25-hydroxycholesterol-3-sulfate attenuates inflammatory response via PPARγ signaling in human THP-1 macrophages

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 7, 2012, Pages

  Xu, Leyuan ^a,b   Shen, Shanwei ^a,b   Ma, Yongjie ^a,b   Kim, Jin Koung ^a,b   Rodriguez Agudo, Daniel ^a,b   Heuman, Douglas M ^a,b   Hylemon, Phillip B ^a,b   Pandak, William M ^a,b   Ren, Shunlin ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cholesterol metabolites; Inflammatory response; Macrophages; Nuclear factor KB signaling pathway; Oxysterol sulfation; Oxysterols; Peroxisome proliferator activated receptor

Indexed keywords

25 HYDROXYCHOLESTEROL; 25 HYDROXYCHOLESTEROL 3 SULFATE; CYCLOOXYGENASE 2; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; LUCIFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INFLAMMATION; LIPID METABOLISM; MACROPHAGE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANTI-INFLAMMATORY AGENTS; BLOTTING, WESTERN; CELL NUCLEUS; CHOLESTEROL ESTERS; CYTOKINES; CYTOSOL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; HYDROXYCHOLESTEROLS; HYPOGLYCEMIC AGENTS; I-KAPPA B PROTEINS; LIPOPOLYSACCHARIDES; MACROPHAGES; NF-KAPPA B; PPAR GAMMA; PROTEIN TRANSPORT; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES;

EID: 84859463296     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00337.2011     Document Type: Article

References (59)

