Membrane-Bound Thrombomodulin Regulates Macrophage Inflammation in Abdominal Aortic Aneurysm

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 11, 2015, Pages 2412-2422

  Wang, Kuan Chieh ^a,b,c   Li, Yi Heng ^a,c,d   Shi, Guey Yueh ^c   Tsai, Hung Wen ^d   Luo, Chawn Yau ^c   Cheng, Min Hua ^a   Ma, Chih Yuan ^a,c   Hsu, Yun Yan ^a,c   Cheng, Tsung Lin ^e,f   Chang, Bi Ing ^a,c   Lai, Chao Han ^c,e   Wu, Hua Lin ^a,c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b Institute of Basic Medical Sciences   (Taiwan)

^c Institute of Clinical Medicine   (Taiwan)

^d Department of Internal Medicine ^*  (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^f KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

abdominal aortic aneurysm; macrophages; monocytes; myeloid cells; thrombomodulin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALCIUM CHLORIDE; CD31 ANTIGEN; CD68 ANTIGEN; ELASTIN; GELATINASE A; GELATINASE B; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; THROMBOMODULIN; TRANSGELIN; TUMOR NECROSIS FACTOR ALPHA; ANGIOTENSIN II; AUTACOID; MMP9 PROTEIN, MOUSE; THBD PROTEIN, HUMAN; THBD PROTEIN, MOUSE;

ABDOMINAL AORTA ANEURYSM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL INFILTRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME SYNTHESIS; HYPERLIPIDEMIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VASCULAR SMOOTH MUSCLE CELL; VASCULITIS; WILD TYPE; ABDOMINAL AORTA; ANIMAL; AORTITIS; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE; CHEMICALLY INDUCED; CHEMOTAXIS; DEFICIENCY; DISEASE MODEL; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; RETROSPECTIVE STUDY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TIME; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; AORTITIS; CALCIUM CHLORIDE; CELL MEMBRANE; CELLS, CULTURED; CHEMOTAXIS; DISEASE MODELS, ANIMAL; ELASTIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION MEDIATORS; MACROPHAGES, PERITONEAL; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OXIDATIVE STRESS; RETROSPECTIVE STUDIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THROMBOMODULIN; TIME FACTORS; TRANSFECTION;

EID: 84945445867     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.305529     Document Type: Article

References (50)

