Association of serum HMGB2 levels with in-stent restenosis HMGB2 promotes neointimal hyperplasia in mice with femoral artery injury and proliferation and migration of VSMCs

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 4, 2017, Pages 717-729

  He, Yu Hu ^a   Wang, Xiao Qun ^a   Zhang, Jian ^b   Liu, Zhu Hui ^a   Pan, Wen Qi ^a   Shen, Ying ^a   Zhu, Zheng Bin ^a   Wang, Ling Jie ^a   Yan, Xiao Xiang ^a   Yang, Ke ^a   Zhang, Rui Yan ^a   Shen, Wei Feng ^a   Ding, Feng Hua ^a   Lu, Lin ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Chinese Academy of Sciences   (China)

Author keywords

HMGB2; In stent restenosis; Neointimal hyperplasia; P47phox; ROS

Indexed keywords

HIGH MOBILITY GROUP B2 PROTEIN; PROTEIN P47; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4; ADVANCED GLYCATION END PRODUCT RECEPTOR; AGER PROTEIN, HUMAN; BIOLOGICAL MARKER; NEUTROPHIL CYTOSOLIC FACTOR 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTIC SMOOTH MUSCLE CELL; ARTERY INJURY; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY ANGIOGRAPHY; FEMALE; FEMORAL ARTERY; HUMAN; IN-STENT RESTENOSIS; MAJOR CLINICAL STUDY; MALE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; VASCULAR SMOOTH MUSCLE CELL; ADVERSE EFFECTS; ANIMAL; BLOOD; BLOOD VESSEL INJURY; C57BL MOUSE; CASE CONTROL STUDY; CELL CULTURE; CELL MOTION; CORONARY ARTERY DISEASE; CORONARY RESTENOSIS; DEFICIENCY; DEVICES; DIAGNOSTIC IMAGING; DISEASE MODEL; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; HYPERPLASIA; INJURIES; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; MINIPIG; MULTIVARIATE ANALYSIS; PATHOLOGY; PERCUTANEOUS CORONARY INTERVENTION; PHENOTYPE; PHOSPHORYLATION; PIG; RISK FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; STATISTICAL MODEL; STENT; VASCULAR SMOOTH MUSCLE;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; AGED; ANIMALS; BIOMARKERS; CASE-CONTROL STUDIES; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CORONARY ANGIOGRAPHY; CORONARY ARTERY DISEASE; CORONARY RESTENOSIS; DISEASE MODELS, ANIMAL; FEMALE; FEMORAL ARTERY; GENETIC PREDISPOSITION TO DISEASE; HMGB2 PROTEIN; HUMANS; HYPERPLASIA; LOGISTIC MODELS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MULTIVARIATE ANALYSIS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; NEOINTIMA; PERCUTANEOUS CORONARY INTERVENTION; PHENOTYPE; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RISK FACTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STENTS; SWINE; SWINE, MINIATURE; TRANSFECTION; VASCULAR SYSTEM INJURIES;

EID: 85012131936     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.308210     Document Type: Article

References (34)