1. Ahmed W, Ziouzenkova O, Brown J, Devchand P, Francis S, Kadakia M, Kanda T, Orasanu G, Sharlach M, Zandbergen F, Plutzky J. PPARs and their metabolic modulation: new mechanisms for transcrip-tional regulation? J Intern Med 262: 184-198, 2007.
2. An J, Nakajima T, Kuba K, Kimura A. Losartan inhibits LPS-induced inflammatory signaling through a PPARgamma-dependent mechanism in human THP-1 macrophages. Hypertens Res 33: 831-835, 2010.
3. Bai Q, Xu L, Kakiyama G, Runge-Morris MA, Hylemon PB, Yin L, Pandak WM, Ren S. Sulfation of 25-hydroxycholesterol by SULT2B1b decreases cellular lipids via the LXR/SREBP-1c signaling pathway in human aortic endothelial cells. Atherosclerosis 214: 350-356, 2011.
4. Bensinger SJ, Tontonoz P. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454: 470-477, 2008.
5. Boitier E, Gautier JC, Roberts R. Advances in understanding the regulation of apoptosis and mitosis by peroxisome-proliferator activated receptors in pre-clinical models: relevance for human health and disease. Comp Hepatol 2: 3, 2003.
6. Bouhlel MA, Derudas B, Rigamonti E, Dievart R, Brozek J, Haulon S, Zawadzki C, Jude B, Torpier G, Marx N, Staels B, Chinetti-Gbaguidi G. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 6: 137-143, 2007.
7. Buroker NE, Barboza J, Huang JY. The IkappaBalpha gene is a peroxisome proliferator-activated receptor cardiac target gene. FEBS J 276: 3247-3255, 2009.
8. Calkin AC, Jandeleit-Dahm KA, Sebekova E, Allen TJ, Mizrahi J, Cooper ME, Tikellis C. PPARs and diabetes-associated atherosclerosis. Curr Pharm Des 13: 2736-2741, 2007.
9. Calleros L, Lasa M, Toro MJ, Chiloeches A. Low cell cholesterol levels increase NFkappaB activity through a p38 MAPK-dependent mechanism. Cell Signal 18: 2292-2301, 2006.
10. Castrillo A, Tontonoz P. Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation. Annu Rev Cell Dev Biol 20: 455-480, 2004.
11. Castrillo A, Tontonoz P. PPARs in atherosclerosis: the clot thickens. J Clin Invest 114: 1538-1540, 2004.
12. Castro-Caldas M, Mendes AF, Carvalho AP, Duarte CB, Lopes MC. Dexamethasone prevents interleukin-1beta-induced nuclear factor-kappaB activation by upregulating IkappaB-alpha synthesis, in lymphoblastic cells. Mediators Inflamm 12: 37-46, 2003.
13. Catley MC, Sukkar MB, Chung KF, Jaffee B, Liao SM, Coyle AJ, Haddad E, Barnes PJ, Newton R. Validation of the anti-inflammatory properties of small-molecule IkappaB Kinase (IKK)-2 inhibitors by comparison with adenoviral-mediated delivery of dominant-negative IKK1 and IKK2 in human airways smooth muscle. Mol Pharmacol 70: 697-705, 2006.
14. Chandra V, Huang P, Hamuro Y, Raghuram S, Wang Y, Burris TP, Rastinejad F. Structure of the intact PPAR-gamma-RXR-nuclear receptor complex on DNA. Nature 456: 350-356, 2008.
15. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, Evans RM. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med 7: 48-52, 2001.
16. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, Tontonoz P. APPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell 7: 161-171, 2001.
17. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ. Nuclear receptors and lipid physiology: opening the X-files. Science 294: 1866-1870, 2001.
18. Chen W, Chen G, Head DL, Mangelsdorf DJ, Russell DW. Enzymatic reduction of oxysterols impairs LXR signaling in cultured cells and the livers of mice. Cell Metab 5: 73-79, 2007.
19. Cheng YC, Prusoff WH. A new rapid assay for measuring deoxycytidy-late- and deoxythymidylate-kinase activities. Anal Biochem 60: 545-550, 1974.
20. Chira EC, McMillen TS, Wang S, Haw A, III, O'Brien KD, Wight TN, Chait A. Tesaglitazar, a dual peroxisome proliferator-activated receptor alpha/gamma agonist, reduces atherosclerosis in female low density lipoprotein receptor deficient mice. Atherosclerosis 195: 100-109, 2007.
21. Culman J, Zhao Y, Gohlke P, Herdegen T. PPAR-gamma: therapeutic target for ischemic stroke. Trends Pharmacol Sci 28: 244-249, 2007.
