Activation of Nrf2 by dimethyl fumarate improves vascular calcification

Vascular Pharmacology

Volumn 63, Issue 1, 2014, Pages 29-36

  Ha, Chae Myeong ^a   Park, Sungmi ^a   Choi, Young Keun ^a   Jeong, Ji Yun ^b   Oh, Chang Joo ^a   Bae, Kwi Hyun ^b   Lee, Sun Joo ^a   Kim, Ji Hyun ^a   Park, Keun Gyu ^a,b   Jun, Do Youn ^a   Lee, In Kyu ^a,b  

^a Kyungpook National University   (South Korea)

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

Author keywords

Dimethyl fumarate; Hyperphosphatemia; NF E2 related factor 2; Osteoblast; Vascular calcification

Indexed keywords

CALCIUM; COLECALCIFEROL; FUMARIC ACID DIMETHYL ESTER; MESSENGER RNA; TRANSCRIPTION FACTOR NRF2; VITAMIN D RECEPTOR; FUMARIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; AORTA DISEASE; ARTICLE; BLOOD VESSEL CALCIFICATION; COMMON CAROTID ARTERY; CONTROLLED STUDY; DRUG EFFICACY; EX VIVO STUDY; GENE SILENCING; HUMAN; HUMAN CELL; HYPERPHOSPHATEMIA; IMMUNOMODULATION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OSTEOBLAST; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE FIBER; THORACIC AORTA; TRANSCRIPTION INITIATION; VASCULAR SMOOTH MUSCLE; ANIMAL; C57BL MOUSE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; UPREGULATION; VASCULAR CALCIFICATION;

ANIMALS; AORTA, THORACIC; CALCIUM; CAROTID ARTERY, COMMON; DIMETHYL FUMARATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FUMARATES; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; UP-REGULATION; VASCULAR CALCIFICATION;

EID: 84908010890     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2014.06.007     Document Type: Article

References (47)