1. Byrne RA, Joner M, Kastrati A. Stent thrombosis and restenosis: what have we learned and where are we going? The Andreas Grüntzig Lecture ESC 2014. Eur Heart J. 2015; 36: 3320-3331. doi: 10.1093/eurheartj/ehv511.
2. Dangas GD, Claessen BE, Caixeta A, Sanidas EA, Mintz GS, Mehran R. In-stent restenosis in the drug-eluting stent era. J Am Coll Cardiol. 2010; 56: 1897-1907. doi: 10.1016/j.jacc.2010.07.028.
3. Kaul U, Bangalore S, Seth A, Arambam P, Abhaichand RK, Abhaychand RK, Patel TM, Banker D, Abhyankar A, Mullasari AS, Shah S, Jain R, Kumar PR, Bahuleyan CG; TUXEDO-India Investigators. Paclitaxeleluting versus everolimus-eluting coronary stents in diabetes. N Engl J Med. 2015; 373: 1709-1719. doi: 10.1056/NEJMoa1510188.
4. Alfonso F, Byrne RA, Rivero F, Kastrati A. Current treatment of in-stent restenosis. J Am Coll Cardiol. 2014; 63: 2659-2673. doi: 10.1016/j.jacc.2014.02.545.
5. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation. 2005; 111: 2257-2273. doi: 10.1161/01.CIR.0000163587.36485.A7.
6. Simon DI Inflammation and vascular injury: basic discovery to drug development. Circ J. 2012; 76: 1811-1818.
7. Juni RP, Duckers HJ, Vanhoutte PM, Virmani R, Moens AL. Oxidative stress and pathological changes after coronary artery interventions. J Am Coll Cardiol. 2013; 61: 1471-1481. doi: 10.1016/j.jacc.2012.11.068.
8. Lu L, Wang YN, Sun WH, et al. Two-dimensional fluorescence in-gel electrophoresis of coronary restenosis tissues in minipigs: increased adipocyte fatty acid binding protein induces reactive oxygen species-mediated growth and migration in smooth muscle cells. Arterioscler Thromb Vasc Biol. 2013; 33: 572-580. doi: 10.1161/ATVBAHA.112.301016.
9. Yang K, Lu L, Liu Y, Zhang Q, Pu LJ, Wang LJ, Zhu ZB, Wang YN, Meng H, Zhang XJ, Du R, Chen QJ, Shen WF. Increase of ADAM10 level in coronary artery in-stent restenosis segments in diabetic minipigs: high ADAM10 expression promoting growth and migration in human vascular smooth muscle cells via Notch 1 and 3. PLoS One. 2013; 8: e83853. doi: 10.1371/journal.pone.0083853.
10. Yanai H, Ban T, Taniguchi T. High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol. 2012; 33: 633-640. doi: 10.1016/j.it.2012.10.005.
11. Yanai H, Ban T, Wang Z, et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature. 2009; 462: 99-103. doi: 10.1038/nature08512.
12. Cai J, Wen J, Bauer E, Zhong H, Yuan H, Chen AF. The role of HMGB1 in cardiovascular biology: danger signals. Antioxid Redox Signal. 2015; 23: 1351-1369. doi: 10.1089/ars.2015.6408.
13. Cai J, Yuan H, Wang Q, et al. HMGB1-driven inflammation and intimal hyperplasia after aArterial injury involves cell-specific actions mediated by TLR4. Arterioscler Thromb Vasc Biol. 2015; 35: 2579-2593. doi: 10.1161/ATVBAHA.115.305789.
14. Kanellakis P, Agrotis A, Kyaw TS, Koulis C, Ahrens I, Mori S, Takahashi HK, Liu K, Peter K, Nishibori M, Bobik A. High-mobility group box protein 1 neutralization reduces development of diet-induced atherosclerosis in apolipoprotein e-deficient mice. Arterioscler Thromb Vasc Biol. 2011; 31: 313-319. doi: 10.1161/ATVBAHA.110.218669.
15. Kang R, Chen R, Zhang Q, et al. HMGB1 in health and disease. Mol Aspects Med. 2014; 40: 1-116. doi: 10.1016/j.mam.2014.05.001.
16. Barreiro-Alonso A, Lamas-Maceiras M, Rodríguez-Belmonte E, Vizoso-Vázquez Á, Quindós M, Cerdán ME. High mobility group B proteins, their partners, and other redox sensors in ovarian and prostate cancer. Oxid Med Cell Longev. 2016; 2016: 5845061. doi: 10.1155/2016/5845061.
17. Avgousti DC, Herrmann C, Kulej K, et al. A core viral protein binds host nucleosomes to sequester immune danger signals. Nature. 2016; 535: 173-177. doi: 10.1038/nature18317.
