Nrf2 in bone marrow-derived cells positively contributes to the advanced stage of atherosclerotic plaque formation

Free Radical Biology and Medicine

Volumn 53, Issue 12, 2012, Pages 2256-2262

  Harada, Nobuhiko ^a   Ito, Koichi ^b   Hosoya, Tomonori ^a   Mimura, Junsei ^a   Maruyama, Atsushi ^a   Noguchi, Noriko ^c   Yagami, Ken Ichi ^d   Morito, Naoki ^d   Takahashi, Satoru ^d   Maher, Jon M ^e   Yamamoto, Masayuki ^e   Itoh, Ken ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

^c DOSHISHA UNIVERSITY   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

ApoE knockout mice; Atherosclerosis; Cholesterol; Macrophage polarization; Nrf2

Indexed keywords

ARGINASE; ARGINASE 1; ARGINASE II; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; HEART INFARCTION; HO 1 GENE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MALE; MAMMAL; MOUSE; NONHUMAN; NRF2 GENE; OXIDATIVE STRESS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SLPI GENE;

A0N0; A0N2; APOE; APOE KNOCKOUT MICE; APOE KO AND NRF2 KO; APOE KO AND NRF2 WT; APOLIPOPROTEIN E; ARGI; ARGII; ARGINASE I; ARGINASE II; ATHEROSCLEROSIS; BM; BMT; BONE MARROW; BONE MARROW TRANSPLANTATION; CHO; CHOLESTEROL; CHYLOMICRON; CM; GCLM; GLUTAMATE-CYSTEINE LIGASE, MODIFIER SUBUNIT; HDL; HEME OXYGENASE-1; HFC DIET; HIGH FAT AND HIGH CHOLESTEROL DIET; HIGH-DENSITY LIPOPROTEIN; HO-1; ICAM-1; IL-6; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; INTERCELLULAR CELL ADHESION MOLECULE 1; INTERLEUKIN-6; KNOCKOUT; KO; LDL; LOW DENSITY LIPOPROTEIN; MACROPHAGE POLARIZATION; NAD(P)H DEHYDROGENASE, QUINONE 1; NF-E2-RELATED FACTOR 2; NQO1; NRF2; OXIDIZED LDL; OXLDL; SECRETORY LEUKOCYTE PROTEASE INHIBITOR; SLPI; SRXN1; SULFIREDOXIN 1 HOMOLOG; TG; TNF-Α; TRIGLYCERIDE; TUMOR NECROSIS FACTOR Α TXNRD1, THIOREDOXIN REDUCTASE 1; VASCULAR CELL ADHESION MOLECULE 1; VCAM-1; VERY LOW DENSITY LIPOPROTEIN; VLDL; WILD TYPE; WT;

ANIMALS; AORTA; ATHEROSCLEROSIS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; FEMALE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; PLAQUE, ATHEROSCLEROTIC; TRANSCRIPTIONAL ACTIVATION;

MAMMALIA; MUS;

EID: 84870219810     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.10.001     Document Type: Article

References (29)

