Adam17 Deficiency promotes atherosclerosis by enhanced TNFR2 signaling in Mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 2, 2017, Pages 247-257

  Nicolaou, Alexandros ^a,b   Zhao, Zhen ^a   Northoff, Bernd H ^a   Sass, Kristina ^a   Herbst, Andreas ^a   Kohlmaier, Alexander ^a   Chalaris, Athena ^c   Wolfrum, Christian ^a   Weber, Christian ^a,b,d,e   Steffens, Sabine ^e   Rose John, Stefan ^c   Teupser, Daniel ^a   Holdt, Lesca M ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d ETH ZURICH   (Switzerland)

^e DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

atherosclerosis; metalloproteases; models, genetic; receptors, tumor necrosis factor; vascular disease

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CASPASE 3; CD68 ANTIGEN; FRACTALKINE; GAMMA INTERFERON; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 1 RECEPTOR TYPE II; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6 RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR; ADAM17 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; AORTA ROOT; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW DERIVED MACROPHAGE; CELL ADHESION; CELL MEMBRANE; CELL PROLIFERATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE SILENCING; HETEROZYGOSITY; HOMOZYGOSITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAW 264.7 CELL LINE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; AORTA; AORTIC DISEASE; ATHEROSCLEROSIS; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DISEASE MODEL; ENDOTHELIUM CELL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PATHOLOGY; PHENOTYPE; TIME FACTOR; VASCULAR SMOOTH MUSCLE;

ADAM17 PROTEIN; ANIMALS; AORTA; AORTIC DISEASES; APOPTOSIS; ATHEROSCLEROSIS; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85007252576     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.308682     Document Type: Article

References (63)

