Transcription of Liver X Receptor Is Down-Regulated by 15-Deoxy-Δ12,14-Prostaglandin J2 through Oxidative Stress in Human Neutrophils

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Alba, Gonzalo ^a   Reyes, María Edith ^a   Santa María, Consuelo ^a   Ramírez, Remedios ^a   Geniz, Isabel ^b   Jiménez, Juan ^a   Martín Nieto, José ^c   Pintado, Elízabeth ^a   Sobrino, Francisco ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b Distrito Sanitario Sevilla Norte   (Spain)

^c UNIVERSITY OF ALICANTE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

15 DEOXY DELTA12,14 PROSTAGLANDIN J2; LIGAND; LIVER X RECEPTOR ALPHA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; REACTIVE OXYGEN METABOLITE; SERINE;

ABCA1 GENE; ABCG1 GENE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LXRALPHA GENE; MACROPHAGE; NEUTROPHIL; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; RNA SYNTHESIS; SREBP1C GENE;

BASE SEQUENCE; BLOTTING, WESTERN; CELLS, CULTURED; CHEMOTAXIS, LEUKOCYTE; DNA PRIMERS; DOWN-REGULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INFLAMMATION MEDIATORS; NEUTROPHILS; ORPHAN NUCLEAR RECEPTORS; OXIDATIVE STRESS; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROSTAGLANDIN D2; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SERINE; TRANSCRIPTION, GENETIC;

EID: 84868103662     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042195     Document Type: Article

References (82)

1. Laffitte BA, Joseph SB, Walczak R, Pei L, Wilpitz DC, et al. (2001) Autoregulation of the Human Liver X Receptor Alpha Promoter. Mol Cell Biol 21: 7558-7568.
2. Whitney KD, Watson MA, Goodwin B, Galardi CM, Maglich JM, et al. (2001) Liver X Receptor (LXR) Regulation of the LXRalpha Gene in Human Macrophages. J Biol Chem 276: 43509-43515.
3. Repa JJ, Mangelsdorf DJ, (2000) The Role of Orphan Nuclear Receptors in the Regulation of Cholesterol Homeostasis. Annu Rev Cell Dev Biol 16: 459-481.
4. Zelcer N, Tontonoz P, (2006) Liver X Receptors as Integrators of Metabolic and Inflammatory Signaling. J Clin Invest 116: 607-614.
5. Yu L, Hammer RE, Li-Hawkins J, Von Bergmann K, Lutjohann D, et al. (2002) Disruption of Abcg5 and Abcg8 in Mice Reveals their Crucial Role in Biliary Cholesterol Secretion. Proc Natl Acad Sci U S A 99: 16237-16242.
6. Bradley MN, Hong C, Chen M, Joseph SB, Wilpitz DC, et al. (2007) Ligand Activation of LXR Beta Reverses Atherosclerosis and Cellular Cholesterol Overload in Mice Lacking LXR Alpha and apoE. J Clin Invest 117: 2337-2346.
7. Repa JJ, Turley SD, Lobaccaro JA, Medina J, Li L, et al. (2000) Regulation of Absorption and ABC1-Mediated Efflux of Cholesterol by RXR Heterodimers. Science 289: 1524-1529.
8. Castrillo A, Joseph SB, Marathe C, Mangelsdorf DJ, Tontonoz P, (2003) Liver X Receptor-Dependent Repression of Matrix Metalloproteinase-9 Expression in Macrophages. J Biol Chem 278: 10443-10449.
9. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P, (2003) Reciprocal Regulation of Inflammation and Lipid Metabolism by Liver X Receptors. Nat Med 9: 213-219.
10. Castrillo A, Joseph SB, Vaidya SA, Haberland M, Fogelman AM, et al. (2003) Crosstalk between LXR and Toll-Like Receptor Signaling Mediates Bacterial and Viral Antagonism of Cholesterol Metabolism. Mol Cell 12: 805-816.
11. Castrillo A, Tontonoz P, (2004) Nuclear Receptors in Macrophage Biology: At the Crossroads of Lipid Metabolism and Inflammation. Annu Rev Cell Dev Biol 20: 455-480.
12. Valledor AF, (2005) The Innate Immune Response Under the Control of the LXR Pathway. Immunobiology 210: 127-132.
13. Pascual-Garcia M, Valledor AF (2012) Biological Roles of Liver X Receptors in Immune Cells. Arch Immunol Ther Exp (Warsz).
