souza AWS, Westra J, Limburg PC, Bijl M, Kallenberg CGM. HMGB1 in vascular diseases: Its role in vascular inflammation and atherosclerosis. Autoimmun Rev 2012; 11(12): 909-17.
[http://dx.doi.org/10.1016/j.autrev.2012.03.007] [PMID: 22495229]
[92]
Assad OM, Aly Labib DA, Ahmed Rashed L. Dexmedetomidine protects against myocardial ischaemia/reperfusion-induced renal damage in rats. Egypt J Anaesth 2018; 34(1): 33-9.
[http://dx.doi.org/10.1016/j.egja.2017.09.005]
[93]
Di Maggio S, Milano G, De Marchis F, et al. Non-oxidizable HMGB1 induces cardiac fibroblasts migration via CXCR4 in a CXCL12-independent manner and worsens tissue remodeling after myocardial infarction. Biochim Biophys Acta Mol Basis Dis 2017; 1863(11): 2693-704.
[http://dx.doi.org/10.1016/j.bbadis.2017.07.012] [PMID: 28716707]
[94]
Soh S, Jun JH, Song JW, et al. Ethyl pyruvate attenuates myocardial ischemia-reperfusion injury exacerbated by hyperglycemia via retained inhibitory effect on HMGB1. Int J Cardiol 2018; 252: 156-62.
[http://dx.doi.org/10.1016/j.ijcard.2017.11.038] [PMID: 29169909]
[95]
Schlueter C, Weber H, Meyer B, et al. Angiogenetic signaling through hypoxia: HMGB1: an angiogenetic switch molecule. Am J Pathol 2005; 166(4): 1259-63.
[http://dx.doi.org/10.1016/S0002-9440(10)62344-9] [PMID: 15793304]
[96]
Mitola S, Belleri M, Urbinati C, et al. Cutting edge: extracellular high mobility group box-1 protein is a proangiogenic cytokine. J Immunol 2006; 176(1): 12-5.
[http://dx.doi.org/10.4049/jimmunol.176.1.12] [PMID: 16365390]
[97]
Chavakis E, Hain A, Vinci M, et al. High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ Res 2007; 100(2): 204-12.
[http://dx.doi.org/10.1161/01.RES.0000257774.55970.f4] [PMID: 17218606]
[98]
Tzeng H-P, Fan J, Vallejo JG, et al. Negative inotropic effects of high-mobility group box 1 protein in isolated contracting cardiac myocytes. Am J Physiol Heart Circ Physiol 2008; 294(3): H1490-6.
[http://dx.doi.org/10.1152/ajpheart.00910.2007] [PMID: 18223193]
[99]
Hagiwara S, Iwasaka H, Uchino T, Noguchi T. 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 2008; 72(6): 1012-7.
[http://dx.doi.org/10.1253/circj.72.1012] [PMID: 18503231]
[100]
Andrassy M, Volz HC, Igwe JC, et al. High-mobility group box-1 in ischemia-reperfusion injury of the heart. Circulation 2008; 117(25): 3216-26.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.769331] [PMID: 18574060]
[101]
Ito T, Kawahara K, Nakamura T, et al. High-mobility group box 1 protein promotes development of microvascular thrombosis in rats. J Thromb Haemost 2007; 5(1): 109-16.
[http://dx.doi.org/10.1111/j.1538-7836.2006.02255.x] [PMID: 17239166]
[102]
Cirillo P, Giallauria F, Pacileo M, et al. Increased high mobility group box-1 protein levels are associated with impaired cardiopulmonary and echocardiographic findings after acute myocardial infarction. J Card Fail 2009; 15(4): 362-7.
[http://dx.doi.org/10.1016/j.cardfail.2008.11.010] [PMID: 19398086]
[103]
Maekawa Y, Anzai T, Yoshikawa T, et al. Effect of granulocyte-macrophage colony-stimulating factor inducer on left ventricular remodeling after acute myocardial infarction. J Am Coll Cardiol 2004; 44(7): 1510-20.
[http://dx.doi.org/10.1016/j.jacc.2004.05.083] [PMID: 15464336]
[104]
Maekawa Y, Anzai T, Yoshikawa T, et al. Prognostic significance of peripheral monocytosis after reperfused acute myocardial infarction:a possible role for left ventricular remodeling. J Am Coll Cardiol 2002; 39(2): 241-6.
