Ethyl pyruvate attenuates murine allergic rhinitis partly by decreasing high mobility group box 1 release

Experimental Biology and Medicine

Volumn 240, Issue 11, 2015, Pages 1490-1499

  Chen, Shan ^a   Wang, Yanjun ^a   Gong, Guoqing ^a   Chen, Jianjun ^a   Niu, Yongzhi ^a   Kong, Weijia ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

allergic rhinitis; ethyl pyruvate; high mobility group box 1; IgE; Mouse model

Indexed keywords

DNA BINDING PROTEIN; ETHYL PYRUVATE; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 4; OVALBUMIN; PYRUVIC ACID; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; CYTOKINE; HMGB1 PROTEIN, MOUSE; PYRUVIC ACID DERIVATIVE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ALLERGIC RHINITIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL HYPERPLASIA; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN ALLERGY; TH2 CELL; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CHEMISTRY; DISEASE MODEL; INFLAMMATION; METABOLISM; PATHOLOGY; RHINITIS, ALLERGIC; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HMGB1 PROTEIN; IMMUNOGLOBULIN E; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICE; MICE, INBRED BALB C; OVALBUMIN; PYRUVATES; RHINITIS, ALLERGIC; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 84945967377     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370214566563     Document Type: Article

References (60)

1. Fokkens WJ, Lund VJ, Mullol J, Bachert C, Alobid I, Baroody F, Cohen N, Cervin A, Douglas R, Gevaert P, Georgalas C, Goossens H, Harvey R, Hellings P, Hopkins C, Jones N, Joos G, Kalogjera L, Kern B, Kowalski M, Price D, Riechelmann H, Schlosser R, Senior B, Thomas M, Toskala E, Voegels R, Wang de Y, Wormald PJ. European position paper on rhinosinusitis and nasal polyps 2012. Rhinology 2012;50:1--299
2. C.SalpietroC.CuppariL.GrassoM.A.ToscaM.Miraglia Del GiudiceM.La RosaG.L.MarsegliaA.SalpietroG.Ciprandi. Nasal high-mobility group box-1 protein in children with allergic rhinitis. Int Arch Allergy Immunol2013; 161: 116–21.
3. H.H.KariyawasamG.Rotiroti. Allergic rhinitis, chronic rhinosinusitis and asthma: unravelling a complex relationship. Curr Opin Otolaryngol Head Neck Surg2013; 21: 79–86.
4. D.H.Broide. Allergic rhinitis: pathophysiology. Allergy Asthma Proc2010; 31: 370–4.
5. L.ZhangD.HanD.HuangY.WuZ.DongG.XuW.KongC.Bachert. Prevalence of self-reported allergic rhinitis in eleven major cities in china. Int Arch Allergy Immunol2009; 149: 47–57.
6. Y.ZhangL.Zhang. Prevalence of allergic rhinitis in china. Allergy Asthma Immunol Res2014; 6: 105–13.
7. L.M.BellussiL.ChenD.ChenF.M.PassaliD.Passali. The role of High Mobility Group Box 1 chromosomal protein in the pathogenesis of chronic sinusitis and nasal polyposis. Acta Otorhinolaryngol Ital2012; 32: 386–92.
8. S.M.HongJ.S.ChoJ.Y.UmJ.M.ShinI.H.ParkS.H.LeeS.H.LeeH.M.Lee. Increased expression of high-mobility group protein B1 in chronic rhinosinusitis. Am J Rhinol Allergy2013; 27: 278–82.
9. D.ChenM.MaoL.M.BellussiD.PassaliL.Chen. Increase of high mobility group box chromosomal protein 1 in eosinophilic chronic rhinosinusitis with nasal polyps. Int Forum Allergy Rhinol2014; 4: 453–62.
