Activation of liver-X-receptor α but not liver-X-receptor β protects against myocardial ischemia/reperfusion injury

Circulation: Heart Failure

Volumn 7, Issue 6, 2014, Pages 1032-1041

  He, Qing ^a   Pu, Jun ^a   Yuan, Ancai ^a   Lau, Wayne Bond ^b   Gao, Erhe ^c   Koch, Walter J ^c   Ma, Xin Liang ^b   He, Ben ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cytoplasmic and nuclear; Myocardium; Receptors; Reperfusion injury

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; ANTIOXIDANT; CASPASE 12; CASPASE 3; CASPASE 8; CASPASE 9; CCAAT ENHANCER BINDING PROTEIN; CYTOCHROME C; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; BENZOIC ACID DERIVATIVE; BENZYLAMINE DERIVATIVE; ISOPROTEIN; LIVER X RECEPTOR; ORPHAN NUCLEAR RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENE SILENCING; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE METABOLISM; HEART PROTECTION; HEART RATE; IN VIVO STUDY; MEAN ARTERIAL PRESSURE; MOUSE; NITRATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; TREATMENT OUTCOME; UPREGULATION; AGONISTS; ANIMAL; ENDOPLASMIC RETICULUM; KNOCKOUT MOUSE; LIVER MITOCHONDRION; MALE; METABOLISM; MYOCARDIAL REPERFUSION INJURY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BENZOATES; BENZYLAMINES; ENDOPLASMIC RETICULUM; GENE SILENCING; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; MYOCARDIAL REPERFUSION INJURY; ORPHAN NUCLEAR RECEPTORS; OXIDATIVE STRESS; PROTEIN ISOFORMS; UP-REGULATION;

EID: 84923855325     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.114.001260     Document Type: Article

References (33)