14. Joseph SB, McKilligin E, Pei L, Watson MA, Collins AR, et al. (2002) Synthetic LXR Ligand Inhibits the Development of Atherosclerosis in Mice. Proc Natl Acad Sci U S A 99: 7604-7609.
15. Fowler AJ, Sheu MY, Schmuth M, Kao J, Fluhr JW, et al. (2003) Liver X Receptor Activators Display Anti-Inflammatory Activity in Irritant and Allergic Contact Dermatitis Models: Liver-X-Receptor-Specific Inhibition of Inflammation and Primary Cytokine Production. J Invest Dermatol 120: 246-255.
16. Wang YY, Dahle MK, Agren J, Myhre AE, Reinholt FP, et al. (2006) Activation of the Liver X Receptor Protects Against Hepatic Injury in Endotoxemia by Suppressing Kupffer Cell Activation. Shock 25: 141-146.
17. Landis MS, Patel HV, Capone JP, (2002) Oxysterol Activators of Liver X Receptor and 9-Cis-Retinoic Acid Promote Sequential Steps in the Synthesis and Secretion of Tumor Necrosis Factor-Alpha from Human Monocytes. J Biol Chem 277: 4713-4721.
18. Fontaine C, Rigamonti E, Nohara A, Gervois P, Teissier E, et al. (2007) Liver X Receptor Activation Potentiates the Lipopolysaccharide Response in Human Macrophages. Circ Res 101: 40-49.
19. Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, et al. (2004) NAD(P)H Oxidase Nox-4 Mediates 7-Ketocholesterol-Induced Endoplasmic Reticulum Stress and Apoptosis in Human Aortic Smooth Muscle Cells. Mol Cell Biol 24: 10703-10717.
20. Lemaire-Ewing S, Prunet C, Montange T, Vejux A, Berthier A, et al. (2005) Comparison of the Cytotoxic, Pro-Oxidant and Pro-Inflammatory Characteristics of Different Oxysterols. Cell Biol Toxicol 21: 97-114.
21. Kawahito Y, Kondo M, Tsubouchi Y, Hashiramoto A, Bishop-Bailey D, et al. (2000) 15-Deoxy-Delta(12,14)-PGJ(2) Induces Synoviocyte Apoptosis and Suppresses Adjuvant-Induced Arthritis in Rats. J Clin Invest 106: 189-197.
22. Law RE, Goetze S, Xi XP, Jackson S, Kawano Y, et al. (2000) Expression and Function of PPARgamma in Rat and Human Vascular Smooth Muscle Cells. Circulation 101: 1311-1318.
23. Takata Y, Kitami Y, Yang ZH, Nakamura M, Okura T, et al. (2002) Vascular Inflammation is Negatively Autoregulated by Interaction between CCAAT/enhancer-Binding Protein-Delta and Peroxisome Proliferator-Activated Receptor-Gamma. Circ Res 91: 427-433.
24. Kliewer SA, Lenhard JM, Willson TM, Patel I, Morris DC, et al. (1995) A Prostaglandin J2 Metabolite Binds Peroxisome Proliferator-Activated Receptor Gamma and Promotes Adipocyte Differentiation. Cell 83: 813-819.
25. Couturier C, Brouillet A, Couriaud C, Koumanov K, Bereziat G, et al. (1999) Interleukin 1beta Induces Type II-Secreted Phospholipase A(2) Gene in Vascular Smooth Muscle Cells by a Nuclear Factor kappaB and Peroxisome Proliferator-Activated Receptor-Mediated Process. J Biol Chem 274: 23085-23093.
26. Meade EA, McIntyre TM, Zimmerman GA, Prescott SM, (1999) Peroxisome Proliferators Enhance Cyclooxygenase-2 Expression in Epithelial Cells. J Biol Chem 274: 8328-8334.
27. Harris SG, Smith RS, Phipps RP, (2002) 15-Deoxy-Delta 12,14-PGJ2 Induces IL-8 Production in Human T Cells by a Mitogen-Activated Protein Kinase Pathway. J Immunol 168: 1372-1379.
28. Imaizumi T, Kumagai M, Hatakeyama M, Tamo W, Yamashita K, et al. (2003) 15-Deoxy-Delta 12,14-Prostaglandin J2 Inhibits the Expression of Granulocyte-Macrophage Colony-Stimulating Factor in Endothelial Cells Stimulated with Lipopolysaccharide. Prostaglandins Other Lipid Mediat 71: 293-299.
29. Monneret G, Li H, Vasilescu J, Rokach J, Powell WS, (2002) 15-Deoxy-Delta 12,14-Prostaglandins D2 and J2 are Potent Activators of Human Eosinophils. J Immunol 168: 3563-3569.