1. Demer L.L., Tintut Y. Vascular calcification: pathobiology of a multifaceted disease. Circulation 2008, 117:2938-2948.
2. Reaven P.D., Sacks J. Coronary artery and abdominal aortic calcification are associated with cardiovascular disease in type 2 diabetes. Diabetologia 2005, 48:379-385.
3. Schwarz U., Buzello M., Ritz E., Stein G., Raabe G., Wiest G., et al. Morphology of coronary atherosclerotic lesions in patients with end-stage renal failure. Nephrol Dial Transplant 2000, 15:218-223.
4. Chen G., Deng C., Li Y.P. TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012, 8:272-288.
5. Johnson R.C., Leopold J.A., Loscalzo J. Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res 2006, 99:1044-1059.
6. Byon C.H., Javed A., Dai Q., Kappes J.C., Clemens T.L., Darley-Usmar V.M., et al. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by Akt signaling. J Biol Chem 2008, 283:15319-15327.
7. Harada H., Tagashira S., Fujiwara M., Ogawa S., Katsumata T., Yamaguchi A., et al. Cbfa1 isoforms exert functional differences in osteoblast differentiation. J Biol Chem 1999, 274:6972-6978.
8. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., et al. Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev Dyn 1999, 214:279-290.
9. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
10. Jono S., McKee M.D., Murry C.E., Shioi A., Nishizawa Y., Mori K., et al. Phosphate regulation of vascular smooth muscle cell calcification. Circ Res 2000, 87:e10-e17.
11. Giachelli C.M. The emerging role of phosphate in vascular calcification. Kidney Int 2009, 75:890-897.
12. Shanahan C.M., Crouthamel M.H., Kapustin A., Giachelli C.M. Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ Res 2011, 109:697-711.
13. Madamanchi N.R., Vendrov A., Runge M.S. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol 2005, 25:29-38.
14. Galle J. Oxidative stress in chronic renal failure. Nephrol Dial Transplant 2001, 16:2135-2137.
15. Hayden M.R., Tyagi S.C., Kolb L., Sowers J.R., Khanna R. Vascular ossification-calcification in metabolic syndrome, type 2 diabetes mellitus, chronic kidney disease, and calciphylaxis-calcific uremic arteriolopathy: the emerging role of sodium thiosulfate. Cardiovasc Diabetol 2005, 4:4.
16. Fadini G.P., Albiero M., Menegazzo L., Boscaro E., Vigili de Kreutzenberg S., Agostini C., et al. Widespread increase in myeloid calcifying cells contributes to ectopic vascular calcification in type 2 diabetes. Circ Res 2011, 108:1112-1121.
17. Chen N.X., Duan D., O'Neill K.D., Wolisi G.O., Koczman J.J., Laclair R., et al. The mechanisms of uremic serum-induced expression of bone matrix proteins in bovine vascular smooth muscle cells. Kidney Int 2006, 70:1046-1053.
18. Hinoi E., Fujimori S., Wang L., Hojo H., Uno K., Yoneda Y. Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activation. J Biol Chem 2006, 281:18015-18024.
19. Copple I.M. The Keap1-Nrf2 cell defense pathway - a promising therapeutic target?. Adv Pharmacol 2012, 63:43-79.
20. Kim H., Kim H.J., Lee K., Kim J.M., Kim H.S., Kim J.R., et al. Alpha-lipoic acid attenuates vascular calcification via reversal of mitochondrial function and restoration of Gas6/Axl/Akt survival pathway. J Cell Mol Med 2012, 16:273-286.
21. Linker R.A., Lee D.-H., Ryan S., van Dam A.M., Conrad R., Bista P., et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 2011, 134:678-692.
22. Oh C.J., Kim J.Y., Choi Y.K., Kim H.J., Jeong J.Y., Bae K.H., et al. Dimethylfumarate attenuates renal fibrosis via NF-E2-related factor 2-mediated inhibition of transforming growth factor-beta/Smad signaling. PLoS One 2012, 7:e45870.
23. Wiesner D., Merdian I., Lewerenz J., Ludolph A.C., Dupuis L., Witting A. Fumaric acid esters stimulate astrocytic VEGF expression through HIF-1alpha and Nrf2. PLoS One 2013, 8:e76670.
24. Takaya K., Suzuki T., Motohashi H., Onodera K., Satomi S., Kensler T.W., et al. Validation of the multiple sensor mechanism of the Keap1-Nrf2 system. Free Radic Biol Med 2012, 53:817-827.
25. Moharregh-Khiabani D., Linker R., Gold R., Stangel M. Fumaric acid and its esters: an emerging treatment for multiple sclerosis. Curr Neuropharmacol 2009, 7:60.
26. Gold R., Linker R.A., Stangel M. Fumaric acid and its esters: an emerging treatment for multiple sclerosis with antioxidative mechanism of action. Clin Immunol 2012, 142:44-48.
