Liver X receptor α activation with the synthetic ligand T0901317 reduces lung injury and inflammation after hemorrhage and resuscitation via inhibition of the nuclear factor κB pathway

Shock

Volumn 35, Issue 4, 2011, Pages 367-374

  Solan, Patrick D ^a,b   Piraino, Giovanna ^b   Hake, Paul W ^b   Denenberg, Alvin ^b   O'Connor, Michael ^b   Lentsch, Alex ^a   Zingarelli, Basilia ^b  

^a UNIVERSITY OF CINCINNATI   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Acute lung injury; Hemorrhage; Liver X receptor ; Nuclear factor B; T0901317

Indexed keywords

BICARBONATE; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LACTIC ACID; LIVER X RECEPTOR ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; N (2,2,2 TRIFLUOROETHYL) N [4 [2,2,2 TRIFLUORO 1 HYDROXY 1 (TRIFLUOROMETHOXY)ETHYL]PHENYL]BENZENESULFONAMIDE; TUMOR NECROSIS FACTOR ALPHA; CCL2 PROTEIN, RAT; CHOLESTEROL; FLUORINATED HYDROCARBON; INTERLEUKIN 10; LIVER X RECEPTOR; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; ORPHAN NUCLEAR RECEPTOR; SULFONAMIDE; TO-901317;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BICARBONATE BLOOD LEVEL; BLOOD PRESSURE; CONTROLLED STUDY; DNA BINDING; DRUG EFFECT; HEMORRHAGIC SHOCK; LACTATE BLOOD LEVEL; LUNG INJURY; MALE; MEAN ARTERIAL PRESSURE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; RAT; RESUSCITATION; ANIMAL; BLOOD; DISEASE MODEL; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; BICARBONATES; CHEMOKINE CCL2; CHEMOKINE CCL3; CHOLESTEROL; DISEASE MODELS, ANIMAL; HYDROCARBONS, FLUORINATED; INTERLEUKIN-10; INTERLEUKIN-6; LACTIC ACID; MALE; NF-KAPPA B; ORPHAN NUCLEAR RECEPTORS; RATS; RATS, WISTAR; SHOCK, HEMORRHAGIC; SIGNAL TRANSDUCTION; SULFONAMIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79961088146     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181f7d742     Document Type: Article

References (46)