1. Lusis AJ, Mar R, Pajukanta P. Genetics of atherosclerosis. Annu Rev Genomics Hum Genet. 2004;5:189-218. doi: 10.1146/annurev. genom.5.061903.175930.
2. Teupser D, Tan M, Persky AD, Breslow JL. Atherosclerosis quantitative trait loci are sex-and lineage-dependent in an intercross of C57BL/6 and FVB/N low-density lipoprotein receptor-/-mice. Proc Natl Acad Sci USA. 2006;103:123-128. doi: 10.1073/pnas.0509570102.
3. Holdt LM, Thiery J, Breslow JL, Teupser D. Increased ADAM17 mRNA expression and activity is associated with atherosclerosis resistance in LDL-receptor deficient mice. Arterioscler Thromb Vasc Biol. 2008;28:1097-1103. doi: 10.1161/ATVBAHA.108.165654.
4. Canault M, Peiretti F, Kopp F, Bonardo B, Bonzi MF, Coudeyre JC, Alessi MC, Juhan-Vague I, Nalbone G. The TNF alpha converting enzyme (TACE/ADAM17) is expressed in the atherosclerotic lesions of apolipoprotein E-deficient mice: possible contribution to elevated plasma levels of soluble TNF alpha receptors. Atherosclerosis. 2006;187:82-91. doi: 10.1016/j.atherosclerosis.2005.08.031.
5. Satoh M, Ishikawa Y, Itoh T, Minami Y, Takahashi Y, Nakamura M. The expression of TNF-alpha converting enzyme at the site of ruptured plaques in patients with acute myocardial infarction. Eur J Clin Invest. 2008;38:97-105. doi: 10.1111/j.1365-2362.2007.01912.x.
6. Dreymueller D, Uhlig S, Ludwig A. ADAM-family metalloproteinases in lung inflammation: potential therapeutic targets. Am J Physiol Lung Cell Mol Physiol. 2015;308:L325-L343. doi: 10.1152/ ajplung.00294.2014.
7. White JM. ADAMs: modulators of cell-cell and cell-matrix interactions. Curr Opin Cell Biol. 2003;15:598-606.
8. Blobel CP, White JM. Structure, function and evolutionary relationship of proteins containing a disintegrin domain. Curr Opin Cell Biol. 1992;4:760-765.
9. Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature. 1997;385:729-733. doi: 10.1038/385729a0.
10. Scheller J, Chalaris A, Garbers C, Rose-John S. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 2011;32:380-387. doi: 10.1016/j.it.2011.05.005.
11. Koenen RR, Pruessmeyer J, Soehnlein O, Fraemohs L, Zernecke A, Schwarz N, Reiss K, Sarabi A, Lindbom L, Hackeng TM, Weber C, Ludwig A. Regulated release and functional modulation of junctional adhesion molecule A by disintegrin metalloproteinases. Blood. 2009;113:4799-4809. doi: 10.1182/blood-2008-04-152330.
12. Gooz M. ADAM-17: the enzyme that does it all. Crit Rev Biochem Mol Biol. 2010;45:146-169. doi: 10.3109/10409231003628015.
13. Zheng X, Jiang F, Katakowski M, Zhang ZG, Lu QE, Chopp M. ADAM17 promotes breast cancer cell malignant phenotype through EGFR-PI3KAKT activation. Cancer Biol Ther. 2009;8:1045-1054.
14. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med. 2011;17:1410-1422. doi: 10.1038/nm.2538.
15. Peschon JJ, Slack JL, Reddy P, et al. An essential role for ectodomain shedding in mammalian development. Science. 1998;282:1281-1284.
16. Chalaris A, Adam N, Sina C, et al. Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J Exp Med. 2010;207:1617-1624. doi: 10.1084/jem.20092366.
17. Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y, Toyama Y, Blobel CP. Cutting edge: TNF-alpha-converting enzyme (TACE/ ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J Immunol. 2007;179:2686-2689.
18. Gravano DM, McLelland BT, Horiuchi K, Manilay JO. ADAM17 deletion in thymic epithelial cells alters aire expression without affecting T cell developmental progression. PLoS One. 2010;5:e13528. doi: 10.1371/ journal.pone.0013528.
19. Horiuchi K, Kimura T, Miyamoto T, Miyamoto K, Akiyama H, Takaishi H, Morioka H, Nakamura T, Okada Y, Blobel CP, Toyama Y. Conditional inactivation of TACE by a Sox9 promoter leads to osteoporosis and increased granulopoiesis via dysregulation of IL-17 and G-CSF. J Immunol. 2009;182:2093-2101. doi: 10.4049/jimmunol.0802491.
20. Driscoll WS, Vaisar T, Tang J, Wilson CL, Raines EW. Macrophage ADAM17 deficiency augments CD36-dependent apoptotic cell uptake and the linked anti-inflammatory phenotype. Circ Res. 2013;113:52-61. doi: 10.1161/CIRCRESAHA.112.300683.
21. Weskamp G, Mendelson K, Swendeman S, Le Gall S, Ma Y, Lyman S, Hinoki A, Eguchi S, Guaiquil V, Horiuchi K, Blobel CP. Pathological neovascularization is reduced by inactivation of ADAM17 in endothelial cells but not in pericytes. Circ Res. 2010;106:932-940. doi: 10.1161/ CIRCRESAHA.109.207415.