30. Alba G, El Bekay R, Chacon P, Reyes ME, Ramos E, et al. (2008) Heme Oxygenase-1 Expression is Down-Regulated by Angiotensin II and Under Hypertension in Human Neutrophils. J Leukoc Biol 84: 397-405.
31. Kondo M, Oya-Ito T, Kumagai T, Osawa T, Uchida K, (2001) Cyclopentenone Prostaglandins as Potential Inducers of Intracellular Oxidative Stress. J Biol Chem 276: 12076-12083.
32. Alvarez-Maqueda M, El Bekay R, Alba G, Monteseirin J, Chacon P, et al. (2004) 15-Deoxy-Delta 12,14-Prostaglandin J2 Induces Heme Oxygenase-1 Gene Expression in a Reactive Oxygen Species-Dependent Manner in Human Lymphocytes. J Biol Chem 279: 21929-21937.
33. Chen YC, Shen SC, Tsai SH, (2005) Prostaglandin D(2) and J(2) Induce Apoptosis in Human Leukemia Cells Via Activation of the Caspase 3 Cascade and Production of Reactive Oxygen Species. Biochim Biophys Acta 1743: 291-304.
34. Mazor R, Shurtz-Swirski R, Farah R, Kristal B, Shapiro G, et al. (2008) Primed Polymorphonuclear Leukocytes Constitute a Possible Link between Inflammation and Oxidative Stress in Hyperlipidemic Patients. Atherosclerosis 197: 937-943.
35. Beaulieu AD, Paquin R, Rathanaswami P, McColl SR, (1992) Nuclear Signaling in Human Neutrophils. Stimulation of RNA Synthesis is a Response to a Limited Number of Proinflammatory Agonists. J Biol Chem 267: 426-432.
36. Carballo M, Marquez G, Conde M, Martin-Nieto J, Monteseirin J, et al. (1999) Characterization of Calcineurin in Human Neutrophils. Inhibitory Effect of Hydrogen Peroxide on its Enzyme Activity and on NF-kappaB DNA Binding. J Biol Chem 274: 93-100.
37. Gilbert C, Rollet-Labelle E, Naccache PH, (2002) Preservation of the Pattern of Tyrosine Phosphorylation in Human Neutrophil Lysates. II. A Sequential Lysis Protocol for the Analysis of Tyrosine Phosphorylation-Dependent Signalling. J Immunol Methods 261: 85-101.
38. Davies JQ, Gordon S, (2005) Isolation and Culture of Human Macrophages. Methods Mol Biol 290: 105-116.
39. Bradford MM, (1976) A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal Biochem 72: 248-254.
40. Naughton P, Foresti R, Bains SK, Hoque M, Green CJ, et al. (2002) Induction of Heme Oxygenase 1 by Nitrosative Stress. A Role for Nitroxyl Anion. J Biol Chem 277: 40666-40674.
41. El Bekay R, Alvarez M, Carballo M, Martin-Nieto J, Monteseirin J, et al. (2002) Activation of Phagocytic Cell NADPH Oxidase by Norfloxacin: A Potential Mechanism to Explain its Bactericidal Action. J Leukoc Biol 71: 255-261.
42. Mansfield MA, (1995) Rapid Immunodetection on Polyvinylidene Fluoride Membrane Blots without Blocking. Anal Biochem 229: 140-143.
43. Rothe G, Valet G, (1990) Flow Cytometric Analysis of Respiratory Burst Activity in Phagocytes with Hydroethidine and 2′,7′-Dichlorofluorescin. J Leukoc Biol 47: 440-448.
44. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, et al. (2001) A PPAR Gamma-LXR-ABCA1 Pathway in Macrophages is Involved in Cholesterol Efflux and Atherogenesis. Mol Cell 7: 161-171.
45. Santoro MG, (1994) Heat Shock Proteins and Virus Replication: Hsp70s as Mediators of the Antiviral Effects of Prostaglandins. Experientia 50: 1039-1047.
46. Chen M, Bradley MN, Beaven SW, Tontonoz P, (2006) Phosphorylation of the Liver X Receptors. FEBS Lett 580: 4835-4841.
47. Torra IP, Ismaili N, Feig JE, Xu CF, Cavasotto C, et al. (2008) Phosphorylation of Liver X Receptor Alpha Selectively Regulates Target Gene Expression in Macrophages. Mol Cell Biol 28: 2626-2636.