1. Golledge J, Muller J, Daugherty A, Norman P, Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol 2006 26 2605 2613. doi: 10.1161/01.ATV.0000245819.32762.cb
2. Miyake T, Morishita R, Pharmacological treatment of abdominal aortic aneurysm. Cardiovasc Res 2009 83 436 443. doi: 10.1093/cvr/cvp155
3. Baxter BT, Terrin MC, Dalman RL, Medical management of small abdominal aortic aneurysms. Circulation 2008 117 1883 1889. doi: 10.1161/CIRCULATIONAHA.107.735274
4. Ginhoux F, Jung S, Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 2014 14 392 404. doi: 10.1038/nri3671
5. Daugherty A, Cassis LA, Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 2004 24 429 434. doi: 10.1161/01.ATV.0000118013.72016.ea
6. Shimizu K, Mitchell RN, Libby P, Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 2006 26 987 994. doi: 10.1161/01.ATV.0000214999.12921.4f
7. Tazume H, Miyata K, Tian Z, Macrophage-derived angiopoietin-like protein 2 accelerates development of abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol 2012 32 1400 1409. doi: 10.1161/ATVBAHA.112.247866
8. Li F, Downing BD, Smiley LC, Mund JA, Distasi MR, Bessler WK, Sarchet KN, Hinds DM, Kamendulis LM, Hingtgen CM, Case J, Clapp DW, Conway SJ, Stansfield BK, Ingram DA Jr, Neurofibromin-deficient myeloid cells are critical mediators of aneurysm formation in vivo. Circulation 2014 129 1213 1224. doi: 10.1161/CIRCULATIONAHA.113.006320
9. Blomkalns AL, Gavrila D, Thomas M, CD14 directs adventitial macrophage precursor recruitment: role in early abdominal aortic aneurysm formation. J Am Heart Assoc 2013 2 e000065. doi: 10.1161/JAHA.112.000065
10. Daugherty A, Powell JT, Recent highlights of ATVB: aneurysms. Arterioscler Thromb Vasc Biol 2014 34 691 694. doi: 10.1161/ATVBAHA.114.303353
11. Conway EM, Thrombomodulin and its role in inflammation. Semin Immunopathol 2012 34 107 125. doi: 10.1007/s00281-011-0282-8
12. Wei HJ, Li YH, Shi GY, Liu SL, Chang PC, Kuo CH, Wu HL, Thrombomodulin domains attenuate atherosclerosis by inhibiting thrombin-induced endothelial cell activation. Cardiovasc Res 2011 92 317 327. doi: 10.1093/cvr/cvr220
13. Esmon CT, The roles of protein C and thrombomodulin in the regulation of blood coagulation. J Biol Chem 1989 264 4743 4746
14. Griffin JH, Fernández JA, Gale AJ, Mosnier LO, Activated protein C. J Thromb Haemost 2007 5 suppl 1 73 80. doi: 10.1111/j.1538-7836.2007.02491.x
15. Conway EM, Van de Wouwer M, Pollefeyt S, Jurk K, Van Aken H, De Vriese A, Weitz JI, Weiler H, Hellings PW, Schaeffer P, Herbert JM, Collen D, Theilmeier G, The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappaB and mitogen-activated protein kinase pathways. J Exp Med 2002 196 565 577
16. Van de Wouwer M, Plaisance S, De Vriese A, Waelkens E, Collen D, Persson J, Daha MR, Conway EM, The lectin-like domain of thrombomodulin interferes with complement activation and protects against arthritis. J Thromb Haemost 2006 4 1813 1824
17. Abeyama K, Stern DM, Ito Y, Kawahara K, Yoshimoto Y, Tanaka M, Uchimura T, Ida N, Yamazaki Y, Yamada S, Yamamoto Y, Yamamoto H, Iino S, Taniguchi N, Maruyama I, The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest 2005 115 1267 1274. doi: 10.1172/JCI22782
18. Shi CS, Shi GY, Hsiao HM, Hsiao SM, Kao YC, Kuo KL, Ma CY, Kuo CH, Chang BI, Chang CF, Lin CH, Wong CH, Wu HL, Lectin-like domain of thrombomodulin binds to its specific ligand Lewis Y antigen and neutralizes lipopolysaccharide-induced inflammatory response. Blood 2008 112 3661 3670. doi: 10.1182/blood-2008-03-142760