27. 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. Respir Res 2010, 11:145.
28. Meili-Butz S., Niermann T., Fasler-Kan E., Barbosa V., Butz N., John D., et al. Dimethyl fumarate, a small molecule drug for psoriasis, inhibits nuclear factor-kappaB and reduces myocardial infarct size in rats. Eur J Pharmacol 2008, 586:251-258.
29. Ashrafian H., Czibik G., Bellahcene M., Aksentijevic D., Smith A.C., Mitchell S.J., et al. Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway. Cell Metab 2012, 15:361-371.
30. Cross S.A., Cook D.R., Chi A.W., Vance P.J., Kolson L.L., Wong B.J., et al. Dimethyl fumarate, an immune modulator and inducer of the antioxidant response, suppresses HIV replication and macrophage-mediated neurotoxicity: a novel candidate for HIV neuroprotection. J Immunol 2011, 187:5015-5025.
31. Leik C.E., Willey A., Graham M.F., Walsh S.W. Isolation and culture of arterial smooth muscle cells from human placenta. Hypertension 2004, 43:837-840.
32. Kim H.-J., Yoo E.-K., Kim J.-Y., Choi Y.-K., Lee H.-J., Kim J.-K., et al. Protective role of clusterin/apolipoprotein J against neointimal hyperplasia via antiproliferative effect on vascular smooth muscle cells and cytoprotective effect on endothelial cells. Arterioscler Thromb Vasc Biol 2009, 29:1558-1564.
33. Price P.A., Chan W.S., Jolson D.M., Williamson M.K. The elastic lamellae of devitalized arteries calcify when incubated in serum: evidence for a serum calcification factor. Arterioscler Thromb Vasc Biol 2006, 26:1079-1085.
34. Neven E., D'Haese P.C. Vascular calcification in chronic renal failure: what have we learned from animal studies?. Circ Res 2011, 108:249-264.
35. Han M.S., Che X., Cho G.H., Park H.R., Lim K.E., Park N.R., et al. Functional cooperation between vitamin D receptor and Runx2 in vitamin D-induced vascular calcification. PLoS One 2013, 8:e83584.
36. Scannevin R.H., Chollate S., Jung M.Y., Shackett M., Patel H., Bista P., et al. Fumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathway. J Pharmacol Exp Ther 2012, 341:274-284.
37. Giachelli C.M. Vascular calcification mechanisms. J Am Soc Nephrol 2004, 15:2959-2964.
38. Hinoi E., Takarada T., Fujimori S., Wang L., Iemata M., Uno K., et al. Nuclear factor E2 p45-related factor 2 negatively regulates chondrogenesis. Bone 2007, 40:337-344.
39. Li X., Yang H.Y., Giachelli C.M. BMP-2 promotes phosphate uptake, phenotypic modulation, and calcification of human vascular smooth muscle cells. Atherosclerosis 2008, 199:271-277.
40. Steitz S.A., Speer M.Y., Curinga G., Yang H.Y., Haynes P., Aebersold R., et al. Smooth muscle cell phenotypic transition associated with calcification: upregulation of cbfa1 and downregulation of smooth muscle lineage markers. Circ Res 2001, 89:1147-1154.
41. Tanaka T., Sato H., Doi H., Yoshida C.A., Shimizu T., Matsui H., et al. Runx2 represses myocardin-mediated differentiation and facilitates osteogenic conversion of vascular smooth muscle cells. Mol Cell Biol 2008, 28:1147-1160.
42. Speer M.Y., Li X., Hiremath P.G., Giachelli C.M. Runx2/Cbfa1, but not loss of myocardin, is required for smooth muscle cell lineage reprogramming toward osteochondrogenesis. J Cell Biochem 2010, 110:935-947.
43. Mann G.E., Niehueser-Saran J., Watson A., Gao L., Ishii T., de Winter P., et al. Nrf2/ARE regulated antioxidant gene expression in endothelial and smooth muscle cells in oxidative stress: implications for atherosclerosis and preeclampsia. Sheng Li Xue Bao 2007, 59:117-127.
44. Levonen A.L., Inkala M., Heikura T., Jauhiainen S., Jyrkkanen H.K., Kansanen E., et al. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol 2007, 27:741-747.
45. Dreger H., Westphal K., Wilck N., Baumann G., Stangl V., Stangl K., et al. Protection of vascular cells from oxidative stress by proteasome inhibition depends on Nrf2. Cardiovasc Res 2010, 85:395-403.
46. Fox R.J., Miller D.H., Phillips J.T., Hutchinson M., Havrdova E., Kita M., et al. Placebo-controlled phase 3 study of oral BG-12 or glatiramer in multiple sclerosis. N Engl J Med 2012, 367:1087-1097.
47. Gold R., Kappos L., Arnold D.L., Bar-Or A., Giovannoni G., Selmaj K., et al. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N Engl J Med 2012, 367:1098-1107.