[http://dx.doi.org/10.1016/S0735-1097(01)01721-1] [PMID: 11788214]
[105]
Sun M, Dawood F, Wen WH, et al. Excessive tumor necrosis factor activation after infarction contributes to susceptibility of myocardial rupture and left ventricular dysfunction. Circulation 2004; 110(20): 3221-8.
[http://dx.doi.org/10.1161/01.CIR.0000147233.10318.23] [PMID: 15533863]
[106]
Nian M, Lee P, Khaper N, Liu P. Inflammatory cytokines and postmyocardial infarction remodeling. Circ Res 2004; 94(12): 1543-53.
[http://dx.doi.org/10.1161/01.RES.0000130526.20854.fa] [PMID: 15217919]
[107]
Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res 2002; 53(1): 31-47.
[http://dx.doi.org/10.1016/S0008-6363(01)00434-5] [PMID: 11744011]
[108]
Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005; 201(7): 1135-43.
[http://dx.doi.org/10.1084/jem.20042614] [PMID: 15795240]
[109]
Kim J-B, Sig Choi J, Yu Y-M, et al. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 2006; 26(24): 6413-21.
[http://dx.doi.org/10.1523/JNEUROSCI.3815-05.2006] [PMID: 16775128]
[110]
Andersson U, Wang H, Palmblad K, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000; 192(4): 565-70.
[http://dx.doi.org/10.1084/jem.192.4.565] [PMID: 10952726]
[111]
Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5(4): 331-42.
[http://dx.doi.org/10.1038/nri1594] [PMID: 15803152]
[112]
Kohno T, Anzai T, Naito K, et al. Role of high-mobility group box 1 protein in post-infarction healing process and left ventricular remodelling. Cardiovasc Res 2009; 81(3): 565-73.
[http://dx.doi.org/10.1093/cvr/cvn291] [PMID: 18984601]
[113]
Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448(7152): 427-34.
[http://dx.doi.org/10.1038/nature06005] [PMID: 17653185]
[114]
Guo X, Guo R, Luo X, Zhou L. Ethyl pyruvate ameliorates experimental colitis in mice by inhibiting the HMGB1-Th17 and Th1/Tc1 responses. Int Immunopharmacol 2015; 29(2): 454-61.
[http://dx.doi.org/10.1016/j.intimp.2015.10.015] [PMID: 26541861]
[115]
Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6(11): 1133-41.
[http://dx.doi.org/10.1038/ni1261] [PMID: 16200068]
[116]
van Bruggen N, Ouyang W. Th17 cells at the crossroads of autoimmunity, inflammation, and atherosclerosis. Immunity 2014; 40(1): 10-2.
[http://dx.doi.org/10.1016/j.immuni.2013.12.006] [PMID: 24439264]
[117]
Su Z, Sun C, Zhou C, et al. HMGB1 blockade attenuates experimental autoimmune myocarditis and suppresses Th17-cell expansion. Eur J Immunol[Internet] 2011; 41(12): 3586-95.
[http://dx.doi.org/10.1002/eji.201141879] [PMID: 21928275]
[118]
Vénéreau E, Ceriotti C, Bianchi ME. DAMPs from cell death to new life. Front Immunol 2015; 6: 422.
[http://dx.doi.org/10.3389/fimmu.2015.00422] [PMID: 26347745]
[119]
Kaneko Y, Pappas C, Malapira T, et al. Extracellular hmgb1 modulates glutamate metabolism associated with kainic acid-induced epilepsy-like hyperactivity in primary rat neural cells. Cell Physiol Biochem 2017; 41(3): 947-59.
[http://dx.doi.org/10.1159/000460513] [PMID: 28222432]
[120]
Fu L, Liu K, Wake H, et al. Therapeutic effects of anti-HMGB1 monoclonal antibody on pilocarpine-induced status epilepticus in mice. Sci Rep 2017; 7(1): 1179.
[http://dx.doi.org/10.1038/s41598-017-01325-y] [PMID: 28446773]
[121]
Parker TM, Nguyen AH, Rabang JR, Patil AA, Agrawal DK. The danger zone: Systematic review of the role of HMGB1 danger signalling in traumatic brain injury. Brain Inj 2017; 31(1): 2-8.