1. Kauvar DS, Lefering R, Wade CE: Impact of hemorrhage on trauma outcome: an overview of epidemiology, clinical presentations, and therapeutic considerations. J Trauma 60:S3-S11, 2006.
2. Hierholzer C, Billiar TR: Molecular mechanisms in the early phase of hemorrhagic shock. Langenbecks Arch Surg 386:302-308, 2001.
3. Giannoudis PV: Current concepts of the inflammatory response after major trauma: an update. Injury 34:397-404, 2003.
4. Angele MK, Schneider CP, Chaudry IH: Bench-to-bedside review: latest results in hemorrhagic shock. Crit Care 12:218, 2008.
5. Jamroz-Wisniewska A, Wojcicka G, Horoszewicz K, Beltowski J: Liver X receptors (LXRs). Part II: non-lipid effects, role in pathology, and therapeutic implications. Postepy Hig Med Dosw (Online) 61:760-785, 2007.
6. Wojcicka G, Jamroz-Wisniewska A, Horoszewicz K, Beltowski J: Liver X receptors (LXRs). Part I: structure, function, regulation of activity, and role in lipid metabolism. Postepy Hig Med Dosw (Online) 61:736-759, 2007.
7. Baranowski M: Biological role of liver X receptors. J Physiol Pharmacol 59(Suppl 7):31-55, 2008.
8. Mangelsdorf DJ, Evans RM: The RXR heterodimers and orphan receptors. Cell 83:841-850, 1995.
9. Bensinger SJ, Tontonoz P: Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454:470-477, 2008.
10. Castrillo A, Joseph SB, Marathe C, Mangelsdorf DJ, Tontonoz P: Liver X receptor-dependent repression of matrix metalloproteinase-9 expression in macrophages. J Biol Chem 278:10443-10449, 2003.
11. Joseph SB, Castrillo A, Laffitte BA, Mangelsdorf DJ, Tontonoz P: Reciprocal regulation of inflammation and lipid metabolism by liver X receptors. Nat Med 9:213-219, 2003.
12. Myhre AE, Agren J, Dahle MK, Tamburstuen MV, Lyngstadaas SP, Collins AJ, Foster SJ, Thiemermann C, Aasen AO, Wang JE: Liver X receptor is a key regulator of cytokine release in human monocytes. Shock 29:468-474, 2008.
13. Wang YY, Dahle MK, Agren J, Myhre AE, Reinholt FP, Foster SJ, Collins JL, Thiemermann C, Aasen AO, Wang JE: Activation of the liver X receptor protects against hepatic injury in endotoxemia by suppressing Kupffer cell activation. Shock 25:141-146, 2006.
14. Fowler AJ, Sheu MY, Schmuth M, Kao J, Fluhr JW, Rhein L, Collins JL, Willson TM, Mangelsdorf DJ, Elias PM, et al.: 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, 2003.
15. Birrell MA, Catley MC, Hardaker E, Wong S, Willson TM, McCluskie K, Leonard T, Farrow SN, Collins JL, Haj-Yahia S, et al.: Novel role for the liver X nuclear receptor in the suppression of lung inflammatory responses. J Biol Chem 282:31882-31890, 2007.
16. Crisafulli C, Mazzon E, Paterniti I, Galuppo M, Bramanti P, Cuzzocrea S: Effects of Liver x receptor agonist treatment on signal transduction pathways in acute lung inflammation. Respir Res 11:19, 2010.
17. Zingarelli B: Nuclear factor-kappaB. Crit Care Med 33:S414-S416, 2005.
18. Zingarelli B, Sheehan M, Wong HR: Nuclear factor-kappaB as a therapeutic target in critical care medicine. Crit Care Med 31:S105-S111, 2003.
19. Piraino G, Cook JA, O'Connor M, Hake PW, Burroughs TJ, Teti D, Zingarelli B: Synergistic effect of peroxisome proliferator activated receptor-gamma and liver X receptor-alpha in the regulation of inflammation in macrophages. Shock 26:146-153, 2006.
20. Zingarelli B, Hake PW, Mangeshkar P, O'Connor M, Burroughs TJ, Piraino G, Denenberg A, Wong HR: Diverse cardioprotective signaling mechanisms of peroxisome proliferator-activated receptor-gamma ligands, 15-deoxy-Delta12,14- prostaglandin J2 and ciglitazone, in reperfusion injury: role of nuclear factor-kappaB, heat shock factor 1, and Akt. Shock 28:554-563, 2007.
21. Zingarelli B, Hake PW, O'Connor M, Burroughs TJ, Wong HR, Solomkin JS, Lentsch AB: Lung injury after hemorrhage is age dependent: role of peroxisome proliferator-activated receptor gamma. Crit Care Med 37:1978-1987, 2009.
22. Chima RS, Hake PW, Piraino G, Mangeshkar P, Denenberg A, Zingarelli B: Ciglitazone ameliorates lung inflammation by modulating the inhibitor kappaB protein kinase/nuclear factor-kappaB pathway after hemorrhagic shock. Crit Care Med 36:2849-2857, 2008.
23. Zingarelli B, Sheehan M, Hake PW, O'Connor M, Denenberg A, Cook JA: Peroxisome proliferator activator receptor-gamma ligands, 15-deoxy-Delta(12,14)- prostaglandin J2 and ciglitazone, reduce systemic inflammation in polymicrobial sepsis by modulation of signal transduction pathways. J Immunol 171:6827-6837, 2003.
24. Kim MS, Sweeney TR, Shigenaga JK, Chui LG, Moser A, Grunfeld C, Feingold KR: 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, 2007.