19. Lin WL, Chang CF, Shi CS, Shi GY, Wu HL, Recombinant lectin-like domain of thrombomodulin suppresses vascular inflammation by reducing leukocyte recruitment via interacting with Lewis Y on endothelial cells. Arterioscler Thromb Vasc Biol 2013 33 2366 2373. doi: 10.1161/ATVBAHA.113.301221
20. Lai CH, Shi GY, Lee FT, Kuo CH, Cheng TL, Chang BI, Ma CY, Hsu FC, Yang YJ, Wu HL, Recombinant human thrombomodulin suppresses experimental abdominal aortic aneurysms induced by calcium chloride in mice. Ann Surg 2013 258 1103 1110. doi: 10.1097/SLA.0b013e31827df7cb
21. Yang SM, Ka SM, Wu HL, Thrombomodulin domain 1 ameliorates diabetic nephropathy in mice via anti-NF-κB/NLRP3 inflammasome-mediated inflammation, enhancement of NRF2 antioxidant activity and inhibition of apoptosis. Diabetologia 2014 57 424 434. doi: 10.1007/s00125-013-3115-6
22. McCachren SS, Diggs J, Weinberg JB, Dittman WA, Thrombomodulin expression by human blood monocytes and by human synovial tissue lining macrophages. Blood 1991 78 3128 3132
23. Tsai CS, Tsai YT, Lin CY, Lin TC, Huang GS, Hong GJ, Lin FY, Expression of thrombomodulin on monocytes is associated with early outcomes in patients with coronary artery bypass graft surgery. Shock 2010 34 31 39. doi: 10.1097/SHK.0b013e3181d494c4
24. Hwang SM, Kim JE, Han KS, Kim HK, Thrombomodulin phenotype of a distinct monocyte subtype is an independent prognostic marker for disseminated intravascular coagulation. Crit Care 2011 15 R113. doi: 10.1186/cc10139
25. Ma CY, Shi GY, Shi CS, Kao YC, Lin SW, Wu HL, Monocytic thrombomodulin triggers LPS-and gram-negative bacteria-induced inflammatory response. J Immunol 2012 188 6328 6337. doi: 10.4049/jimmunol.1102266
26. Chiou AC, Chiu B, Pearce WH, Murine aortic aneurysm produced by periarterial application of calcium chloride. J Surg Res 2001 99 371 376. doi: 10.1006/jsre.2001.6207
27. Qin Y, Cao X, Yang Y, Shi GP, Cysteine protease cathepsins and matrix metalloproteinases in the development of abdominal aortic aneurysms. Future Cardiol 2013 9 89 103. doi: 10.2217/fca.12.71
28. Isermann B, Hendrickson SB, Zogg M, Wing M, Cummiskey M, Kisanuki YY, Yanagisawa M, Weiler H, Endothelium-specific loss of murine thrombomodulin disrupts the protein C anticoagulant pathway and causes juvenile-onset thrombosis. J Clin Invest 2001 108 537 546. doi: 10.1172/JCI13077
29. Wang Y, Krishna S, Golledge J, The calcium chloride-induced rodent model of abdominal aortic aneurysm. Atherosclerosis 2013 226 29 39. doi: 10.1016/j.atherosclerosis.2012.09.010
30. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT, Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest 2002 110 625 632. doi: 10.1172/JCI15334
31. Morimoto K, Hasegawa T, Tanaka A, Wulan B, Yu J, Morimoto N, Okita Y, Okada K, Free-radical scavenger edaravone inhibits both formation and development of abdominal aortic aneurysm in rats. J Vasc Surg 2012 55 1749 1758. doi: 10.1016/j.jvs.2011.11.059
32. McCormick ML, Gavrila D, Weintraub NL, Role of oxidative stress in the pathogenesis of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 2007 27 461 469. doi: 10.1161/01.ATV.0000257552.94483.14
33. Gong Y, Hart E, Shchurin A, Hoover-Plow J, Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest 2008 118 3012 3024. doi: 10.1172/JCI32750
34. McEver RP, Zhu C, Rolling cell adhesion. Annu Rev Cell Dev Biol 2010 26 363 396. doi: 10.1146/annurev.cellbio.042308.113238
35. Wang YX, Martin-McNulty B, da Cunha V, Fasudil, a Rho-kinase inhibitor, attenuates angiotensin II-induced abdominal aortic aneurysm in apolipoprotein E-deficient mice by inhibiting apoptosis and proteolysis. Circulation 2005 111 2219 2226. doi: 10.1161/01.CIR.0000163544.17221.BE