22. Wilson CL, Gough PJ, Chang CA, Chan CK, Frey JM, Liu Y, Braun KR, Chin MT, Wight TN, Raines EW. Endothelial deletion of ADAM17 in mice results in defective remodeling of the semilunar valves and cardiac dysfunction in adults. Mech Dev. 2013;130:272-289. doi: 10.1016/j. mod.2013.01.001.
23. Yoda M, Kimura T, Tohmonda T, Morioka H, Matsumoto M, Okada Y, Toyama Y, Horiuchi K. Systemic overexpression of TNFα-converting enzyme does not lead to enhanced shedding activity in vivo. PLoS One. 2013;8:e54412. doi: 10.1371/journal.pone.0054412.
24. Teupser D, Persky AD, Breslow JL. Induction of atherosclerosis by lowfat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/ NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler Thromb Vasc Biol. 2003;23:1907-1913. doi: 10.1161/01.ATV.0000090126.34881.B1.
25. Grell M, Douni E, Wajant H, Löhden M, Clauss M, Maxeiner B, Georgopoulos S, Lesslauer W, Kollias G, Pfizenmaier K, Scheurich P. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell. 1995;83:793-802.
26. Pan S, An P, Zhang R, He X, Yin G, Min W. Etk/Bmx as a tumor necrosis factor receptor type 2-specific kinase: role in endothelial cell migration and angiogenesis. Mol Cell Biol. 2002;22:7512-7523.
27. Qiu Y, Kung HJ. Signaling network of the Btk family kinases. Oncogene. 2000;19:5651-5661. doi: 10.1038/sj.onc.1203958.
28. Chen S, Jiang X, Gewinner CA, Asara JM, Simon NI, Cai C, Cantley LC, Balk SP. Tyrosine kinase BMX phosphorylates phosphotyrosine-primed motif mediating the activation of multiple receptor tyrosine kinases. Sci Signal. 2013;6:ra40. doi: 10.1126/scisignal.2003936.
29. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241. doi: 10.1038/35025203.
30. Pimentel-Muiños FX, Seed B. Regulated commitment of TNF receptor signaling: a molecular switch for death or activation. Immunity. 1999;11:783-793.
31. Bech-Serra JJ, Santiago-Josefat B, Esselens C, Saftig P, Baselga J, Arribas J, Canals F. Proteomic identification of desmoglein 2 and activated leukocyte cell adhesion molecule as substrates of ADAM17 and ADAM10 by difference gel electrophoresis. Mol Cell Biol. 2006;26:5086-5095. doi: 10.1128/MCB.02380-05.
32. Garton KJ, Gough PJ, Philalay J, Wille PT, Blobel CP, Whitehead RH, Dempsey PJ, Raines EW. Stimulated shedding of vascular cell adhesion molecule 1 (VCAM-1) is mediated by tumor necrosis factor-alpha-converting enzyme (ADAM 17). J Biol Chem. 2003;278:37459-37464. doi: 10.1074/jbc.M305877200.
33. Tsakadze NL, Sithu SD, Sen U, English WR, Murphy G, D'Souza SE. Tumor necrosis factor-alpha-converting enzyme (TACE/ADAM-17) mediates the ectodomain cleavage of intercellular adhesion molecule-1 (ICAM-1). J Biol Chem. 2006;281:3157-3164. doi: 10.1074/jbc.M510797200.
34. Schreyer SA, Vick CM, LeBoeuf RC. Loss of lymphotoxin-alpha but not tumor necrosis factor-alpha reduces atherosclerosis in mice. J Biol Chem. 2002;277:12364-12368. doi: 10.1074/jbc.M111727200.
35. Branén L, Hovgaard L, Nitulescu M, Bengtsson E, Nilsson J, Jovinge S. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2004;24:2137-2142. doi: 10.1161/01.ATV.0000143933.20616.1b.
36. Canault M, Peiretti F, Mueller C, Kopp F, Morange P, Rihs S, Portugal H, Juhan-Vague I, Nalbone G. Exclusive expression of transmembrane TNF-alpha in mice reduces the inflammatory response in early lipid lesions of aortic sinus. Atherosclerosis. 2004;172:211-218. doi: 10.1016/j. atherosclerosis.2003.10.004.
37. Ohta H, Wada H, Niwa T, Kirii H, Iwamoto N, Fujii H, Saito K, Sekikawa K, Seishima M. Disruption of tumor necrosis factor-alpha gene diminishes the development of atherosclerosis in ApoE-deficient mice. Atherosclerosis. 2005;180:11-17. doi: 10.1016/j.atherosclerosis.2004.11.016.
38. Xiao N, Yin M, Zhang L, Qu X, Du H, Sun X, Mao L, Ren G, Zhang C, Geng Y, An L, Pan J. Tumor necrosis factor-alpha deficiency retards early fatty-streak lesion by influencing the expression of inflammatory factors in apoE-null mice. Mol Genet Metab. 2009;96:239-244. doi: 10.1016/j. ymgme.2008.11.166.
39. Boesten LS, Zadelaar AS, van Nieuwkoop A, Gijbels MJ, de Winther MP, Havekes LM, van Vlijmen BJ. Tumor necrosis factor-alpha promotes atherosclerotic lesion progression in APOE∗3-Leiden transgenic mice. Cardiovasc Res. 2005;66:179-185. doi: 10.1016/j.cardiores.2005.01.001.
40. Fischer R, Maier O, Naumer M, Krippner-Heidenreich A, Scheurich P, Pfizenmaier K. Ligand-induced internalization of TNF receptor 2 mediated by a di-leucin motif is dispensable for activation of the NFκB pathway. Cell Signal. 2011;23:161-170. doi: 10.1016/j.cellsig.2010.08.016.