10. C.C.LeeY.T.LaiH.T.ChangJ.W.LiaoW.C.ShyuC.Y.LiC.N.Wang. Inhibition of high-mobility group box 1 in lung reduced airway inflammation and remodeling in a mouse model of chronic asthma. Biochem Pharmacol2013; 86: 940–9.
11. E.J.ShimE.ChunH.S.LeeB.R.BangT.W.KimS.H.ChoK.U.MinH.W.Park. The role of high-mobility group box-1 (HMGB1) in the pathogenesis of asthma. Clin Exp Allergy2012; 42: 958–65.
12. T.WatanabeK.AsaiH.FujimotoH.TanakaH.KanazawaK.Hirata. Increased levels of HMGB-1 and endogenous secretory RAGE in induced sputum from asthmatic patients. Respir Med2011; 105: 519–25.
13. H.TangH.ZhaoJ.SongH.DongL.YaoZ.LiangY.LvF.ZouS.Cai. Ethyl pyruvate decreases airway neutrophil infiltration partly through a high mobility group box 1-dependent mechanism in a chemical-induced murine asthma model. Int Immunopharmacol2014; 21: 163–70.
14. M.Stros. HMGB proteins: interactions with DNA and chromatin. Biochim Biophys Acta2010; 1799: 101–13.
15. L.UlloaF.M.BatliwallaU.AnderssonP.K.GregersenK.J.Tracey. High mobility group box chromosomal protein 1 as a nuclear protein, cytokine, and potential therapeutic target in arthritis. Arthritis Rheum2003; 48: 876–81.
16. H.WangO.BloomM.ZhangJ.M.VishnubhakatM.OmbrellinoJ.CheA.FrazierH.YangS.IvanovaL.BorovikovaK.R.ManogueE.FaistE.AbrahamJ.AnderssonU.AnderssonP.E.MolinaN.N.AbumradA.SamaK.J.Tracey. HMG-1 as a late mediator of endotoxin lethality in mice. Science1999; 285: 248–51.
17. L.F.LiK.C.KaoC.T.YangC.C.HuangY.Y.Liu. Ethyl pyruvate reduces ventilation-induced neutrophil infiltration and oxidative stress. Exp Biol Med (Maywood)2012; 237: 720–7.
18. S.QinH.WangR.YuanH.LiM.OchaniK.OchaniM.Rosas-BallinaC.J.CzuraJ.M.HustonE.MillerX.LinB.SherryA.KumarG.LarosaW.NewmanK.J.TraceyH.Yang. Role of HMGB1 in apoptosis-mediated sepsis lethality. J Exp Med2006; 203: 1637–42.
19. H.E.HarrisU.AnderssonD.S.Pisetsky. HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol2012; 8: 195–202.
20. E.VenereauM.CasalgrandiM.SchiraldiD.J.AntoineA.CattaneoF.De MarchisJ.LiuA.AntonelliA.PretiL.RaeliS.S.ShamsH.YangL.VaraniU.AnderssonK.J.TraceyA.BachiM.UguccioniM.E.Bianchi. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med2012; 209: 1519–28.
21. M.E.Bianchi. HMGB1 loves company. J Leukoc Biol2009; 86: 573–6.
22. Ullah MA, Loh Z, Gan WJ, Zhang V, Yang H, Li JH, Yamamoto Y, Schmidt AM, Armour CL, Hughes JM, Phipps S, Sukkar MB. Receptor for advanced glycation end products and its ligand high-mobility group box-1 mediate allergic airway sensitization and airway inflammation. J Allergy Clin Immunol 2014;134:440--50
23. J.ShiQ.LuoF.ChenD.ChenG.XuH.Li. Induction of IL-6 and IL-8 by house dust mite allergen Der p1 in cultured human nasal epithelial cells is associated with PAR/PI3K/NFkappaB signaling. ORL J Otorhinolaryngol Relat Spec2010; 72: 256–65.
24. U.AnderssonH.WangK.PalmbladA.C.AvebergerO.BloomH.Erlandsson-HarrisA.JansonR.KokkolaM.ZhangH.YangK.J.Tracey. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med2000; 192: 565–70.
25. D.TangR.KangH.J.Zeh3rdM.T.Lotze. High-mobility group box 1, oxidative stress, and disease. Antioxid Redox Signal2011; 14: 1315–35.