48. McLeish KR, Klein JB, Coxon PY, Head KZ, Ward RA, (1998) Bacterial Phagocytosis Activates Extracellular Signal-Regulated Kinase and p38 Mitogen-Activated Protein Kinase Cascades in Human Neutrophils. J Leukoc Biol 64: 835-844.
49. El Bekay R, Alvarez M, Monteseirin J, Alba G, Chacon P, et al. (2003) Oxidative Stress is a Critical Mediator of the Angiotensin II Signal in Human Neutrophils: Involvement of Mitogen-Activated Protein Kinase, Calcineurin, and the Transcription Factor NF-kappaB. Blood 102: 662-671.
50. Lu Y, Cederbaum A, (2007) The Mode of Cisplatin-Induced Cell Death in CYP2E1-Overexpressing HepG2 Cells: Modulation by ERK, ROS, Glutathione, and Thioredoxin. Free Radic Biol Med 43: 1061-1075.
51. Rochette-Egly C, (2003) Nuclear Receptors: Integration of Multiple Signalling Pathways through Phosphorylation. Cell Signal 15: 355-366.
52. Weigel NL, Zhang Y, (1998) Ligand-Independent Activation of Steroid Hormone Receptors. J Mol Med 76: 469-479.
53. Mo J, Fang SJ, Chen W, Blobe GC, (2002) Regulation of ALK-1 Signaling by the Nuclear Receptor LXRbeta. J Biol Chem 277: 50788-50794.
54. Tamura K, Chen YE, Horiuchi M, Chen Q, Daviet L, et al. (2000) LXRalpha Functions as a cAMP-Responsive Transcriptional Regulator of Gene Expression. Proc Natl Acad Sci U S A 97: 8513-8518.
55. Smoak K, Madenspacher J, Jeyaseelan S, Williams B, Dixon D, et al. (2008) Effects of Liver X Receptor Agonist Treatment on Pulmonary Inflammation and Host Defense. J Immunol 180: 3305-3312.
56. Baranowski M, (2008) Biological Role of Liver X Receptors. J Physiol Pharmacol 59Suppl 7: 31-55.
57. Mayadas TN, Tsokos GC, Tsuboi N, (2009) Mechanisms of Immune Complex-Mediated Neutrophil Recruitment and Tissue Injury. Circulation 120: 2012-2024.
58. Madamanchi NR, Vendrov A, Runge MS, (2005) Oxidative Stress and Vascular Disease. Arterioscler Thromb Vasc Biol 25: 29-38.
59. Puddu GM, Cravero E, Arnone G, Muscari A, Puddu P, (2005) Molecular Aspects of Atherogenesis: New Insights and Unsolved Questions. J Biomed Sci 12: 839-853.
60. Yasunari K, Watanabe T, Nakamura M, (2006) Reactive Oxygen Species Formation by Polymorphonuclear Cells and Mononuclear Cells as a Risk Factor of Cardiovascular Diseases. Curr Pharm Biotechnol 7: 73-80.
61. Rosenblat M, Aviram M, (2002) Oxysterol-Induced Activation of Macrophage NADPH-Oxidase Enhances Cell-Mediated Oxidation of LDL in the Atherosclerotic Apolipoprotein E Deficient Mouse: Inhibitory Role for Vitamin E. Atherosclerosis. 160: 69-80.
62. Joffre C, Leclere L, Buteau B, Martine L, Cabaret S, et al. (2007) Oxysterols Induced Inflammation and Oxidation in Primary Porcine Retinal Pigment Epithelial Cells. Curr Eye Res 32: 271-280.
63. Scher JU, Pillinger MH, (2009) The Anti-Inflammatory Effects of Prostaglandins. J Investig Med 57: 703-708.
64. Kim EH, Surh YJ, (2006) 15-Deoxy-Delta12,14-Prostaglandin J2 as a Potential Endogenous Regulator of Redox-Sensitive Transcription Factors. Biochem Pharmacol 72: 1516-1528.
65. Hong HY, Jeon WK, Kim BC, (2008) Up-Regulation of Heme Oxygenase-1 Expression through the Rac1/NADPH oxidase/ROS/p38 Signaling Cascade Mediates the Anti-Inflammatory Effect of 15-Deoxy-Delta 12,14-Prostaglandin J2 in Murine Macrophages. FEBS Lett 582: 861-868.
66. Moore KJ, Rosen ED, Fitzgerald ML, Randow F, Andersson LP, et al. (2001) The Role of PPAR-Gamma in Macrophage Differentiation and Cholesterol Uptake. Nat Med 7: 41-47.
67. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, et al. (2001) PPAR-Gamma Dependent and Independent Effects on Macrophage-Gene Expression in Lipid Metabolism and Inflammation. Nat Med 7: 48-52.