41. Chandrasekharan UM, Mavrakis L, Bonfield TL, Smith JD, DiCorleto PE. Decreased atherosclerosis in mice deficient in tumor necrosis factor-alpha receptor-II (p75). Arterioscler Thromb Vasc Biol. 2007;27:e16-e17. doi: 10.1161/01.ATV.0000255551.33365.22.
42. Lucas R, Juillard P, Decoster E, Redard M, Burger D, Donati Y, Giroud C, Monso-Hinard C, De Kesel T, Buurman WA, Moore MW, Dayer JM, Fiers W, Bluethmann H, Grau GE. Crucial role of tumor necrosis factor (TNF) receptor 2 and membrane-bound TNF in experimental cerebral malaria. Eur J Immunol. 1997;27:1719-1725. doi: 10.1002/eji.1830270719.
43. Bertok S, Wilson MR, Dorr AD, Dokpesi JO, O'Dea KP, Marczin N, Takata M. Characterization of TNF receptor subtype expression and signaling on pulmonary endothelial cells in mice. Am J Physiol Lung Cell Mol Physiol. 2011;300:L781-L789. doi: 10.1152/ajplung.00326.2010.
44. Loetscher H, Stueber D, Banner D, Mackay F, Lesslauer W. Human tumor necrosis factor alpha (TNF alpha) mutants with exclusive specificity for the 55-kDa or 75-kDa TNF receptors. J Biol Chem. 1993;268:26350-26357.
45. Tartaglia LA, Ayres TM, Wong GH, Goeddel DV. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 1993;74:845-853.
46. Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell. 2003;114:181-190.
47. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145:341-355. doi: 10.1016/j.cell.2011.04.005.
48. Stoneman VE, Bennett MR. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci (Lond). 2004;107:343-354. doi: 10.1042/CS20040086.
49. Kitagawa K, Matsumoto M, Sasaki T, Hashimoto H, Kuwabara K, Ohtsuki T, Hori M. Involvement of ICAM-1 in the progression of atherosclerosis in APOE-knockout mice. Atherosclerosis. 2002;160:305-310.
50. Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest. 2001;107:1255-1262. doi: 10.1172/JCI11871.
51. Teupser D, Pavlides S, Tan M, Gutierrez-Ramos JC, Kolbeck R, Breslow JL. Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci USA. 2004;101:17795-17800. doi: 10.1073/pnas.0408096101.
52. Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M. Lack of interleukin-1beta decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:656-660. doi: 10.1161/01.ATV.0000064374.15232.C3.
53. Dekkers PE, Lauw FN, ten Hove T, te Velde AA, Lumley P, Becherer D, van Deventer SJ, van der Poll T. The effect of a metalloproteinase inhibitor (GI5402) on tumor necrosis factor-alpha (TNF-alpha) and TNF-alpha receptors during human endotoxemia. Blood. 1999;94:2252-2258.
54. Grootveld M, McDermott MF. BMS-561392. Bristol-Myers Squibb. Curr Opin Investig Drugs. 2003;4:598-602.
55. Zhou BB, Peyton M, He B, et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell. 2006;10:39-50. doi: 10.1016/j.ccr.2006.05.024.
56. Fridman JS, Caulder E, Hansbury M, et al. Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin Cancer Res. 2007;13:1892-1902. doi: 10.1158/1078-0432. CCR-06-2116.
57. Thabet MM, Huizinga TW. Drug evaluation: apratastat, a novel TACE/ MMP inhibitor for rheumatoid arthritis. Curr Opin Investig Drugs. 2006;7:1014-1019.
58. Morimoto Y, Nishikawa K, Ohashi M. KB-R7785, a novel matrix metalloproteinase inhibitor, exerts its antidiabetic effect by inhibiting tumor necrosis factor-alpha production. Life Sci. 1997;61:795-803.
59. Moss ML, Sklair-Tavron L, Nudelman R. Drug insight: tumor necrosis factor-converting enzyme as a pharmaceutical target for rheumatoid arthritis. Nat Clin Pract Rheumatol. 2008;4:300-309. doi: 10.1038/ ncprheum0797.
60. Arribas J, Esselens C. ADAM17 as a therapeutic target in multiple diseases. Curr Pharm Des. 2009;15:2319-2335.
61. Ban L, Zhang J, Wang L, Kuhtreiber W, Burger D, Faustman DL. Selective death of autoreactive T cells in human diabetes by TNF or TNF receptor 2 agonism. Proc Natl Acad Sci USA. 2008;105:13644-13649. doi: 10.1073/ pnas.0803429105.
62. Faustman D, Davis M. TNF receptor 2 pathway: drug target for autoimmune diseases. Nat Rev Drug Discov. 2010;9:482-493. doi: 10.1038/nrd3030.
63. Roubille C, Richer V, Starnino T, et al. The effects of tumour necrosis factor inhibitors, methotrexate, non-steroidal anti-inflammatory drugs and corticosteroids on cardiovascular events in rheumatoid arthritis, psoriasis and psoriatic arthritis: a systematic review and meta-analysis. Ann Rheum Dis. 2015;74:480-489. doi: 10.1136/annrheumdis-2014-206624.