22. Delvecchio CJ, Bilan P, Radford K, Stephen J, Trigatti BL, Cox G, Parameswaran K, Capone JP. Liver X receptor stimulates cholesterol efflux and inhibits expression of proinflammatory mediators in human airway smooth muscle cells. Mol Endocrinol 21: 1324-1334, 2007.
23. Dushkin MI, Khoshchenko OM, Posokhova EN, Schvarts YS. Agonists of PPAR-alpha, PPAR-gamma, and RXR inhibit the formation of foam cells from macrophages in mice with inflammation. Bull Exp Biol Med 144: 713-716, 2007.
24. Erlinger TP, Miller ER 3rd, Charleston J, Appel LJ. Inflammation modifies the effects of a reduced-fat low-cholesterol diet on lipids: results from the DASH-sodium trial. Circulation 108: 150-154, 2003.
25. Ferreiro DU, Komives EA. Molecular mechanisms of system control of NF-kappaB signaling by IkappaBalpha. Biochemistry 49: 1560-1567, 2010.
26. Geeraert B, De Keyzer D, Davey PC, Crombe F, Benhabiles N, Holvoet P. Oxidized low-density lipoprotein-induced expression of ABCA1 in blood monocytes precedes coronary atherosclerosis and is associated with plaque complexity in hypercholesterolemic pigs. J Thromb Haemost 5: 2529-2536, 2007.
27. Gill S, Chow R, Brown AJ. Sterol regulators of cholesterol homeostasis and beyond: the oxysterol hypothesis revisited and revised. Prog Lipid Res 47: 391-404, 2008.
28. Glass CK, Ogawa S. Combinatorial roles of nuclear receptors in inflammation and immunity. Nat Rev Immunol 6: 44-55, 2006.
29. Heliovaara MK, Teppo AM, Karonen SL, Ebeling P. Inflammation affects lipid metabolism during recovery from hyperinsulinaemia. Eur J Clin Invest 36: 860-865, 2006.
30. Hideshima T, Chauhan D, Richardson P, Mitsiades C, Mitsiades N, Hayashi T, Munshi N, Dang L, Castro A, Palombella V, Adams J, Anderson KC. NF-kappa B as a therapeutic target in multiple myeloma. J Biol Chem 277: 16639-16647, 2002.
31. Hwang HJ, Lee HJ, Kim CJ, Shim I, Hahm DH. Inhibitory Effect of Amygdalin on Lipopolysaccharide-inducible TNF-alpha and IL-1beta mRNA Expression and Carrageenan-induced Rat Arthritis. J Microbiol Biotechnol 18: 1641-1647, 2008.
32. Jin JQ, Li CQ, He LC. Down-regulatory effect of usnic acid on nuclear factor-kappaB-dependent tumor necrosis factor-alpha and inducible nitric oxide synthase expression in lipopolysaccharide-stimulated macrophages RAW 264.7. Phytother Res 2008.
33. Joffre C, Leclere L, Buteau B, Martine L, Cabaret S, Malvitte L, Acar N, Lizard G, Bron A, Creuzot-Garcher C, Bretillon L. Oxysterols induced inflammation and oxidation in primary porcine retinal pigment epithelial cells. Curr Eye Res 32: 271-280, 2007.
34. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, Grunfeld C. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. J Lipid Res 45: 1169-1196, 2004.
35. Lee PC, Sever N, Bose-Boyd RA. Isolation of sterol-resistant Chinese hamster ovary cells with genetic deficiencies in both Insig-1 and Insig-2. J Biol Chem 280: 25242-25249, 2005.
36. Li X, Pandak WM, Erickson SK, Ma Y, Yin L, Hylemon P, Ren S. Biosynthesis of the regulatory oxysterol, 5-cholesten-3beta,25-diol 3-sul-fate, in hepatocytes. J Lipid Res 48: 2587-2596, 2007.
37. Libby P. Current concepts of the pathogenesis of the acute coronary syndromes. Circulation 104: 365-372, 2001.
38. Ma Y, Xu L, Rodriguez-Agudo D, Li X, Heuman DM, Hylemon PB, Pandak WM, Ren S. 25-Hydroxycholesterol-3-sulfate regulates macro-phage lipid metabolism via the LXR/SREBP-1 signaling pathway. Am J Physiol Endocrinol Metab 295: E1369-E1379, 2008.
39. McIntyre TM, Pontsler AV, Silva AR, St HA, Xu Y, Hinshaw JC, Zimmerman GA, Hama K, Aoki J, Arai H, Prestwich GD. Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. Proc Natl Acad Sci USA 100: 131-136, 2003.
40. Mogensen TH, Berg RS, Paludan SR, Ostergaard L. Mechanisms of dexamethasone-mediated inhibition of Toll-like receptor signaling induced by Neisseria meningitidis and Streptococcus pneumoniae. Infect Immun 76: 189-197, 2008.