26. M.P.Fink. Ethyl pyruvate: a novel anti-inflammatory agent. J Intern Med2007; 261: 349–62.
27. S.H.DaveJ.S.TilstraK.MatsuokaF.LiR.A.DeMarcoD.Beer-StolzA.R.SepulvedaM.P.FinkM.T.LotzeS.E.Plevy. Ethyl pyruvate decreases HMGB1 release and ameliorates murine colitis. J Leukoc Biol2009; 86: 633–43.
28. Z.G.LuanJ.ZhangX.H.YinX.C.MaR.X.Guo. Ethyl pyruvate significantly inhibits tumour necrosis factor-alpha, interleukin-1beta and high mobility group box 1 releasing and attenuates sodium taurocholate-induced severe acute pancreatitis associated with acute lung injury. Clin Exp Immunol2013; 172: 417–26.
29. H.SaitoK.HowieJ.WattieA.DenburgR.EllisM.D.InmanJ.A.Denburg. Allergen-induced murine upper airway inflammation: local and systemic changes in murine experimental allergic rhinitis. Immunology2001; 104: 226–34.
30. K.K.KaoM.P.Fink. The biochemical basis for the anti-inflammatory and cytoprotective actions of ethyl pyruvate and related compounds. Biochem Pharmacol2010; 80: 151–9.
31. S.H.ChoS.Y.OhZ.ZhuJ.LeeA.P.Lane. Spontaneous eosinophilic nasal inflammation in a genetically-mutant mouse: comparative study with an allergic inflammation model. PLoS One2012; 7: e35114.–e35114.
32. H.ZhouX.ChenW.M.ZhangL.P.ZhuL.Cheng. HIF-1alpha inhibition reduces nasal inflammation in a murine allergic rhinitis model. PLoS One2012; 7: e48618.–e48618.
33. H.J.JeongH.A.OhB.J.LeeH.M.Kim. Inhibition of IL-32 and TSLP production through the attenuation of caspase-1 activation in an animal model of allergic rhinitis by Naju Jjok (Polygonum tinctorium). Int J Mol Med2014; 33: 142–50.
34. H.YangD.J.AntoineU.AnderssonK.J.Tracey. The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J Leukoc Biol2013; 93: 865–73.
35. S.MullerL.RonfaniM.E.Bianchi. Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J Intern Med2004; 255: 332–43.
36. M.Bustin. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol Cell Biol1999; 19: 5237–46.
37. U.AnderssonK.J.Tracey. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol2011; 29: 139–62.
38. P.ScaffidiT.MisteliM.E.Bianchi. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature2002; 418: 191–5.
39. Wang M, Gorasiya S, Antoine DJ, Sitapara RA, Wu W, Sharma L, Yang H, Ashby CR Jr, Vasudevan D, Zur M, Thomas DD, Mantell LL. The compromise of macrophage functions by hyperoxia is attenuated by ethacrynic acid via inhibition of NF-kappaB-mediated release of HMGB1. Am J Respir Cell Mol Biol 2015;52:171--82
40. M.SongJ.A.KellumH.KaldasM.P.Fink. Evidence that glutathione depletion is a mechanism responsible for the anti-inflammatory effects of ethyl pyruvate in cultured lipopolysaccharide-stimulated RAW 264.7 cells. J Pharmacol Exp Ther2004; 308: 307–16.
41. Y.HanJ.A.EnglertR.YangR.L.DeludeM.P.Fink. Ethyl pyruvate inhibits nuclear factor-kappaB-dependent signaling by directly targeting p65. J Pharmacol Exp Ther2005; 312: 1097–105.
42. M.P.Fink. Ethyl pyruvate: a novel treatment for sepsis and shock. Minerva Anestesiol2004; 70: 365–71.
43. A.MizutaniN.MaedaS.TokuY.IsohamaK.SugaharaH.Yamamoto. Inhibition by ethyl pyruvate of the nuclear translocation of nuclear factor-kappaB in cultured lung epithelial cells. Pulm Pharmacol Ther2010; 23: 308–15.
