HMGB1 contributes to allergen-induced airway remodeling in a murine model of chronic asthma by modulating airway inflammation and activating lung fibroblasts

Cellular and Molecular Immunology

Volumn 12, Issue 4, 2015, Pages 409-423

  Hou, Changchun ^a   Kong, Jinliang ^a   Liang, Yue ^a   Huang, Hong ^a   Wen, Hanchun ^a   Zheng, Xiaowen ^a   Wu, Lihong ^a   Chen, Yiqiang ^a  

^a FIRST AFFILIATED HOSPITAL OF GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

airway remodeling; asthma; high mobility group box protein 1 (HMGB1); murine mouse model

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; GELATINASE B; HIGH MOBILITY GROUP B1 PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN ANTIBODY; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; PROTEIN ANTIBODY; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; ACTIN; AUTACOID; HMGB1 PROTEIN, MOUSE; IL1B PROTEIN, MOUSE; MMP9 PROTEIN, MOUSE; TGFB1 PROTEIN, MOUSE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

AIRWAY REMODELING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG RESPONSE; ENZYME ACTIVITY; EOSINOPHIL; FEMALE; HUMAN; HUMAN CELL; LUNG FIBROBLAST; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CELL MOTION; CHEMICALLY INDUCED; CHRONIC DISEASE; DISEASE MODEL; FIBROBLAST; IMMUNOLOGY; LUNG; PATHOLOGY;

MURINAE; MUS;

ACTINS; ANIMALS; ASTHMA; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLASTS; HMGB1 PROTEIN; IMMUNOGLOBULIN E; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; LUNG; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; TRANSFORMING GROWTH FACTOR BETA1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84936151118     PISSN: 16727681     EISSN: 20420226     Source Type: Journal    
DOI: 10.1038/cmi.2014.60     Document Type: Article

References (35)

1. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5: 331-342
2. Karlsson S, Pettilä V, Tenhunen J, Laru-Sompa R, Hynninen M, Ruokonen E. HMGB1 as a predictor of organ dysfunction and outcome in patients with severe sepsis. Intensive Care Med 2008; 34: 1046-1053
3. Taniguchi N, Kawahara K, Yone K, Hashiguchi T, Yamakuchi M, Goto Met 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: 971-981
4. Hou C, Zhao H, Liu L, Li W, Zhou X, Lv Y, et al. High mobility group protein B1 (HMGB1) in Asthma: comparison of patients with chronic obstructive pulmonary disease and healthy controls. Mol Med 2011; 17: 807-815
5. Hou CC, Zhao HJ, Cai SX, Liu LY, Shen XB, Mo GW. Expression of high mobility group box-1 in the lung tissue and BALF of asthmatic mice and the influence of dexamethasone. Nan Fang Yi Ke Da Xue Xue Bao 2010; 30: 2051-2054
6. Shim EJ, Chun E, Lee HS, Bang BR, Kim TW, Cho SH, et al. The role of high-mobility group box-1 (HMGB1) in the pathogenesis of asthma. Clin Exp Allergy 2012; 42: 958-965
7. Hamada N, Maeyama T, Kawaguchi T, Yoshimi M, Fukumoto J, Yamada M, et al. The role of high mobility group box1 in pulmonary fibrosis. Am J Respir Cell Mol Biol 2008; 39: 440-447
8. Biscetti F, Straface G, de Cristofaro R, Lancellotti S, Rizzo P, Arena V, et al. High-mobility group box-1 protein promotes angiogenesis after peripheral ischemia in diabetic mice through a VEGF-dependent mechanism. Diabetes 2010; 59: 1496-1505
9. Liu K, Mori S, Takahashi HK, Tomono Y, Wake H, Kanke T, et al. Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rat. FASEB J 2007; 21: 3904-3916
10. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protocols 2007; 2: 329-333
11. Sugiura H, Liu X, Duan F, Kawasaki S, Togo S, Kamio K, et al. Cultured lung fibroblasts from ovalbumin-challenged asthmaticmice differ functionally from normal. Am J Respir Cell Mol Biol 2007; 37: 424-430
12. Everitt JI, Boreiko CJ, Mangum JB, Martin JT, Iglehart JD, Hesterberg TW. Development of a tracheal implant xenograft model to expose human bronchial epithelial cells to to Xic gases. Toxicol Pathol 1989; 17: 465-473
13. Sha Y, Zmijewski J, Xu Z, Abraham E. HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J Immunol 2008; 180: 2531-2537
14. Zimmermann N, Conkright JJ, Rothenberg ME. CC chemokine receptor-3 undergoes prolongedligand-induced internalization. J Biol Chem 1999; 274: 12611-12618
15. Schleimer RP, Rutledge BK. Cultured human vascular endothelial cells acquire adhesiveness for neutrophils after stimulation with interleukin 1, endotoxin, and tumor-promoting phorbol diesters. J Immunol 1986; 136: 649-654
16. Halwani R, Al-Muhsen S, Al-Jahdali H, Hamid Q. Role of transforming growth factor-b in airway remodeling in asthma. Am J Respir Cell Mol Biol 2011; 44: 127-33
17. Ohbayashi H, Shimokata K. Matrix metalloproteinase-9 and airway remodeling in asthma. Curr Drug Targets Inflamm Allergy 2005; 4: 177-181
18. Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 2004; 10: 1095-1103
19. Lee CC, Lai YT, Chang HT, Liao JW, Shyu WC, Li CY, et al. Inhibition of high-mobility group box 1 in lung reduced airway inflammation and remodeling in a mouse model of chronic asthma. Biochem Pharmacol 2013; 86: 940-949
20. Hou C, Zhao H, Li W, Cai S. Hydrogen peroxide induces high mobility group box 1 release in human bronchial epithelial cells. Nan Fang Yi Ke Da Xue Xue Bao 2012; 32: 1131-1134
21. Ferhani N, Letuve S, Kozhich A, Thibaudeau O, Grandsaigne M, Maret M, et al. Expression of high-mobility group box 1 and of receptor for advanced glycatio end products in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2010; 181: 917-927
22. Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, et al. A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 2007; 26: 1129-1139
23. Cockcroft DW, Davis BE. Mechanisms of airway hyperresponsiveness. J Allergy Clin Immunol 2006; 118: 551-559
24. Elias JA, Zhu Z, Chupp G, Homer RJ. Airway remodeling in asthma. J Clin Invest 1999; 104: 1001-1006
25. Lappalainen U, Whitsett JA, Wert SE, Tichelaar JW, Bry K. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 2005; 32: 311-318
26. Cho JY, Pham A, Rosenthal P, Miller M, Doherty T, Broide DH. Chronic OVA allergen challenged TNF p55/p75 receptor deficient mice have reduced airway remodeling. Int Immunopharmacol 2011; 11: 1038-1044
27. Degryse B, Bonaldi T, Scaffidi P, Müller S, Resnati M, Sanvito F, 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: 1197-1206
28. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 1999; 103: 779-788
29. Tagaya E, Tamaoki J. Mechanisms of airway remodeling in asthma. Allergol Int 2007; 56: 331-340
30. Lotfi R, Herzog GI, DeMarco RA, Beer-Stolz D, Lee JJ, Rubartelli A, et al. Eosinophils oxidize damage-Associated molecular pattern molecules derived from stressed cells. J Immunol 2009; 183: 5023-5031
31. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 2000; 192: 565-570
32. Park JS, Arcaroli J, Yum HK, Yang H, Wang H, Yang KY, et al. Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am J Physiol Cell Physiol 2003; 284: C870-C879
33. Liu PL, Tsai JR, Hwang JJ, Chou SH, Cheng YJ, Lin FY, et al. Highmobility group box 1-mediated matrix metalloproteinase-9 expression in non-small cell lung cancer contributes to tumor cell invasiveness. Am J Respir Cell Mol Biol 2010; 43: 530-538
34. Kawahara K, Hashiguchi T, Kikuchi K, Tancharoen S, Miura N, Ito T, et al. Induction of high mobility group box 1 release from serotoninstimulated human umbilical vein endothelial cells. Int J Mol Med 2008; 22: 639-644
35. Ye YL, Chuang YH, Chiang BL. Strategies of mucosal immunotherapy for allergic diseases. Cell Mol Immunol 2011; 8: 453-461