41. Morello F, Saglio E, Noghero A, Schiavone D, Williams TA, Verhovez A, Bussolino F, Veglio F, Mulatero P. LXR-activating oxysterols induce the expression of inflammatory markers in endothelial cells through LXR-independent mechanisms. Atherosclerosis 207: 38-44, 2009.
42. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Eagle AR, Vats D, Brombacher F, Ferrante AW, Chawla A. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120, 2007.
43. Ogata T, Miyauchi T, Sakai S, Irukayama-Tomobe Y, Goto K, Yamaguchi I. Stimulation of peroxisome-proliferator-activated receptor alpha (PPAR alpha) attenuates cardiac fibrosis and endothelin-1 production in pressure-overloaded rat hearts. Clin Sci (Lond) 103, Suppl 48: 284S-288S, 2002.
44. Pandak WM, Ren S, Marques D, Hall E, Redford K, Mallonee D, Bohdan P, Heuman D, Gil G, Hylemon P. Transport of cholesterol into mitochondria is rate-limiting for bile acid synthesis via the alternative pathway in primary rat hepatocytes. J Biol Chem 277: 48158-48164, 2002.
45. Park BH, Breyer B, He TC. Peroxisome proliferator-activated receptors: roles in tumorigenesis and chemoprevention in human cancer. Curr Opin Oncol 13: 78-83, 2001.
46. Prunet C, Montange T, Vejux A, Laubriet A, Rohmer JF, Riedinger JM, Athias A, Lemaire-Ewing S, Neel D, Petit JM, Steinmetz E, Brenot R, Gambert P, Lizard G. Multiplexed flow cytometric analyses of pro- and anti-inflammatory cytokines in the culture media of oxysterol-treated human monocytic cells and in the sera of atherosclerotic patients. Cytometry A 69: 359-373, 2006.
47. Rao P, Hayden MS, Long M, Scott ML, West AP, Zhang D, Oeck-inghaus A, Lynch C, Hoffmann A, Baltimore D, Ghosh S. IkappaBbeta acts to inhibit and activate gene expression during the inflammatory response. Nature 466: 1115-1119, 2010.
48. Ray M, Yu S, Sharda DR, Wilson CB, Liu Q, Kaushal N, Prabhu KS, Hankey PA. Inhibition of TLR4-induced IkappaB kinase activity by the RON receptor tyrosine kinase and its ligand, macrophage-stimulating protein. J Immunol 185: 7309-7316, 2010.
49. Ren S, Hylemon P, Marques D, Hall E, Redford K, Gil G, Pandak WM. Effect of increasing the expression of cholesterol transporters (StAR, MLN64, and SCP-2) on bile acid synthesis. J Lipid Res 45: 2123-2131, 2004.
50. Ren S, Hylemon P, Zhang ZP, Rodriguez-Agudo D, Marques D, Li X, Zhou H, Gil G, Pandak WM. Identification of a novel sulfonated oxysterol, 5-cholesten-3beta,25-diol 3-sulfonate, in hepatocyte nuclei and mitochondria. J Lipid Res 47: 1081-1090, 2006.
51. Ren S, Hylemon PB, Marques D, Gurley E, Bodhan P, Hall E, Redford K, Gil G, Pandak WM. Overexpression of cholesterol transporter StAR increases in vivo rates of bile acid synthesis in the rat and mouse. Hepatology 40: 910-917, 2004.
52. Ren S, Li X, Rodriguez-Agudo D, Gil G, Hylemon P, Pandak WM. Sulfated oxysterol, 25HC3S, is a potent regulator of lipid metabolism in human hepato-cytes. Biochem Biophys Res Commun 360: 802-808, 2007.
53. Rosklint T, Ohlsson BG, Wiklund O, Noren K, Hulten LM. Oxysterols induce interleukin-1beta production in human macrophages. Eur J Clin Invest 32: 35-42, 2002.
54. Solt LA, May MJ. The IkappaB kinase complex: master regulator of NF-kappaB signaling. Immunol Res 42: 3-18, 2008.
55. Torocsik D, Szanto A, Nagy L. Oxysterol signaling links cholesterol metabolism and inflammation via the liver X receptor in macrophages. Mol Aspects Med 30: 134-152, 2009.
56. Vejux A, Malvitte L, Lizard G. Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis. Braz J Med Biol Res 41: 545-556, 2008.
57. von Knethen A, Soller M, Brune B. Peroxisome proliferator-activated receptor gamma (PPAR gamma) and sepsis. Arch Immunol Ther Exp (Warsz) 55: 19-25, 2007.
58. Xu L, Bai Q, Rodriguez-Agudo D, Hylemon PB, Heuman DM, Pandak WM, Ren S. Regulation of hepatocyte lipid metabolism and inflammatory response by 25-hydroxycholesterol and 25-hydroxycholesterol-3-sulfate. Lipids 45: 821-832, 2010.
59. Yamamoto M, Takeda K. Role of nuclear IkappaB proteins in the regulation of host immune responses. J Infect Chemother 14: 265-269, 2008.