68. Kim MS, Sweeney TR, Shigenaga JK, Chui LG, Moser A, et al. (2007) Tumor Necrosis Factor and Interleukin 1 Decrease RXRalpha, PPARalpha, PPARgamma, LXRalpha, and the Coactivators SRC-1, PGC-1alpha, and PGC-1beta in Liver Cells. Metabolism 56: 267-279.
69. Li AC, Binder CJ, Gutierrez A, Brown KK, Plotkin CR, et al. (2004) Differential Inhibition of Macrophage Foam-Cell Formation and Atherosclerosis in Mice by PPARalpha, beta/delta, and Gamma. J Clin Invest 114: 1564-1576.
70. Wang JJ, Mak OT, (2011) Induction of Apoptosis by 15d-PGJ2 Via ROS Formation: An Alternative Pathway without PPARgamma Activation in Non-Small Cell Lung Carcinoma A549 Cells. Prostaglandins Other Lipid Mediat 94: 104-111.
71. Shin SW, Seo CY, Han H, Han JY, Jeong JS, et al. (2009) 15d-PGJ2 Induces Apoptosis by Reactive Oxygen Species-Mediated Inactivation of Akt in Leukemia and Colorectal Cancer Cells and shows in Vivo Antitumor Activity. Clin Cancer Res 15: 5414-5425.
72. Calpe-Berdiel L, Rotllan N, Fievet C, Roig R, Blanco-Vaca F, et al. (2008) Liver X Receptor-Mediated Activation of Reverse Cholesterol Transport from Macrophages to Feces in Vivo Requires ABCG5/G8. J Lipid Res 49: 1904-1911.
73. Stocker R, Keaney JF Jr, (2004) Role of Oxidative Modifications in Atherosclerosis. Physiol Rev 84: 1381-1478.
74. Bergt C, Pennathur S, Fu X, Byun J, O'Brien K, et al. (2004) The Myeloperoxidase Product Hypochlorous Acid Oxidizes HDL in the Human Artery Wall and Impairs ABCA1-Dependent Cholesterol Transport. Proc Natl Acad Sci U S A 101: 13032-13037.
75. Chen M, Li W, Wang N, Zhu Y, Wang X, (2007) ROS and NF-kappaB but Not LXR Mediate IL-1beta Signaling for the Downregulation of ATP-Binding Cassette Transporter A1. Am J Physiol Cell Physiol 292: C1493-501.
76. Moon HS, Chung CS, Lee HG, Kim TG, Choi YJ, et al. (2007) Inhibitory Effect of (-)-Epigallocatechin-3-Gallate on Lipid Accumulation of 3T3-L1 Cells. Obesity (Silver Spring) 15: 2571-2582.
77. Costet P, Luo Y, Wang N, Tall AR, (2000) Sterol-Dependent Transactivation of the ABC1 Promoter by the Liver X receptor/retinoid X Receptor. J Biol Chem 275: 28240-28245.
78. Hu E, Kim JB, Sarraf P, Spiegelman BM, (1996) Inhibition of Adipogenesis through MAP Kinase-Mediated Phosphorylation of PPARgamma. Science 274: 2100-2103.
79. Zhang B, Berger J, Zhou G, Elbrecht A, Biswas S, et al. (1996) Insulin- and Mitogen-Activated Protein Kinase-Mediated Phosphorylation and Activation of Peroxisome Proliferator-Activated Receptor Gamma. J Biol Chem 271: 31771-31774.
80. Zhou X, Yin Z, Guo X, Hajjar DP, Han J, (2010) Inhibition of ERK1/2 and Activation of Liver X Receptor Synergistically Induce Macrophage ABCA1 Expression and Cholesterol Efflux. J Biol Chem 285: 6316-6326.
81. Chen ZY, Tseng CC, (2005) 15-Deoxy-Delta12,14 Prostaglandin J2 Up-Regulates Kruppel-Like Factor 4 Expression Independently of Peroxisome Proliferator-Activated Receptor Gamma by Activating the Mitogen-Activated Protein Kinase kinase/extracellular Signal-Regulated Kinase Signal Transduction Pathway in HT-29 Colon Cancer Cells. Mol Pharmacol 68: 1203-1213.
82. Kim EH, Na HK, Surh YJ, (2006) Upregulation of VEGF by 15-Deoxy-Delta12,14-Prostaglandin J2 Via Heme Oxygenase-1 and ERK1/2 Signaling in MCF-7 Cells. Ann N Y Acad Sci 1090: 375-384.