Dimethylfumarate attenuates restenosis after acute vascular injury by cell-specific and Nrf2-dependent mechanisms

Redox Biology

Volumn 2, Issue 1, 2014, Pages 855-864

  Oh, Chang Joo ^a   Park, Sungmi ^b   Kim, Joon Young ^a,c   Kim, Han Jong ^a,d   Jeoung, Nam Ho ^e   Choi, Young Keun ^a   Go, Younghoon ^a   Park, Keun Gyu ^a,b   Lee, In Kyu ^a,b  

^a Kyungpook National University School of Medicine   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c Gwangju Institute of Science and Technology (GIST)   (South Korea)

^d Chonnam National University Research Institute of Medical Sciences   (South Korea)

^e The Catholic University of Korea   (South Korea)

Author keywords

Cell cycle protein; Neointimal hyperplasia; P53 Pathway; Reactive oxygen species; Restenosis; Vascular remodeling

Indexed keywords

CD31 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FUMARIC ACID DIMETHYL ESTER; HEME OXYGENASE 1; MESSENGER RNA; PROTEIN P21; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; FUMARIC ACID DERIVATIVE; IMMUNOSUPPRESSIVE AGENT; NQO1 PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BLOOD VESSEL INJURY; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; EXPERIMENTAL BALLOON CATHETER INJURY; G1 PHASE CELL CYCLE CHECKPOINT; GENE TARGETING; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; RAT; RESTENOSIS; SMOOTH MUSCLE FIBER; TRANSLUMINAL CORONARY ANGIOPLASTY; ANIMAL; ANTAGONISTS AND INHIBITORS; CAROTID ARTERY INJURY; CELL CULTURE; CORONARY RESTENOSIS; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; HYPERPLASIA; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; CAROTID ARTERY INJURIES; CELL PROLIFERATION; CELLS, CULTURED; CORONARY RESTENOSIS; FUMARATES; G1 PHASE CELL CYCLE CHECKPOINTS; HEME OXYGENASE-1; HUMANS; HYPERPLASIA; IMMUNOSUPPRESSIVE AGENTS; MALE; MUSCLE, SMOOTH, VASCULAR; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84903824542     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2014.06.003     Document Type: Article

References (31)

