CARD9 mediates necrotic smooth muscle cell-induced inflammation in macrophages contributing to neointima formation of vein grafts

Cardiovascular Research

Volumn 108, Issue 1, 2015, Pages 148-158

  Liu, Yan ^a   Wang, Ying ^a   Shi, Hongtao ^a   Jia, Lixin ^a   Cheng, Jizhong ^a   Cui, Wei ^a   Li, Huihua ^a   Li, Ping ^a   Du, Jie ^a  

^a CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

CARD9; Cardiovascular inflammation; Macrophage; Neointima; Vein graft

Indexed keywords

CASPASE ASSOCIATED RECRUITMENT DOMAIN 9; COLLAGEN; COLLAGENASE; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; CARD9 PROTEIN, MOUSE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR INFLAMMATION; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE EXPRESSION; IMMUNOFLUORESCENCE TEST; INNATE IMMUNITY; MACROPHAGE; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; VEIN GRAFT; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; INFLAMMATION; MALE; NECROSIS; PATHOLOGY; PHYSIOLOGY; SMOOTH MUSCLE CELL; TRANSPLANTATION; VASCULAR SMOOTH MUSCLE; VEIN;

ANIMALS; CARD SIGNALING ADAPTOR PROTEINS; CELLS, CULTURED; CYTOKINES; INFLAMMATION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NECROSIS; NEOINTIMA; NF-KAPPA B; RNA, MESSENGER; VEINS;

EID: 84943369716     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv211     Document Type: Article

References (49)

