NF-E2-related factor 2 promotes atherosclerosis by effects on plasma lipoproteins and cholesterol transport that overshadow antioxidant protection

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 1, 2011, Pages 58-66

  Barajas, Berenice ^a   Che, Nam ^a   Yin, Fen ^a   Rowshanrad, Amir ^a   Orozco, Luz D ^a   Gong, Ke Wei ^a   Wang, Xuping ^a   Castellani, Lawrence W ^a   Reue, Karen ^a   Lusis, Aldons J ^a   Araujo, Jesus A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

atherosclerosis; cytokines; foam cell formation; lipogenesis; lipoproteins; Nrf2; reactive oxygen species

Indexed keywords

ANTIOXIDANT; APOENZYME; APOLIPOPROTEIN; CD36 ANTIGEN; CHOLESTEROL; LIPOPROTEIN; SCAVENGER RECEPTOR; TRANSCRIPTION FACTOR NRF2;

AORTA ATHEROSCLEROSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CHOLESTEROL LIVER LEVEL; CHOLESTEROL TRANSPORT; HEMATOPOIESIS; KNOCKOUT MOUSE; LIPOGENESIS; MACROPHAGE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD36; ANTIOXIDANTS; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BIOLOGICAL TRANSPORT; CHOLESTEROL; DISEASE MODELS, ANIMAL; FEMALE; FOAM CELLS; GENE EXPRESSION REGULATION; LIPOGENESIS; LIPOPROTEINS; LIVER; MALE; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES; SEX FACTORS;

EID: 78650913866     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.210906     Document Type: Article

References (37)

1. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
2. Araujo JA, Barajas B, Kleinman M, Wang X, Bennett BJ, Gong KW, Navab M, Harkema J, Sioutas C, Lusis AJ, Nel AE. Ambient particulate pollutants in the ultrafine range promote early atherosclerosis and systemic oxidative stress. Circ Res. 2008;102:589-596.
3. Berliner JA, Heinecke JW. The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med. 1996;20:707-727.
4. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148.
5. Segal AW, Abo A. The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci. 1993;18:43-47.
6. Matsubara T, Ziff M. Superoxide anion release by human endothelial cells: synergism between a phorbol ester and a calcium ionophore. J Cell Physiol. 1986;127:207-210. (Pubitemid 16074724)
7. Levonen AL, Vahakangas E, Koponen JK, Yla-Herttuala S. Antioxidant gene therapy for cardiovascular disease: current status and future perspectives. Circulation. 2008;117:2142-2150.
8. Stocker R, Keaney JF Jr. Role of oxidative modifications in atherosclerosis. Physiol Rev. 2004;84:1381-1478.
9. Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene. 2002;294:1-12.
10. Kwak MK, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler TW. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway: identification of novel gene clusters for cell survival. J Biol Chem. 2003;278:8135-8145.
11. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest. 2004;114:1248-1259.
12. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med. 2004;10:549-557.
13. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 2002;62:5196-5203.
14. Numazawa S, Yoshida T. Nrf2-dependent gene expressions: a molecular toxicological aspect. J Toxicol Sci. 2004;29:81-89.
15. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T, Harada T, Yamamoto M. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci. 2001;59:169-177.
16. Chan K, Lu R, Chang JC, Kan YW. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA. 1996;93:13943-13948.
17. Chan K, Kan YW. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA. 1999;96:12731-12736.
18. Li J, Stein TD, Johnson JA. Genetic dissection of systemic autoimmune disease in Nrf2-deficient mice. Physiol Genomics. 2004;18:261-272.
19. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, Kensler TW, Biswal S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest. 2006; 116:984-995.
20. Gharavi NM, Gargalovic PS, Chang I, Araujo JA, Clark MJ, Szeto WL, Watson AD, Lusis AJ, Berliner JA. High-density lipoprotein modulates oxidized phospholipid signaling in human endothelial cells from proinflammatory to antiinflammatory. Arterioscler Thromb Vasc Biol. 2007;27:1346-1353.
21. Levonen AL, Inkala M, Heikura T, Jauhiainen S, Jyrkkanen HK, Kansanen E, Maatta K, Romppanen E, Turunen P, Rutanen J, Yla- Herttuala S. 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.
22. Jyrkkanen HK, Kansanen E, Inkala M, Kivela AM, Hurttila H, Heinonen SE, Goldsteins G, Jauhiainen S, Tiainen S, Makkonen H, Oskolkova O, Afonyushkin T, Koistinaho J, Yamamoto M, Bochkov VN, Yla-Herttuala S, Levonen AL. Nrf2 regulates antioxidant gene expression evoked by oxidized phospholipids in endothelial cells and murine arteries in vivo. Circ Res. 2008;103:e1-e9.
23. Yet SF, Layne MD, Liu X, Chen YH, Ith B, Sibinga NE, Perrella MA. Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 2003;17:1759-1761.
24. Lewis P, Stefanovic N, Pete J, Calkin AC, Giunti S, Thallas-Bonke V, Jandeleit-Dahm KA, Allen TJ, Kola I, Cooper ME, de Haan JB. Lack of the antioxidant enzyme glutathione peroxidase-1 accelerates atherosclerosis in diabetic apolipoprotein E-deficient mice. Circulation. 2007;115:2178-2187.
25. Araujo JA, Meng L, Tward AD, Hancock WW, Zhai Y, Lee A, Ishikawa K, Iyer S, Buelow R, Busuttil RW, Shih DM, Lusis AJ, Kupiec-Weglinski JW. Systemic rather than local heme oxygenase-1 overexpression improves cardiac allograft outcomes in a new transgenic mouse. J Immunol. 2003;171:1572-1580.
26. Tsuchihashi S, Livhits M, Zhai Y, Busuttil RW, Araujo JA, Kupiec-Weglinski JW. Basal rather than induced heme oxygenase-1 levels are crucial in the antioxidant cytoprotection. J Immunol. 2006;177:4749-4757.
27. Sussan TE, Jun J, Thimmulappa R, Bedja D, Antero M, Gabrielson KL, Polotsky VY, Biswal S. Disruption of Nrf2, a key inducer of antioxidant defenses, attenuates ApoE-mediated atherosclerosis in mice. PLoS ONE. 2008;3:e3791.
28. Orozco LD, Kapturczak MH, Barajas B, Wang X, Weinstein MM, Wong J, Deshane J, Bolisetty S, Shaposhnik Z, Shih DM, Agarwal A, Lusis AJ, Araujo JA. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res. 2007;100:1703-1711.
29. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994; 269:21003-21009.
30. Zhong H, Beaulaurier J, Lum PY, Molony C, Yang X, Macneil DJ, Weingarth DT, Zhang B, Greenawalt D, Dobrin R, Hao K, Woo S, Fabre-Suver C, Qian S, Tota MR, Keller MP, Kendziorski CM, Yandell BS, Castro V, Attie AD, Kaplan LM, Schadt EE. Liver and adipose expression associated SNPs are enriched for association to type 2 diabetes. PLoS Genet 2010;6:e1000932.
31. Reue K, Dwyer JR. Lipin proteins and metabolic homeostasis. J Lipid Res. 2009;50:S109-S114.
32. Liu L, Zhang Y, Chen N, Shi X, Tsang B, Yu YH. Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance. J Clin Invest. 2007; 117:1679-1689.
33. Koliwad SK, Streeper RS, Monetti M, Cornelissen I, Chan L, Terayama K, Naylor S, Rao M, Hubbard B, Farese RV Jr. DGAT1-dependent triacylglycerol storage by macrophages protects mice from diet-induced insulin resistance and inflammation. J Clin Invest. 2010;120:756-767.
34. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-322.
35. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, Randolph GJ. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci USA. 2004;101:11779-11784.
36. Ishii T, Itoh K, Ruiz E, Leake DS, Unoki H, Yamamoto M, Mann GE. 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. 2004;94:609-616.
37. Heider H, Wintergerst ES. Mimicking phosphorylation at Ser-48 strongly reduces surface expression of human macrophage scavenger receptor class A: implications on cell motility. FEBS Lett. 2001;505:185-190.