44. R.YangT.UchiyamaS.K.WatkinsX.HanM.P.Fink. Ethyl pyruvate reduces liver injury in a murine model of extrahepatic cholestasis. Shock2004; 22: 369–75.
45. P.H.HowarthM.SalageanD.Dokic. Allergic rhinitis: not purely a histamine-related disease. Allergy2000; 55: 7–16.
46. D.A.GentileJ.YokitisB.L.AngeliniW.J.DoyleD.P.Skoner. Effect of intranasal challenge with interleukin-6 on upper airway symptomatology and physiology in allergic and nonallergic patients. Ann Allergy Asthma Immunol2001; 86: 531–6.
47. R.YangA.L.ShauflM.E.KilleenM.P.Fink. Ethyl pyruvate ameliorates liver injury secondary to severe acute pancreatitis. J Surg Res2009; 153: 302–9.
48. Z.S.TawadrousR.L.DeludeM.P.Fink. Resuscitation from hemorrhagic shock with Ringer’s ethyl pyruvate solution improves survival and ameliorates intestinal mucosal hyperpermeability in rats. Shock2002; 17: 473–7.
49. M.K.IijimaT.KobayashiH.KamadaN.Shimojo. Exposure to ozone aggravates nasal allergy-like symptoms in guinea pigs. Toxicol Lett2001; 123: 77–85.
50. H.S.KimI.H.ChoJ.E.KimY.J.ShinJ.H.JeonY.KimY.M.YangK.H.LeeJ.W.LeeW.J.LeeS.K.YeM.H.Chung. Ethyl pyruvate has an anti-inflammatory effect by inhibiting ROS-dependent STAT signaling in activated microglia. Free Radic Biol Med2008; 45: 950–63.
51. S.G.TrivediC.M.Lloyd. Eosinophils in the pathogenesis of allergic airways disease. Cell Mol Life Sci2007; 64: 1269–89.
52. R.LotfiG.I.HerzogR.A.DeMarcoD.Beer-StolzJ.J.LeeA.RubartelliH.SchrezenmeierM.T.Lotze. Eosinophils oxidize damage-associated molecular pattern molecules derived from stressed cells. J Immunol2009; 183: 5023–31.
53. A.L.StenfeldtC.Wenneras. Danger signals derived from stressed and necrotic epithelial cells activate human eosinophils. Immunology2004; 112: 605–14.
54. S.P.HoganH.F.RosenbergR.MoqbelS.PhippsP.S.FosterP.LacyA.B.KayM.E.Rothenberg. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy2008; 38: 709–50.
55. R.BaumannM.RabaszowskiI.SteninL.TilgnerK.ScheckenbachJ.WiltfangJ.SchipperA.ChakerM.Wagenmann. Comparison of the nasal release of IL-4, IL-10, IL-17, CCL13/MCP-4, and CCL26/eotaxin-3 in allergic rhinitis during season and after allergen challenge. Am J Rhinol Allergy2013; 27: 266–72.
56. G.J.BraunstahlS.E.OverbeekA.KleinjanJ.B.PrinsH.C.HoogstedenW.J.Fokkens. Nasal allergen provocation induces adhesion molecule expression and tissue eosinophilia in upper and lower airways. J Allergy Clin Immunol2001; 107: 469–76.
57. Z.YangA.ChenH.SunY.YeW.Fang. Ginsenoside Rd elicits Th1 and Th2 immune responses to ovalbumin in mice. Vaccine2007; 25: 161–9.
58. H.J.GouldB.J.Sutton. IgE in allergy and asthma today. Nat Rev Immunol2008; 8: 205–17.
59. J.PunnonenG.AversaB.G.CocksA.N.McKenzieS.MenonG.ZurawskiR.de Waal MalefytJ.E.de Vries. Interleukin 13 induces interleukin 4-independent IgG4 and IgE synthesis and CD23 expression by human B cells. Proc Natl Acad Sci USA1993; 90: 3730–4.
60. Hou C, Kong J, Liang Y, Huang H, Wen H, Zheng X, Wu L, Chen Y. HMGB1 contributes to allergen-induced airway remodeling in a murine model of chronic asthma by modulating airway inflammation and activating lung fibroblasts. Cell Mol Immunol 2014