[http://dx.doi.org/10.1080/02699052.2016.1217045] [PMID: 27819487]
[122]
Ravizza T, Terrone G, Salamone A, et al. High Mobility Group Box 1 is a novel pathogenic factor and a mechanistic biomarker for epilepsy. Brain Behav Immun 2018; 72: 14-21.
[http://dx.doi.org/10.1016/j.bbi.2017.10.008] [PMID: 29031614]
[123]
Wang D, Liu K, Wake H, Teshigawara K, Mori S, Nishibori M. Anti-high mobility group box-1 (HMGB1) antibody inhibits hemorrhage-induced brain injury and improved neurological deficits in rats. Sci Rep 2017; 7: 46243.
[http://dx.doi.org/10.1038/srep46243] [PMID: 28393932]
[124]
Zhao J, Wang Y, Xu C, et al. Therapeutic potential of an anti-high mobility group box-1 monoclonal antibody in epilepsy. Brain Behav Immun 2017; 64: 308-19.
[http://dx.doi.org/10.1016/j.bbi.2017.02.002] [PMID: 28167116]
[125]
Pauletti A, Terrone G, Shekh-Ahmad T, et al. Targeting oxidative stress improves disease outcomes in a rat model of acquired epilepsy. Brain 2017; 140(7): 1885-99.
[http://dx.doi.org/10.1093/brain/awx117] [PMID: 28575153]
[126]
Maroso M, Balosso S, Ravizza T, et al. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat Med 2010; 16(4): 413-9.
[http://dx.doi.org/10.1038/nm.2127] [PMID: 20348922]
[127]
Kang R, Zhang Q, Zeh HJ III, Lotze MT, Tang D. HMGB1 in cancer: good, bad, or both? Clin Cancer Res 2013; 19(15): 4046-57.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-0495] [PMID: 23723299]
[128]
Wei F, Yang F, Li J, et al. Soluble Toll-like receptor 4 is a potential serum biomarker in non-small cell lung cancer. Oncotarget 2016; 7(26): 40106-14.
[http://dx.doi.org/10.18632/oncotarget.9496] [PMID: 27223258]
[129]
Jakubowska K, Naumnik W, Niklińska W, Chyczewska E. Clinical Significance of HMGB-1 and TGF-β Level in Serum and BALF of Advanced Non-Small Cell Lung CancerIn 2015; 49-58..
[http://dx.doi.org/10.1007/5584_2015_115]
[130]
Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care 2010; 33(4): 861-8.
[http://dx.doi.org/10.2337/dc09-1799] [PMID: 20067962]
[131]
Lin E, Freedman JE, Beaulieu LM. Innate immunity and toll-like receptor antagonists: a potential role in the treatment of cardiovascular diseases. Cardiovasc Ther 2009; 27(2): 117-23.
[http://dx.doi.org/10.1111/j.1755-5922.2009.00077.x] [PMID: 19426249]
[132]
Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011; 18(4): 571-80.
[http://dx.doi.org/10.1038/cdd.2010.191] [PMID: 21311563]
[133]
Xiao P, Liu WL. MiR-142-3p functions as a potential tumor suppressor directly targeting HMGB1 in non-small-cell lung carcinoma. Int J Clin Exp Pathol 2015; 8(9): 10800-7.
[PMID: 26617792]
[134]
Zhu J, Luo J, Li Y, et al. HMGB1 induces human non-small cell lung cancer cell motility by activating integrin αvβ3/FAK through TLR4/NF-κB signaling pathway. Biochem Biophys Res Commun 2016; 480(4): 522-7.
[http://dx.doi.org/10.1016/j.bbrc.2016.10.052] [PMID: 27769864]
[135]
Stordal B, Davey M. Understanding cisplatin resistance using cellular models. IUBMB Life 2007; 59(11): 696-9.
[http://dx.doi.org/10.1080/15216540701636287] [PMID: 17885832]
[136]
Amann R, Peskar BA. Anti-inflammatory effects of aspirin and sodium salicylate. Eur J Pharmacol 2002; 447(1): 1-9.
[http://dx.doi.org/10.1016/S0014-2999(02)01828-9] [PMID: 12106797]
[137]
Farahat M, Sharaf M, Attia T. The serum high-mobility group box 1 level and RAGE expression in childhood acute lymphoblastic leukemic patients′. Egypt J Haematol 2015; 40(2): 60.