1. Preisack M.B., Karsch K.R. The paradigm of restenosis following percutaneous transluminal coronary angioplasty. European Heart Journal 1993, 14(Suppl. i):S187-S192.
2. Morice M.C., Serruys P.W., Sousa J.E., Fajadet J., Ban Hayashi E., Perin M., Colombo A., Schuler G., Barragan P., Guagliumi G., Molnar F., Falotico R. A randomized comparison of a sirolimus-eluting stent with a standard stent for coronary revascularization. New England Journal of Medicine 2002, 346:1773-1780. http://www.ncbi.nlm.nih.gov/pubmed/12050336, 10.1016/j.redox.2014.06.003.
3. Moses J.W., Leon M.B., Popma J.J., Fitzgerald P.J., Holmes D.R., O'Shaughnessy C., Caputo R.P., Kereiakes D.J., Williams D.O., Teirstein P.S., Jaeger J.L., Kuntz R.E. Sirolimus-eluting stents versus standard stents in patients with stenosis in a native coronary artery. New England Journal of Medicine 2003, 349:1315-1323. http://www.ncbi.nlm.nih.gov/pubmed/14523139, 10.1016/j.redox.2014.06.003.
4. Bovenschen H.J., Langewouters A.M., van de Kerkhof P.C. Dimethylfumarate for psoriasis: pronounced effects on lesional T-cell subsets, epidermal proliferation and differentiation, but not on natural killer T cells in immunohistochemical study. American Journal of Clinical Dermatology 2010, 11:343-350. http://www.ncbi.nlm.nih.gov/pubmed/20553063, 10.1016/j.redox.2014.06.003.
5. Fox R.J., Miller D.H., Phillips J.T., Hutchinson M., Havrdova E., Kita M., Yang M., Raghupathi K., Novas M., Sweetser M.T., Viglietta V., Dawson K.T. Placebo-controlled phase 3 study of oral BG-12 or glatiramer in multiple sclerosis. New England Journal of Medicine 2012, 367:1087-1097. http://www.ncbi.nlm.nih.gov/pubmed/22992072, 10.1016/j.redox.2014.06.003.
6. Kappos L., Gold R., Miller D.H., Macmanus D.G., Havrdova E., Limmroth V., Polman C.H., Schmierer K., Yousry T.A., Yang M., Eraksoy M., Meluzinova E., Rektor I., Dawson K.T., Sandrock A.W., O'Neill G.N. Efficacy and safety of oral fumarate in patients with relapsing-remitting multiple sclerosis: a multicentre, randomised, double-blind, placebo-controlled phase IIb study. Lancet 2008, 372:1463-1472. http://www.ncbi.nlm.nih.gov/pubmed/18970976, 10.1016/j.redox.2014.06.003.
7. Ashrafian H., Czibik G., Bellahcene M., Aksentijević D., Smith A.C., Mitchell S.J., Dodd M.S., Kirwan J., Byrne J.J., Ludwig C., Isackson H., Yavari A., Støttrup N.B., Contractor H., Cahill T.J., Sahgal N., Ball D.R., Birkler R.I., Hargreaves I., Tennant D.A., Land J., Lygate C.A., Johannsen M., Kharbanda R.K., Neubauer S., Redwood C., de Cabo R., Ahmet I., Talan M., Günther U.L., Robinson A.J., Viant M.R., Pollard P.J., Tyler D.J., Watkins H. Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway. Cell Metabolism 2012, 15:361-371. http://www.ncbi.nlm.nih.gov/pubmed/22405071, 10.1016/j.redox.2014.06.003.
8. Oh C.J., Kim J.Y., Choi Y.K., Kim H.J., Jeong J.Y., Bae K.H., Park K.G., Lee I.K. Dimethylfumarate attenuates renal fibrosis via NF-E2-related factor 2-mediated inhibition of transforming growth factor-β/Smad signaling. PloS One 2012, 7:e45870. http://www.ncbi.nlm.nih.gov/pubmed/23056222, 10.1016/j.redox.2014.06.003.
9. Kang H.J., Seo H.A., Go Y., Oh C.J., Jeoung N.H., Park K.G., Lee I.K. Dimethylfumarate suppresses adipogenic differentiation in 3T3-L1 preadipocytes through inhibition of STAT3 activity. PloS One 2013, 8:e61411. http://www.ncbi.nlm.nih.gov/pubmed/23637829, 10.1016/j.redox.2014.06.003.
10. Seidel P., Goulet S., Hostettler K., Tamm M., Roth M. DMF inhibits PDGF-BB induced airway smooth muscle cell proliferation through induction of heme-oxygenase-1. Respiratory Research 2010, 11:145. http://www.ncbi.nlm.nih.gov/pubmed/20961405, 10.1016/j.redox.2014.06.003.
