Excess Nitric Oxide Impairs LXR(α)-ABCA1-Dependent Cholesterol Efflux in Macrophage Foam Cells

Journal of Cellular Physiology

Volumn 229, Issue 1, 2014, Pages 117-125

  Zhao, Jin Feng ^a   Shyue, Song Kun ^b   Lin, Shing Jong ^c   Wei, Jeng ^d   Lee, Tzong Shyuan ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d CHENG HSIN GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; APOLIPOPROTEIN E; CD36 ANTIGEN; CHOLESTEROL; INDUCIBLE NITRIC OXIDE SYNTHASE; LIVER X RECEPTOR ALPHA; LOW DENSITY LIPOPROTEIN; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PEROXYNITRITE; SCAVENGER RECEPTOR A; SCAVENGER RECEPTOR BI; TRIACYLGLYCEROL; ABCA1 PROTEIN, MOUSE; LIVER X RECEPTOR; NOS2 PROTEIN, MOUSE; ORPHAN NUCLEAR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; ATHEROSCLEROSIS; BINDING ASSAY; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; FOAM CELL; GENE DELETION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; LIVER; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; CHEMICALLY INDUCED; DRUG EFFECTS; TOXICITY;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; FOAM CELLS; GENE EXPRESSION REGULATION; LIPID METABOLISM; LIPOPROTEINS, LDL; LIVER; MACROPHAGES; MICE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; ORPHAN NUCLEAR RECEPTORS; OXIDATION-REDUCTION; S-NITROSO-N-ACETYLPENICILLAMINE;

EID: 84888010785     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24429     Document Type: Article

References (41)