1. C.K. Glass, and J.L. Witztum Atherosclerosis. The road ahead Cell 104 2001 503 516
2. A.J. Lusis Atherosclerosis Nature 407 2000 233 241
3. R. Kleemann, S. Zadelaar, and T. Kooistra Cytokines and atherosclerosis: a comprehensive review of studies in mice Cardiovasc. Res. 79 2008 360 376
4. A. Mantovani, C. Garlanda, and M. Locati Macrophage diversity and polarization in atherosclerosis: a question of balance Arterioscler. Thromb. Vasc. Biol. 29 2009 1419 1423
5. S. Pan Molecular mechanisms responsible for the atheroprotective effects of laminar shear stress Antioxid. Redox Signal 11 2009 1669 1682
6. Berk, B.C.; Abe, J.-I.; Min, W.; Surapisitchat, J.; Yan, C. Endothelial atheroprotective and anti-inflammatory mechanisms. Ann. N. Y. Acad. Sci. 947:93-109; discussion 109-111; 2001.
7. E. Warabi, W. Takabe, T. Minami, K. Inoue, K. Itoh, M. Yamamoto, T. Ishii, T. Kodama, and N. Noguchi Shear stress stabilizes NF-E2-related factor 2 and induces antioxidant genes in endothelial cells: role of reactive oxygen/nitrogen species Free Radic. Biol. Med. 42 2007 260 269 (Pubitemid 44959746)
8. T. Hosoya, A. Maruyama, M.-I. Kang, Y. Kawatani, T. Shibata, K. Uchida, E. Warabi, N. Noguchi, K. Itoh, and M. Yamamoto Differential responses of the Nrf2-Keap1 system to laminar and oscillatory shear stresses in endothelial cells J. Biol. Chem. 280 2005 27244 27250 (Pubitemid 41040764)
9. X.-L. Chen, G. Dodd, S. Thomas, X. Zhang, M.A. Wasserman, B.H. Rovin, and C. Kunsch Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression Am. J. Physiol. Heart Circ. Physiol 290 2006 H1862 H1870
10. M. Zakkar, K. Van der Heiden, L.A. Luong, H. Chaudhury, S. Cuhlmann, S.S. Hamdulay, R. Krams, I. Edirisinghe, I. Rahman, H. Carlsen, D.O. Haskard, J.C. Mason, and P.C. Evans Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state Arterioscler. Thromb. Vasc. Biol. 29 2009 1851 1857
11. J.L. Johnson, and A.C. Newby Macrophage heterogeneity in atherosclerotic plaques Curr. Opin. Lipidol. 20 2009 370 378
12. A. Kadl, A.K. Meher, P.R. Sharma, M.Y. Lee, A.C. Doran, S.R. Johnstone, M.R. Elliott, F. Gruber, J. Han, W. Chen, T. Kensler, K.S. Ravichandran, B.E. Isakson, B.R. Wamhoff, and N. Leitinger Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2 Circ. Res. 107 2010 737 746
13. T. Ishii, K. Itoh, E. Ruiz, D.S. Leake, H. Unoki, M. Yamamoto, and G.E. Mann Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal Circ. Res. 94 2004 609 616 (Pubitemid 38387743)
14. T.E. Sussan, J. Jun, R. Thimmulappa, D. Bedja, M. Antero, K.L. Gabrielson, V.Y. Polotsky, and S. Biswal Disruption of Nrf2, a key inducer of antioxidant defenses, attenuates ApoE-mediated atherosclerosis in mice PLoS ONE 3 2008 e3791 2008
15. S. Freigang, F. Ampenberger, G. Spohn, S. Heer, A.T. Shamshiev, J. Kisielow, M. Hersberger, M. Yamamoto, M.F. Bachmann, and M. Kopf Nrf2 is essential for cholesterol crystal-induced inflammasome activation and exacerbation of atherosclerosis Eur. J. Immunol. 41 2011 2040 2051
16. B. Barajas, N. Che, F. Yin, A. Rowshanrad, L.D. Orozco, K.W. Gong, X. Wang, L.W. Castellani, K. Reue, A.J. Lusis, and J.A. Araujo NF-E2-related factor 2 promotes atherosclerosis by effects on plasma lipoproteins and cholesterol transport that overshadow antioxidant protection Arterioscler. Thromb. Vasc. Biol. 31 2011 58 66
17. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
18. J. Khallou-Laschet, A. Varthaman, G. Fornasa, C. Compain, A.-T. Gaston, M. Clement, M. Dussiot, O. Levillain, S. Graff-Dubois, A. Nicoletti, and G. Caligiuri Macrophage plasticity in experimental atherosclerosis PLoS ONE 5 2010 e8852
19. Y. Nakashima, A.S. Plump, E.W. Raines, J.L. Breslow, and R. Ross ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree Arterioscler. Thromb. 14 1994 133 140
20. Y. Ishii, K. Itoh, Y. Morishima, T. Kimura, T. Kiwamoto, T. Iizuka, A.E. Hegab, T. Hosoya, A. Nomura, T. Sakamoto, M. Yamamoto, and K. Sekizawa Transcription factor Nrf2 plays a pivotal role in protection against elastase-induced pulmonary inflammationand emphysema J. Immunol. 175 2005 6968 6975 (Pubitemid 41598943)
21. T. Ishii, K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, Y. Katoh, S. Bannai, and M. Yamamoto Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages J. Biol. Chem. 275 2000 16023 16029 (Pubitemid 30366908)
22. Schäfer, M.; Farwanah, H.; Willrodt, A.H.; Huebner, A.J.; Sandhoff, K.; Roop, D.; Hohl, D.; Bloch, W.; Werner, S. Nrf2 links epidermal barrier function with antioxidant defense. EMBO Mol. Med. In press; 2012.
23. T. Iizuka, Y. Ishii, K. Itoh, T. Kiwamoto, T. Kimura, Y. Matsuno, Y. Morishima, A.E. Hegab, S. Homma, A. Nomura, T. Sakamoto, M. Shimura, A. Yoshida, M. Yamamoto, and K. Sekizawa Nrf2-deficient mice are highly susceptible to cigarette smoke-induced emphysema Genes Cells 10 2005 1113 1125 (Pubitemid 41830071)
24. L. Nagy, P. Tontonoz, J.G. Alvarez, H. Chen, and M. Evans Oxidized LDL regulates macrophage gene expression through ligand activation of PPARγ Cell 93 1998 229 240 (Pubitemid 28180856)
25. T. Miyoshi, Y. Li, D.M. Shih, X. Wang, V.E. Laubach, A.H. Matsumoto, G.A. Helm, A.J. Lusis, and W. Shi Deficiency of inducible NO synthase reduces advanced but not early atherosclerosis in apolipoprotein E-deficient mice Life Sci. 79 2006 525 531
26. P. Duewell, H. Kono, K.J. Rayner, C.M. Sirois, G. Vladimer, F.G. Bauernfeind, G.S. Abela, L. Franchi, G. Nuñez, M. Schnurr, T. Espevik, E. Lien, K.A. Fitzgerald, K.L. Rock, K.J. Moore, S.D. Wright, V. Hornung, and E. Latz NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals Nature 464 2010 1357 1361
27. R. Zhou, A.S. Yazdi, P. Menu, and J. Tschopp A role for mitochondria in NLRP3 inflammasome activation Nature 469 2011 221 225
28. K. Kato, K. Takahashi, S. Monzen, H. Yamamoto, A. Maruyama, K. Itoh, and I. Kashiwakura Relationship between radiosensitivity and Nrf2 target gene expression in human hematopoietic stem cells Radiat. Res. 174 2010 177 184
29. J.T. McDonald, K. Kim, A.J. Norris, E. Vlashi, T.M. Phillips, C. Lagadec, L. Della Donna, J. Ratikan, H. Szelag, L. Hlatky, and W.H. McBride Ionizing radiation activates the Nrf2 antioxidant response Cancer Res. 70 2010 8886 8895