25. Morello F, de Boer RA, Steffensen KR, Gnecchi M, Chisholm JW, Boomsma F, Anderson LM, Lawn RM, Gustafsson JA, Lopez-Ilasaca M, et al.: Liver X receptors alpha and beta regulate renin expression in vivo. J Clin Invest 115: 1913-1922, 2005.
26. Leik CE, Carson NL, Hennan JK, Basso MD, Liu QY, Crandall DL, Nambi P: GW3965, a synthetic liver X receptor (LXR) agonist, reduces angiotensin II-mediated pressor responses in Sprague-Dawley rats. Br J Pharmacol 151: 450-456, 2007.
27. Kuipers I, van der Harst P, Kuipers F, van Genne L, Goris M, Lehtonen JY, van Veldhuisen DJ, van Gilst WH, de Boer RA: Activation of liver X receptor-alpha reduces activation of the renal and cardiac renin-angiotensin- aldosterone system. Lab Invest 90:630-636, 2010.
28. Rixen D, Siegel JH: Bench-to-bedside review: oxygen debt and its metabolic correlates as quantifiers of the severity of hemorrhagic and post-traumatic shock. Crit Care 9:441-453, 2005.
29. Giovannini I, Boldrini G, Chiarla C, Giuliante F, Vellone M, Nuzzo G: Path-ophysiologic correlates of hypocholesterolemia in critically ill surgical patients. Intensive Care Med 25:748-751, 1999.
30. Bonville DA, Parker TS, Levine DM, Gordon BR, Hydo LJ, Eachempati SR, Barie PS: The relationships of hypocholesterolemia to cytokine concentrations and mortality in critically ill patients with systemic inflammatory response syndrome. Surg Infect (Larchmt) 5:39-49, 2004.
31. Zhao C, Dahlman-Wright K: Liver X receptor in cholesterol metabolism. J Endocrinol 204:233-240, 2010.
32. Daull P, Blouin A, Cayer J, Beaudoin M, Belleville K, Sirois P, Nantel F, Chang TM, Battistini B: Profiling biochemical and hemodynamic markers using chronically instrumented, conscious and unrestrained rats undergoing severe, acute controlled hemorrhagic hypovolemic shock as an integrated in-vivo model system to assess new blood substitutes. Vascul Pharmacol 43:289-301, 2005.
33. Abarca S, Garcia R: Cholesterol metabolism in rat adrenal gland during reversible endotoxic shock. Eur J Biochem 211:829-834, 1993.
34. Bhatia M, Moochhala S: Role of inflammatory mediators in the pathophysi-ology of acute respiratory distress syndrome. J Pathol 202:145-156, 2004.
35. Abraham E: Neutrophils and acute lung injury. Crit Care Med 31:S195-S199, 2003.
36. Vedder NB, Winn RK, Rice CL, Chi EY, Arfors KE, Harlan JM: A monoclonal antibody to the adherence-promoting leukocyte glycoprotein, CD18, reduces organ injury and improves survival from hemorrhagic shock and resuscitation in rabbits. J Clin Invest 81:939-944, 1988.
37. Smoak K, Madenspacher J, Jeyaseelan S, Williams B, Dixon D, Poch KR, Nick JA, Worthen GS, Fessler MB: Effects of liver X receptor agonist treatment on pulmonary inflammation and host defense. J Immunol 180:3305-3312, 2008.
38. Gong H, He J, Lee JH, Mallick E, Gao X, Li S, Homanics GE, Xie W: Activation of the liver X receptor prevents lipopolysaccharide-induced lung injury. J Biol Chem 284:30113-30121, 2009.
39. Crisafulli C, Di Paola R, Mazzon E, Paterniti I, Galuppo M, Genovese T, Bramanti P, Cappellani A, Cuzzocrea S: Liver X receptor agonist treatment reduced splanchnic ischemia and reperfusion injury. J Leukoc Biol 87:309-321, 2010.
40. Deshmane SL, Kremlev S, Amini S, Sawaya BE: Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313-326, 2009.
41. Maurer M, von Stebut E: Macrophage inflammatory protein-1. Int J Biochem Cell Biol 36:1882-1886, 2004.
42. Kobayashi Y: The role of chemokines in neutrophil biology. Front Biosci 13:2400-2407, 2008.
43. Paterniti I, Genovese T, Mazzon E, Crisafulli C, Di Paola R, Galuppo M, Bramanti P, Cuzzocrea S: Liver X receptor agonist treatment regulates inflammatory response after spinal cord trauma. J Neurochem 112:611-624, 2010.
44. Yasuda T, Kanno M, Kawamoto M, Yuge O, Ninomiya Y: Suppression of inducible nitric oxide synthase and cyclooxygenase-2 gene expression by 22(R)-hydroxycholesterol requires de novo protein synthesis in activated macrophages. J Steroid Biochem Mol Biol 97:376-383, 2005.
45. Ghisletti S, Huang W, Ogawa S, Pascual G, Lin ME, Willson TM, Rosenfeld MG, Glass CK: Parallel SUMOylation-dependent pathways mediate gene- and signal-specific transrepression by LXRs and PPARgamma. Mol Cell 25:57-70, 2007.
46. Zuercher WJ, Buckholz RG, Campobasso N, Collins JL, Galardi CM, Gampe RT, Hyatt SM, Merrihew SL, Moore JT, Oplinger JA, et al.: Discovery of tertiary sulfonamides as potent liver X receptor antagonists. J Med Chem 53:3412-3416, 2010.