1. Alonso D, Radomski MW. 2003. Nitric oxide, platelet function, myocardial infarction and reperfusion therapies. Heart Fail Rev 8:47-54.
2. Arakawa R, Yokoyama S. 2002. Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiolprotease-mediated degradation. J Biol Chem 277:22426-22429.
3. Asztalos BF, de la Llera-Moya M, Dallal GE, Horvath KV, Schaefer EJ, Rothblat GH. 2005. Differential effects of HDL subpopulations on cellular ABCA1- and SR-BI-mediated cholesterol efflux. J Lipid Res 46:2246-2253.
4. Baranova I, Vishnyakova T, Bocharov A, Chen Z, Remaley AT, Stonik J, Eggerman TL, Patterson AP. 2002. Lipopolysaccharide down regulates both scavenger receptor B1 and ATP binding cassette transporter A1 in RAW cells. Infect Immun 70:2995-3003.
5. Beckman JS, Koppenol WH. 1996. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am J Physiol 271:C1424-C1437.
6. Chang GJ, Woo P, Honda HM, Ignarro LJ, Young L, Berliner JA, Demer LL. 1994. Oxidation of LDL to a biologically active form by derivatives of nitric oxide and nitrite in the absence of superoxide. Dependence on pH and oxygen. Arterioscler Thromb 14:1808-1814.
7. Cauwels A. 2007. Nitric oxide in shock. Kidney Int 72:557-565.
8. Cheng LC, Su KH, Kou YR, Shyue SK, Ching LC, Yu YB, Wu YL, Pan CC, Lee TS. 2011. α-Lipoic acid ameliorates foam cell formation via liver X receptor α-dependent upregulation of ATP-binding cassette transporters A1 and G1. Free Radic Biol Med 50:47-54.
9. Daniel T, Alexander M, Hubbard WJ, Chaudry IH, Choudhry MA, Schwacha MG. 2006. Nitric oxide contributes to the development of a post-injury Th2 T-cell phenotype and immune dysfunction. J Cell Physiol 208:418-427.
10. Detmers PA, Hernandez M, Mudgett J, Hassing H, Burton C, Mundt S, Chun S, Fletcher D, Card DJ, Lisnock J, Weikel R, Bergstrom JD, Shevell DE, Hermanowski-Vosatka A, Sparrow CP, Chao YS, Rader DJ, Wright SD, Pure E. 2000. Deficiency in inducible nitric oxide synthase results in reduced atherosclerosis in apolipoprotein E-deficient mice. J Immunol 165:3430-3435.
11. Feng B, Tabas I. 2002. ABCA1-mediated cholesterol efflux is defective in free cholesterol-loaded macrophages: Mechanism involves enhanced ABCA1 degradation in a process requiring full NPC1 activity. J Biol Chem 277:43271-43280.
12. Glass CK, Witztum JL. 2001. Atherosclerosis. the road ahead. Cell 104:503-516.
13. Graham A, Hogg N, Kalyanaraman B, O'Leary V, Darley-Usmar V, Moncada S. 1993. Peroxynitrite modification of low-density lipoprotein leads to recognition by the macrophage scavenger receptor. FEBS Lett 330:181-185.
14. Han KH, Chang MK, Boullier A, Green SR, Li A, Glass CK, Quehenberger O. 2000. Oxidized LDL reduces monocyte CCR2 expression through pathways involving peroxisome proliferator-activated receptor gamma. J Clin Invest 106:793-802.
15. Henry Y, Lepoivre M, Drapier JC, Ducrocq C, Boucher JL, Guissani A. 1993. EPR characterization of molecular targets for NO in mammalian cells and organelles. FASEB J 7:1124-1134.
16. Hoeflich KP, Ikura M. 2002. Calmodulin in action: Diversity in target recognition and activation mechanisms. Cell 108:739-742.
17. Kim M, Han IS, Koh SD, Perrino BA. 2006. Roles of CaM kinase II and phospholamban in SNP-induced relaxation of murine gastric fundus smooth muscles. Am J Physiol Cell Physiol 291:C337-C347.
18. Kim M, Perrino BA. 2007. CaM kinase II activation and phospholamban phosphorylation by SNP in murine gastric antrum smooth muscles. Am J Physiol Gastrointest Liver Physiol 292:1045-1054.
19. Kubes P, Suzuki M, Granger DN. 1991. Nitric oxide: An endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88:4651-4655.
20. Kuhlencordt PJ, Chen J, Han F, Astern J, Huang PL. 2001. Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E-knockout mice. Circulation 103:3099-3104.
21. Laffitte BA, Joseph SB, Walczak R, Pei L, Wilpitz DC, Collins JL, Tontonoz P. 2001. Autoregulation of the human liver X receptor alpha promoter. Mol Cell Biol 21:7558-7568.
22. Leeuwenburgh C, Hardy MM, Hazen SL, Wagner P, Oh-ishi S, Steinbrecher UP, Heinecke JW. 1997. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J Biol Chem 272:1433-1436.
23. Lelamali K, Wang W, Gengaro P, Edelstein C, Schrier RW. 2001. Effects of nitric oxide and peroxynitrite on endotoxin-induced leukocyte adhesion to endothelium. J Cell Physiol 188:337-342.
24. Li AC, Glass CK. 2002. The macrophage foam cell as a target for therapeutic intervention. Nat Med 8:1235-1242.
25. Lin CY, Lee TS, Chen CC, Chang CA, Lin YJ, Hsu YP, Ho LT. 2011. Endothelin-1 exacerbates lipid accumulation by increasing the protein degradation of the ATP-binding cassette transporter G1 in macrophages. J Cell Physiol 226:2198-2205.
26. Liu VW, Huang PL. 2008. Cardiovascular roles of nitric oxide: A review of insights from nitric oxide synthase gene disrupted mice. Cardiovasc Res 77:19-29.
27. Lu KY, Ching LC, Su KH, Yu YB, Kou YR, Hsiao SH, Huang YC, Chen CY, Cheng LC, Pan CC, Lee TS. 2010. Erythropoietin suppresses the formation of macrophage foam cells: Role of liver X receptor α. Circulation 121:1828-1837.
28. Lusis AJ. 2000. Atherosclerosis. Nature 407:233-241.
29. Marcil V, Delvin E, Sané AT, Tremblay A, Levy E. 2006. Oxidative stress influences cholesterol efflux in THP-1 macrophages: Role of ATP-binding cassette A1 and nuclear factors. Cardiovasc Res 72:473-482.
30. Naseem KM. 2005. The role of nitric oxide in cardiovascular diseases. Mol Aspects Med 26:33-65.
31. Nathan C, Xie QW. 1994. Nitric oxide synthases: Roles, tolls, and controls. Cell 78:915-918.
32. Nussler AK, Billiar TR. 1993. Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 54:171-178.
33. Oram JF, Wolfbauer G, Vaughan AM, Tang C, Albers JJ. 2003. Phospholipid transfer protein interacts with and stabilizes ATP-binding cassette transporter A1 and enhances cholesterol efflux from cells. J Biol Chem 278:52379-52385.
34. 2+ signaling pathways in endothelial cells. J Cell Physiol 220:706-715.
35. Satoh S, Kimura T, Toda M, Miyazaki H, Ono S, Narita H, Murayama T, Nomura Y. 1996. NO donors stimulate noradrenaline release from rat hippocampus in a calmodulin-dependent manner in the presence of l-cysteine. J Cell Physiol 169:87-96.
36. 2+ signaling in cardiac myocytes. J Mol Cell Cardiol 52:312-316.
37. Sekine N, Ishikawa T, Okazaki T, Hayashi M, Wollheim CB, Fujita T. 2000. Synergistic activation of NF-kappab and inducible isoform of nitric oxide synthase induction by interferon-gamma and tumor necrosis factor-alpha in INS-1 cells. J Cell Physiol 184:46-57.
38. Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel D, Valeri CR, Loscalzo J. 1992. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89:7674-7677.
39. Wang Y, Chen Z, Liao Y, Mei C, Peng H, Wang M, Guo H, Lu H. 2007. Angiotensin II increases the cholesterol content of foam cells via down-regulating the expression of ATP-binding cassette transporter A1. Biochem Biophys Res Commun 353:650-654.
40. Wang Y, Oram JF. 2002. Unsaturated fatty acids inhibit cholesterol efflux from macrophages by increasing degradation of ATP-binding cassette transporter A1. J Biol Chem 277:5692-5697.
41. Zhao JF, Ching LC, Huang YC, Chen CY, Chiang AN, Kou YR, Shyue SK, Lee TS. 2012. Molecular mechanism of curcumin on the suppression of cholesterol accumulation in macrophage foam cells and atherosclerosis. Mol Nutr Food Res 56:691-701.