[http://dx.doi.org/10.4103/1110-1067.161290]
[138]
Yu Y, Xie M, Kang R, Livesey KM, Cao L, Tang D. HMGB1 is a therapeutic target for leukemia. Am J Blood Res 2012; 2(1): 36-43.
[PMID: 22432086]
[139]
Yang L, Yu Y, Kang R, et al. Up-regulated autophagy by endogenous high mobility group box-1 promotes chemoresistance in leukemia cells. Leuk Lymphoma 2012; 53(2): 315-22.
[http://dx.doi.org/10.3109/10428194.2011.616962] [PMID: 21864037]
[140]
Yan J, Ying S, Cai X. MicroRNA-Mediated Regulation of HMGB1 in Human Hepatocellular Carcinoma. BioMed Res Int 2018; 20182754941
[http://dx.doi.org/10.1155/2018/2754941] [PMID: 29651425]
[141]
Perra A, Kowalik MA, Ghiso E, et al. YAP activation is an early event and a potential therapeutic target in liver cancer development. J Hepatol 2014; 61(5): 1088-96.
[http://dx.doi.org/10.1016/j.jhep.2014.06.033] [PMID: 25010260]
[142]
Wang J, Ma L, Weng W, et al. Mutual interaction between YAP and CREB promotes tumorigenesis in liver cancer. Hepatology 2013; 58(3): 1011-20.
[http://dx.doi.org/10.1002/hep.26420] [PMID: 23532963]
[143]
Chen R, Zhu S, Fan X-G, et al. High mobility group protein B1 controls liver cancer initiation through yes-associated protein -dependent aerobic glycolysis. Hepatology 2018; 67(5): 1823-41.
[http://dx.doi.org/10.1002/hep.29663] [PMID: 29149457]
[144]
Zhang J, Kou YB, Zhu JS, Chen WX, Li S. Knockdown of HMGB1 inhibits growth and invasion of gastric cancer cells through the NF-κB pathway in vitro and in vivo. Int J Oncol 2014; 44(4): 1268-76.
[http://dx.doi.org/10.3892/ijo.2014.2285] [PMID: 24481712]
[145]
Sun KK, Ji C, Li X, et al. Overexpression of high mobility group protein B1 correlates with the proliferation and metastasis of lung adenocarcinoma cells. Mol Med Rep 2013; 7(5): 1678-82.
[http://dx.doi.org/10.3892/mmr.2013.1362] [PMID: 23467607]
[146]
Pang X, Zhang Y, Wei H, et al. Expression and effects of high-mobility group box 1 in cervical cancer. Int J Mol Sci 2014; 15(5): 8699-712.
[http://dx.doi.org/10.3390/ijms15058699] [PMID: 24837834]
[147]
Ohara K, Tanaka Y, Tsunoda H, et al. Assessment of cervical cancer radioresponse by serum squamous cell carcinoma antigen and magnetic resonance imaging. Obstet Gynecol 2002; 100(4): 781-7.
[PMID: 12383549]
[148]
Gaarenstroom KN, Kenter GG, Bonfrer JMG, et al. Can initial serum cyfra 21-1, SCC antigen, and TPA levels in squamous cell cervical cancer predict lymph node metastases or prognosis? Gynecol Oncol 2000; 77(1): 164-70.
[http://dx.doi.org/10.1006/gyno.2000.5732] [PMID: 10739706]
[149]
Madan RA, Arlen PM. Recent advances revolutionize treatment of metastatic prostate cancer. Future Oncol 2013; 9(8): 1133-44.
[http://dx.doi.org/10.2217/fon.13.65] [PMID: 23902245]
[150]
Lonergan PE, Tindall DJ. Androgen receptor signaling in prostate cancer development and progression. J Carcinog 2011; 10: 20.
[http://dx.doi.org/10.4103/1477-3163.83937] [PMID: 21886458]
[151]
Zhang YX, Yuan YQ, Zhang XQ, et al. HMGB1-mediated autophagy confers resistance to gemcitabine in hormone-independent prostate cancer cells. Oncol Lett 2017; 14(5): 6285-90.
[http://dx.doi.org/10.3892/ol.2017.6965] [PMID: 29113279]


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