11. Lüscher T.F., Steffel J., Eberli F.R., Joner M., Nakazawa G., Tanner F.C., Virmani R. Drug-eluting stent and coronary thrombosis: biological mechanisms and clinical implications. Circulation 2007, 115:1051-1058. http://www.ncbi.nlm.nih.gov/pubmed/17325255, 10.1016/j.redox.2014.06.003.
12. Loewe R., Holnthoner W., Gröger M., Pillinger M., Gruber F., Mechtcheriakova D., Hofer E., Wolff K., Petzelbauer P. Dimethylfumarate inhibits TNF-induced nuclear entry of NF-kappa B/p65 in human endothelial cells. Journal of Immunology 2002, 168:4781-4787. 10.1016/j.redox.2014.06.003.
13. Tanaka H., Sukhova G., Schwartz D., Libby P. Proliferating arterial smooth muscle cells after balloon injury express TNF-alpha but not interleukin-1 or basic fibroblast growth factor. Arteriosclerosis, Thrombosis, and Vascular Biology 1996, 16:12-18. http://www.ncbi.nlm.nih.gov/pubmed/8548411, 10.1016/j.redox.2014.06.003.
14. Krasinski K., Spyridopoulos I., Kearney M., Losordo D.W. in vivo blockade of tumor necrosis factor-alpha accelerates functional endothelial recovery after balloon angioplasty. Circulation 2001, 104:1754-1756. http://www.ncbi.nlm.nih.gov/pubmed/11591609, 10.1016/j.redox.2014.06.003.
15. Cho H.Y., Reddy S.P., Yamamoto M., Kleeberger S.R. The transcription factor NRF2 protects against pulmonary fibrosis. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2004, 18:1258-1260. http://www.ncbi.nlm.nih.gov/pubmed/15208274.
16. Zheng H., Whitman S.A., Wu W., Wondrak G.T., Wong P.K., Fang D., Zhang D.D. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 2011, 60:3055-3066. http://www.ncbi.nlm.nih.gov/pubmed/22025779, 10.1016/j.redox.2014.06.003.
17. Xu W., Shao L., Zhou C., Wang H., Guo J. Upregulation of Nrf2 expression in non-alcoholic fatty liver and steatohepatitis. Hepato-Gastroenterology 2011, 58:2077-2080. http://www.ncbi.nlm.nih.gov/pubmed/22024078.
18. Kim J.Y., Cho H.J., Sir J.J., Kim B.K., Hur J., Youn S.W., Yang H.M., Jun S.I., Park K.W., Hwang S.J., Kwon Y.W., Lee H.Y., Kang H.J., Oh B.H., Park Y.B., Kim H.S. Sulfasalazine induces haem oxygenase-1 via ROS-dependent Nrf2 signalling, leading to control of neointimal hyperplasia. Cardiovascular Research 2009, 82:550-560. http://www.ncbi.nlm.nih.gov/pubmed/19234301, 10.1016/j.redox.2014.06.003.
19. Ahn J.D., Morishita R., Kaneda Y., Lee S.J., Kwon K.Y., Choi S.Y., Lee K.U., Park J.Y., Moon I.J., Park J.G., Yoshizumi M., Ouchi Y., Lee I.K. Inhibitory effects of novel AP-1 decoy oligodeoxynucleotides on vascular smooth muscle cell proliferation in vitro and neointimal formation in vivo. Circulation Research 2002, 90:1325-1332. http://www.ncbi.nlm.nih.gov/pubmed/12089071, 10.1016/j.redox.2014.06.003.
20. Kim H.J., Yoo E.K., Kim J.Y., Choi Y.K., Lee H.J., Kim J.K., Jeoung N.H., Lee K.U., Park I.S., Min B.H., Park K.G., Lee C.H., Aronow B.J., Sata M., Lee I.K. Protective role of clusterin/apolipoprotein J against neointimal hyperplasia via antiproliferative effect on vascular smooth muscle cells and cytoprotective effect on endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 2009, 29:1558-1564. http://www.ncbi.nlm.nih.gov/pubmed/19696405, 10.1016/j.redox.2014.06.003.
21. Kim H.J., Kim J.Y., Lee S.J., Kim H.J., Oh C.J., Choi Y.K., Lee H.J., Do J.Y., Kim S.Y., Kwon T.K., Choi H.S., Lee M.O., Park I.S., Park K.G., Lee K.U. Alpha-lipoic acid prevents neointimal hyperplasia via induction of p38 mitogen-activated protein kinase/Nur77-mediated apoptosis of vascular smooth muscle cells and accelerates postinjury reendothelialization. Arteriosclerosis, Thrombosis, and Vascular Biology 2010, 30:2164-2172. http://www.ncbi.nlm.nih.gov/pubmed/20829507, 10.1016/j.redox.2014.06.003.