36. Satoh K, Nigro P, Matoba T, O'Dell MR, Cui Z, Shi X, Mohan A, Yan C, Abe J, Illig KA, Berk BC, Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med 2009 15 649 656. doi: 10.1038/nm.1958
37. Li YH, Chung HC, Luo CY, Chao TH, Shyu KG, Shi GY, Wu HL, Thrombomodulin is upregulated in cardiomyocytes during cardiac hypertrophy and prevents the progression of contractile dysfunction. J Card Fail 2010 16 980 990. doi: 10.1016/j.cardfail.2010.06.415
38. Rabausch K, Bretschneider E, Sarbia M, Meyer-Kirchrath J, Censarek P, Pape R, Fischer JW, Schrör K, Weber AA, Regulation of thrombomodulin expression in human vascular smooth muscle cells by COX-2-derived prostaglandins. Circ Res 2005 96 e1 e6. doi: 10.1161/01.RES.0000153150.27690.f2
39. Lo IC, Lin TM, Chou LH, Liu SL, Wu LW, Shi GY, Wu HL, Jiang MJ, Ets-1 mediates platelet-derived growth factor-BB-induced thrombomodulin expression in human vascular smooth muscle cells. Cardiovasc Res 2009 81 771 779. doi: 10.1093/cvr/cvn351
40. Tohda G, Oida K, Okada Y, Kosaka S, Okada E, Takahashi S, Ishii H, Miyamori I, Expression of thrombomodulin in atherosclerotic lesions and mitogenic activity of recombinant thrombomodulin in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1998 18 1861 1869. doi: 10.1161/01.ATV.18.12.1861
41. Yoshii Y, Okada Y, Sasaki S, Mori H, Oida K, Ishii H, Expression of thrombomodulin in human aortic smooth muscle cells with special reference to atherosclerotic lesion types and age differences. Med Electron Microsc 2003 36 165 172. doi: 10.1007/s00795-003-0212-5
42. Li YH, Hsieh CY, Wang DL, Chung HC, Liu SL, Chao TH, Shi GY, Wu HL, Remodeling of carotid arteries is associated with increased expression of thrombomodulin in a mouse transverse aortic constriction model. Thromb Haemost 2007 97 658 664. doi: 10.1160/TH06-12-0690
43. Brunelli T, Prisco D, Fedi S, Rogolino A, Farsi A, Marcucci R, Giusti B, Pratesi C, Pulli R, Gensini GF, Abbate R, Pepe G, High prevalence of mild hyperhomocysteinemia in patients with abdominal aortic aneurysm. J Vasc Surg 2000 32 531 536. doi: 10.1067/mva.2000.107563
44. Xiong W, MacTaggart J, Knispel R, Worth J, Persidsky Y, Baxter BT, Blocking TNF-alpha attenuates aneurysm formation in a murine model. J Immunol 2009 183 2741 2746. doi: 10.4049/jimmunol.0803164
45. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A III, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR, An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J Clin Invest 2009 119 3637 3651. doi: 10.1172/JCI38308
46. Forman HJ, Torres M, Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med 2002 166 12 pt 2 S4 S8. doi: 10.1164/rccm.2206007
47. McNelis JC, Olefsky JM, Macrophages, immunity, and metabolic disease. Immunity 2014 41 36 48. doi: 10.1016/j.immuni.2014.05.010
48. Schultz G, Tedesco MM, Sho E, Nishimura T, Sharif S, Du X, Myles T, Morser J, Dalman RL, Leung LL, Enhanced abdominal aortic aneurysm formation in thrombin-activatable procarboxypeptidase B-deficient mice. Arterioscler Thromb Vasc Biol 2010 30 1363 1370. doi: 10.1161/ATVBAHA.109.202259
49. Franck G, Dai J, Fifre A, Ngo S, Justine C, Michineau S, Allaire E, Gervais M, Reestablishment of the endothelial lining by endothelial cell therapy stabilizes experimental abdominal aortic aneurysms. Circulation 2013 127 1877 1887. doi: 10.1161/CIRCULATIONAHA.113.001677
50. Kager LM, Wiersinga WJ, Roelofs JJ, Stroo I, Achouiti A, van 't Veer C, Conway EM, van der Poll T, Mice lacking the lectin-like domain of thrombomodulin are protected against melioidosis. Crit Care Med 2014 42 e221 e230. doi: 10.1097/CCM.0000000000000134