1. Bourassa MG. Fate of venous grafts: the past, the present and the future. J Am Coll Cardiol 1991; 17: 1081-1083
2. Bassiouny HS, White S, Glagov S, Choi E, Giddens DP, Zarins CK. Anastomotic intimal hyperplasia: mechanical injury or flow induced. J Vasc Surg 1992; 15: 708-716; discussion 16-17
3. Muto A, Model L, Ziegler K, Eghbalieh SD, Dardik A. Mechanisms of vein graft adaptation to the arterial circulation: insights into the neointimal algorithm and management strategies. Circ J 2010; 74: 1501-1512
4. Predel HG, Yang Z, von Segesser L, Turina M, Buhler FR, Luscher TF. Implications of pulsatile stretch on growth of saphenous vein and mammary artery smooth muscle. Lancet 1992; 340: 878-879
5. Kent KC, Liu B
6. Conte MS, Bandyk DF, Clowes AW, Moneta GL, Seely L, Lorenz TJ, Namini H, Hamdan AD, Roddy SP, Belkin M, Berceli SA, DeMasi RJ, Samson RH, Berman SS. Results of PREVENT III: a multicenter, randomized trial of edifoligide for the prevention of vein graft failure in lower extremity bypass surgery. J Vasc Surg 2006; 43: 742-751; discussion 751
7. Sterpetti AV, Cucina A, Lepidi S, Randone B, Corvino V, DAngelo LS, Cavallaro A. Formation of myointimal hyperplasia and cytokine production in experimental vein grafts. Surgery 1998; 123: 461-469
8. Jiang Z, Berceli SA, Pfahnl CL, Wu L, Goldman D, Tao M, Kagayama M, Matsukawa A, Ozaki CK. Wall shear modulation of cytokines in early vein grafts. J Vasc Surg 2004; 40: 345-350
9. Wolff RA, Tomas JJ, Hullett DA, Stark VE, van Rooijen N, Hoch JR. Macrophage depletion reduces monocyte chemotactic protein-1 and transforming growth factor-beta1 in healing rat vein grafts. J Vasc Surg 2004; 39: 878-888
10. Schepers A, Eefting D, Bonta PI, Grimbergen JM, de Vries MR, vanWeel V, de Vries CJ, Egashira K, van Bockel JH, Quax PH. Anti-MCP-1 gene therapy inhibits vascular smooth muscle cells proliferation and attenuates vein graft thickening both in vitro and in vivo. Arterioscler Thromb Vasc Biol 2006; 26: 2063-2069
11. Zhang L, Sivashanmugam P, Wu JH, Brian L, Exum ST, Freedman NJ, Peppel K. Tumor necrosis factor receptor-2 signaling attenuates vein graft neointima formation by promoting endothelial recovery. Arterioscler Thromb Vasc Biol 2008; 28: 284-289
12. Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell 2010; 140: 798-804
13. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007; 81: 1-5
14. Kanellaki-Kyparissi M, Kouzi-Koliakou K, Marinov G, Knyazev V. Histological study of arterial and venous grafts before their use in aortocoronary bypass surgery. Hellenic J Cardiol 2005; 46: 21-30
15. Hruz P, Eckmann L. Caspase recruitment domain-containing sensors and adaptors in intestinal innate immunity. Curr Opin Gastroenterol 2008; 24: 108-114
16. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nunez G, Flavell RA. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307: 731-734
17. Mariathasan S, Monack DM. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol 2007; 7: 31-40
18. Hara H, Ishihara C, Takeuchi A, Xue L, Morris SW, Penninger JM, Yoshida H, Saito T. Cell type-specific regulation of ITAM-mediated NF-kappaB activation by the adaptors, CARMA1 and CARD9. J Immunol 2008; 181: 918-930
19. Hara H, Ishihara C, Takeuchi A, Imanishi T, Xue L, Morris SW, Inui M, Takai T, Shibuya A, Saijo S, Iwakura Y, Ohno N, Koseki H, Yoshida H, Penninger JM, Saito T. The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-Associated and Toll-like receptors. Nat Immunol 2007; 8: 619-629
20. Hsu YM, Zhang Y, You Y, Wang D, Li H, Duramad O, Qin XF, Dong C, Lin X. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol 2007; 8: 198-205
21. Wu X, Cheng J, Li P, Yang M, Qiu S, Liu P, Du J. Mechano-sensitive transcriptional factor Egr-1 regulates insulin-like growth factor-1 receptor expression and contributes to neointima formation in vein grafts. Arterioscler Thromb Vasc Biol 2010; 30: 471-476
22. Shi HT, Wang Y, Jia LX, Qin YW, Liu Y, Li HH, Qi YF, Du J. Cathepsin S contributes to macrophage migration via degradation of elastic fibre integrity to facilitate vein graft neointimal hyperplasia. Cardiovasc Res 2014; 101: 454-463
23. Cheng J, Wang Y, Liang A, Jia L, Du J. FSP-1 silencing in bone marrow cells suppresses neointima formation in vein graft. Circ Res 2012; 110: 230-240
24. Weischenfeldt J, Porse B. Bone marrow-derived macrophages (BMM): isolation and applications. CSH Protoc 2008; 2008: pdb prot5080
25. Cheng J, Du J. Mechanical stretch simulates proliferation of venous smooth muscle cells through activation of the insulin-like growth factor-1 receptor. Arterioscler Thromb Vasc Biol 2007; 27: 1744-1751