18. Lee S, Nam Y, Koo JY, Lim D, Park J, Ock J, Kim J, Suk K, Park SB. A small molecule binding HMGB1 and HMGB2 inhibits microglia-mediated neuroinflammation. Nat Chem Biol. 2014; 10: 1055-1060. doi: 10.1038/nchembio.1669.
19. Takaishi H, Kanai T, Nakazawa A, Sugata F, Nikai A, Yoshizawa S, Hamamoto Y, Funakoshi S, Yajima T, Iwao Y, Takemura M, Ozaki S, Hibi T. Anti-high mobility group box 1 and box 2 non-histone chromosomal proteins (HMGB1/HMGB2) antibodies and anti-Saccharomyces cerevisiae antibodies (ASCA): accuracy in differentially diagnosing UC and CD and correlation with inflammatory bowel disease phenotype. J Gastroenterol. 2012; 47: 969-977. doi: 10.1007/s00535-012-0566-3.
20. Kwon JH, Kim J, Park J Y, Hong SM, Park CW, Hong SJ, Park SY, Choi YJ, Do IG, Joh JW, Kim DS, Choi KY. Overexpression of high-mobility group box 2 is associated with tumor aggressiveness and prognosis of hepatocellular carcinoma. Clin Cancer Res. 2010; 16: 5511-5521. doi: 10.1158/1078-0432.CCR-10-0825.
21. Bauer EM, Shapiro R, Billiar TR, Bauer PM. High mobility group Box 1 inhibits human pulmonary artery endothelial cell migration via a Toll-like receptor 4- and interferon response factor 3-dependent mechanism(s). J Biol Chem. 2013; 288: 1365-1373. doi: 10.1074/jbc.M112.434142.
22. Montezano AC, Touyz RM. Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal. 2014; 20: 164-182. doi: 10.1089/ars.2013.5302.
23. San Martín A, Griendling KK. Redox control of vascular smooth muscle migration. Antioxid Redox Signal. 2010; 12: 625-640. doi: 10.1089/ars.2009.2852.
24. Szöcs K, Lassègue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002; 22: 21-27.
25. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med. 2008; 45: 1340-1351. doi: 10.1016/j.freeradbiomed.2008.08.013.
26. Dikalova A, Clempus R, Lassègue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D, Taylor WR, Schmidt HH, Owens GK, Lambeth JD, Griendling KK. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation. 2005; 112: 2668-2676. doi: 10.1161/CIRCULATIONAHA.105.538934.
27. Lee MY, San Martin A, Mehta PK, Dikalova AE, Garrido AM, Datla SR, Lyons E, Krause KH, Banfi B, Lambeth JD, Lassègue B, Griendling KK. Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation. Arterioscler Thromb Vasc Biol. 2009; 29: 480-487. doi: 10.1161/ATVBAHA.108.181925.
28. Tong X, Khandelwal AR, Qin Z, Wu X, Chen L, Ago T, Sadoshima J, Cohen RA. Role of smooth muscle Nox4-based NADPH oxidase in neointimal hyperplasia. J Mol Cell Cardiol. 2015; 89(pt B): 185-194. doi: 10.1016/j.yjmcc.2015.11.013.
29. Yang H, Tracey KJ. Targeting HMGB1 in inflammation. Biochim Biophys Acta. 2010; 1799: 149-156. doi: 10.1016/j.bbagrm.2009.11.019.
30. Swier VJ, Tang L, Krueger KD, Radwan MM, Del Core MG, Agrawal DK. Coronary injury score correlates with proliferating cells and alpha-smooth muscle actin expression in stented porcine coronary arteries. PLoS One. 2015; 10: e0138539. doi: 10.1371/journal.pone.0138539.
31. Chen J, Zhang J, Xu L, Xu C, Chen S, Yang J, Jiang H. Inhibition of neointimal hyperplasia in the rat carotid artery injury model by a HMGB1 inhibitor. Atherosclerosis. 2012; 224: 332-339. doi: 10.1016/j.atherosclerosis.2012.07.020.
32. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest. 2001; 108: 1513-1522. doi: 10.1172/JCI11927.
33. Schroeter MR, Leifheit-Nestler M, Hubert A, Schumann B, Glückermann R, Eschholz N, Krüger N, Lutz S, Hasenfuss G, Konstantinides S, Schäfer K. Leptin promotes neointima formation and smooth muscle cell proliferation via NADPH oxidase activation and signalling in caveolin-rich microdomains. Cardiovasc Res. 2013; 99: 555-565. doi: 10.1093/cvr/cvt126.
34. Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y. Central role of RAGE-dependent neointimal expansion in arterial restenosis. J Clin Invest. 2003; 111: 959-972. doi: 10.1172/JCI17115.