22. Kim S.Y., Jeoung N.H., Oh C.J., Choi Y.K., Lee H.J., Kim H.J., Kim J.Y., Hwang J.H., Tadi S., Yim Y.H., Lee K.U., Park K.G., Huh S., Min K.N., Jeong K.H., Park M.G., Kwak T.H., Kweon G.R., Inukai K., Shong M., Lee I.K. Activation of NAD(P)H:quinone oxidoreductase 1 prevents arterial restenosis by suppressing vascular smooth muscle cell proliferation. Circulation Research 2009, 104:842-850. http://www.ncbi.nlm.nih.gov/pubmed/19229058, 10.1016/j.redox.2014.06.003.
23. Rodriguez A.I., Gangopadhyay A., Kelley E.E., Pagano P.J., Zuckerbraun B.S., Bauer P.M. HO-1 and CO decrease platelet-derived growth factor-induced vascular smooth muscle cell migration via inhibition of Nox1. Arteriosclerosis, Thrombosis, and Vascular Biology 2010, 30:98-104. http://www.ncbi.nlm.nih.gov/pubmed/19875720, 10.1016/j.redox.2014.06.003.
24. Rastogi S., Rizwani W., Joshi B., Kunigal S., Chellappan S.P. TNF-alpha response of vascular endothelial and vascular smooth muscle cells involve differential utilization of ASK1 kinase and p73. Cell Death and Differentiation 2012, 19:274-283. http://www.ncbi.nlm.nih.gov/pubmed/21738216, 10.1016/j.redox.2014.06.003.
25. Mrowietz U., Altmeyer P., Bieber T., Rocken M., Schopf R.E., Sterry W. Treatment of psoriasis with fumaric acid esters (Fumaderm). Journal der Deutschen Dermatologischen Gesellschaft (Journal of the German Society of Dermatology) 2007, 5:716-717.
26. Loewe R., Valero T., Kremling S., Pratscher B., Kunstfeld R., Pehamberger H., Petzelbauer P. Dimethylfumarate impairs melanoma growth and metastasis. Cancer Research 2006, 66:11888-11896. http://www.ncbi.nlm.nih.gov/pubmed/17178886, 10.1016/j.redox.2014.06.003.
27. Mitra A.K., Agrawal D.K. In stent restenosis: bane of the stent era. Journal of Clinical Pathology 2006, 59:232-239. http://www.ncbi.nlm.nih.gov/pubmed/16505271, 10.1016/j.redox.2014.06.003.
28. Vandermeeren M., Janssens S., Borgers M., Geysen J. Dimethylfumarate is an inhibitor of cytokine-induced E-selectin, VCAM-1, and ICAM-1 expression in human endothelial cells. Biochemical and Biophysical Research Communications 1997, 234:19-23. http://www.ncbi.nlm.nih.gov/pubmed/9168952, 10.1016/j.redox.2014.06.003.
29. Rubant S.A., Ludwig R.J., Diehl S., Hardt K., Kaufmann R., Pfeilschifter J.M., Boehncke W.H. Dimethylfumarate reduces leukocyte rolling in vivo through modulation of adhesion molecule expression. Journal of Investigative Dermatology 2008, 128:326-331. http://www.ncbi.nlm.nih.gov/pubmed/17671516.
30. Goukassian D.A., Kishore R., Krasinski K., Dolan C., Luedemann C., Yoon Y.S., Kearney M., Hanley A., Ma H., Asahara T., Isner J.M., Losordo D.W. Engineering the response to vascular injury: divergent effects of deregulated E2F1 expression on vascular smooth muscle cells and endothelial cells result in endothelial recovery and inhibition of neointimal growth. Circulation Research 2003, 93:162-169. http://www.ncbi.nlm.nih.gov/pubmed/12829616, 10.1016/j.redox.2014.06.003.
31. Moraes J.A., Barcellos-de-Souza P., Rodrigues G., Nascimento-Silva V., Silva S.V., Assreuy J., Arruda M.A., Barja-Fidalgo C. Heme modulates smooth muscle cell proliferation and migration via NADPH oxidase: a counter-regulatory role for heme oxygenase system. Atherosclerosis 2012, 224:394-400. http://www.ncbi.nlm.nih.gov/pubmed/22954673, 10.1016/j.redox.2014.06.003.