26. Li P, Li YL, Li ZY, Wu YN, Zhang CC, A X, Wang CX, Shi HT, Hui MZ, Xie B, Ahmed M, Du J. Cross talk between vascular smooth muscle cells and monocytes through interleukin-1beta/interleukin-18 signaling promotes vein graft thickening. Arterioscler Thromb Vasc Biol 2014; 34: 2001-2011
27. Yang M, Zheng J, Miao Y, Wang Y, Cui W, Guo J, Qiu S, Han Y, Jia L, Li H, Cheng J, Du J. Serum-glucocorticoid regulated kinase 1 regulates alternatively activated macrophage polarization contributing to angiotensin II-induced inflammation and cardiac fibrosis. Arterioscler Thromb Vasc Biol 2012; 32: 1675-1686
28. Lin J, Li H, Yang M, Ren J, Huang Z, Han F, Huang J, Ma J, Zhang D, Zhang Z, Wu J, Huang D, Qiao M, Jin G, Wu Q, Huang Y, Du J, Han J. A role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep 2013; 3: 200-210
29. Zhang L, Ma Y, Zhang J, Cheng J, Du J. A new cellular signaling mechanism for angiotensin II activation of NF-kappaB: an IkappaB-independent, RSK-mediated phosphorylation of p65. Arterioscler Thromb Vasc Biol 2005; 25: 1148-1153
30. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 1995; 21: 1465-1468
31. Cummings BS, Schnellmann RG. Measurement of cell death in mammalian cells. Curr Protoc Pharmacol 2004; Chapter 12: Unit 12.8
32. Zhang J, Herrera AM, Pare PD, Seow CY. Dense-body aggregates as plastic structures supporting tension in smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2010; 299: L631-L638
33. Ecker J, Liebisch G, Englmaier M, Grandl M, Robenek H, Schmitz G. Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocytes. Proc Natl Acad Sci USA 2010; 107: 7817-7822
34. Smith CC, Yellon DM. Necroptosis, necrostatins and tissue injury. J Cell Mol Med 2011; 15: 1797-1806
35. Degterev A, Yuan J. Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 2008; 9: 378-390
36. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005; 1: 112-119
37. Wu X, Mi Y, Yang H, Hu A, Zhang Q, Shang C. The activation of HMGB1 as a progression factor on inflammation response in normal human bronchial epithelial cells through RAGE/JNK/NF-kappaB pathway. Mol Cell Biochem 2013; 380: 249-257
38. Bertin J, Guo Y, Wang L, Srinivasula SM, Jacobson MD, Poyet JL, Merriam S, Du MQ, Dyer MJ, Robison KE, DiStefano PS, Alnemri ES. CARD9 is a novel caspase recruitment domain-containing protein that interacts with BCL10/CLAP and activates NF-kappa B. J Biol Chem 2000; 275: 41082-41086
39. Rodriguez E, Lambert EH, Magno MG, Mannion JD. Contractile smooth muscle cell apoptosis early after saphenous vein grafting. Ann Thorac Surg 2000; 70: 1145-1153
40. de Haan JJ, Smeets MB, Pasterkamp G, Arslan F. Danger signals in the initiation of the inflammatory response after myocardial infarction. Mediators Inflamm 2013; 2013: 206039
41. Clarke MC, Talib S, Figg NL, Bennett MR. Vascular smooth muscle cell apoptosis induces interleukin-1-directed inflammation: effects of hyperlipidemia-mediated inhibition of phagocytosis. Circ Res 2010; 106: 363-372
42. Zheng Y, Humphry M, Maguire JJ, Bennett MR, Clarke MC. Intracellular interleukin-1 receptor 2 binding prevents cleavage and activity of interleukin-1alpha, controlling necrosis-induced sterile inflammation. Immunity 2013; 38: 285-295
43. Phongsisay V, Iizasa E, Hara H, Yoshida H. Evidence for TLR4 and FcRgamma-CARD9 activation by cholera toxin B subunit and its direct bindings to TREM2 and LMIR5 receptors. Mol Immunol 2015; 66: 463-471
44. Hoch JR, Stark VK, van Rooijen N, Kim JL, Nutt MP, Warner TF. Macrophage depletion alters vein graft intimal hyperplasia. Surgery 1999; 126: 428-437
45. Nilsson J. Cytokines and smooth muscle cells in atherosclerosis. Cardiovasc Res 1993; 27: 1184-1190
46. Alexander MR, Murgai M, Moehle CW, Owens GK. Interleukin-1beta modulates smooth muscle cell phenotype to a distinct inflammatory state relative to PDGF-DD via NF-kappaB-dependent mechanisms. Physiol Genomics 2012; 44: 417-429
47. Stamatiou R, Paraskeva E, Gourgoulianis K, Molyvdas PA, Hatziefthimiou A. Cytokines and growth factors promote airway smooth muscle cell proliferation. ISRN Inflamm 2012; 2012: 731472
48. Viedt C, Vogel J, Athanasiou T, Shen W, Orth SR, Kubler W, Kreuzer J. Monocyte chemoattractant protein-1 induces proliferation and interleukin-6 production in human smooth muscle cells by differential activation of nuclear factor-kappaB and activator protein-1. Arterioscler Thromb Vasc Biol 2002; 22: 914-920
49. Parenti A, Bellik L, Brogelli L, Filippi S, Ledda F. Endogenous VEGF-A is responsible for mitogenic effects of MCP-1 on vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2004; 286: H1978-H1984