1. Pu J, Mintz GS, Brilakis ES, Banerjee S, Abdel-Karim AR, Maini B, Biro S, Lee JB, Stone GW, Weisz G, Maehara A. In vivo characterization of coronary plaques: novel findings from comparing greyscale and virtual histology intravascular ultrasound and near-infrared spectroscopy. Eur Heart J. 2012;33:372-383.
2. Pu J, Mintz GS, Biro S, Lee JB, Sum ST, Madden SP, Burke AP, Zhang P, He B, Goldstein JA, Stone GW, Muller JE, Virmani R, Maehara A. Insights into echo-attenuated plaques, echolucent plaques, and plaques with spotty calcification: novel findings from comparisons among intravascular ultrasound, near-infrared spectroscopy, and pathological histology in 2,294 human coronary artery segments. J Am Coll Cardiol. 2014;63:2220-2233.
3. Lotz C, Lazariotto M, Redel A, Smul TM, Stumpner J, Blomeyer C, Tischer-Zeitz T, Schmidt J, Pociej J, Roewer N, Kehl F, Lange M. Activation of peroxisome-proliferator-activated receptors α and γ mediates remote ischemic preconditioning against myocardial infarction in vivo. Exp Biol Med (Maywood). 2011;236:113-122.
4. Shan P, Pu J, Yuan A, Shen L, Shen L, Chai D, He B. RXR agonists inhibit oxidative stress-induced apoptosis in H9c2 rat ventricular cells. Biochem Biophys Res Commun. 2008;375:628-633.
5. Cheng Z, Völkers M, Din S, Avitabile D, Khan M, Gude N, Mohsin S, Bo T, Truffa S, Alvarez R, Mason M, Fischer KM, Konstandin MH, Zhang XK, Heller Brown J, Sussman MA. Mitochondrial translocation of Nur77 mediates cardiomyocyte apoptosis. Eur Heart J. 2011;32:2179-2188.
6. Pu J, Yuan A, Shan P, Gao E, Wang X, Wang Y, Lau WB, Koch W, Ma XL, He B. Cardiomyocyte-expressed farnesoid-X-receptor is a novel apoptosis mediator and contributes to myocardial ischaemia/reperfusion injury. Eur Heart J. 2013;34:1834-1845.
7. Calkin AC, Tontonoz P. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol. 2012;13:213-224.
8. Ishibashi M, Filomenko R, Rebe C, Chevriaux A, Varin A, Derangere V, Bessede G, Gambert P, Lagrost L, Masson D. Knock-down of the oxysterol receptor LXRalpha impairs cholesterol efflux in human primary macrophages: lack of compensation by LXRbeta activation. Biochem Pharmacol. 2013;86:122-129.
9. Bischoff ED, Daige CL, Petrowski M, Dedman H, Pattison J, Juliano J, Li AC, Schulman IG. Non-redundant roles for LXRalpha and LXRbeta in atherosclerosis susceptibility in low density lipoprotein receptor knockout mice. J Lipid Res. 2010;51:900-906.
10. Bradley MN, Hong C, Chen M, Joseph SB, Wilpitz DC, Wang X, Lusis AJ, Collins A, Hseuh WA, Collins JL, Tangirala RK, Tontonoz P. Ligand activation of LXR beta reverses atherosclerosis and cellular cholesterol overload in mice lacking LXR alpha and apoE. J Clin Invest. 2007;117:2337-2346.
11. Wu S, Yin R, Ernest R, Li Y, Zhelyabovska O, Luo J, Yang Y, Yang Q. Liver X receptors are negative regulators of cardiac hypertrophy via suppressing NF-kappaB signalling. Cardiovasc Res. 2009;84:119-126.
12. Kuipers I, Li J, Vreeswijk-Baudoin I, Koster J, van der Harst P, Silljé HH, Kuipers F, van Veldhuisen DJ, van Gilst WH, de Boer RA. Activation of liver X receptors with T0901317 attenuates cardiac hypertrophy in vivo. Eur J Heart Fail. 2010;12:1042-1050.
13. Lei P, Baysa A, Nebb HI, Valen G, Skomedal T, Osnes JB, Yang Z, Haugen F. Activation of Liver X receptors in the heart leads to accumulation of intracellular lipids and attenuation of ischemia-reperfusion injury. Basic Res Cardiol. 2013;108:323.
14. Morales JR, Ballesteros I, Deniz JM, Hurtado O, Vivancos J, Nombela F, Lizasoain I, Castrillo A, Moro MA. Activation of liver X receptors promotes neuroprotection and reduces brain inflammation in experimental stroke. Circulation. 2008;118:1450-1459.
15. 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. 2010;90:630-636.
16. Ma H, Gong H, Chen Z, Liang Y, Yuan J, Zhang G, Wu J, Ye Y, Yang C, Nakai A, Komuro I, Ge J, Zou Y. Association of Stat3 with HSF1 plays a critical role in G-CSF-induced cardio-protection against ischemia/reperfusion injury. J Mol Cell Cardiol. 2012;52:1282-1290.
17. Kang YM, Zhang AQ, Zhao XF, Cardinale JP, Elks C, Cao XM, Zhang ZW, Francis J. Paraventricular nucleus corticotrophin releasing hormone contributes to sympathoexcitation via interaction with neurotransmitters in heart failure. Basic Res Cardiol. 2011;106:473-483.
18. Apfel R, Benbrook D, Lernhardt E, Ortiz MA, Salbert G, Pfahl M. A novel orphan receptor specific for a subset of thyroid hormone-responsive elements and its interaction with the retinoid/thyroid hormone receptor subfamily. Mol Cell Biol. 1994;14:7025-7035.
19. Fan X, Kim HJ, Bouton D, Warner M, Gustafsson JA. Expression of liver X receptor beta is essential for formation of superficial cortical layers and migration of later-born neurons. Proc Natl Acad Sci U S A. 2008;105:13445-13450.
20. Korach-André M, Parini P, Larsson L, Arner A, Steffensen KR, Gustafsson JA. Separate and overlapping metabolic functions of LXRalpha and LXRbeta in C57Bl/6 female mice. Am J Physiol Endocrinol Metab. 2010;298:E167-E178.
21. Hessvik NP, Boekschoten MV, Baltzersen MA, Kersten S, Xu X, Andersén H, Rustan AC, Thoresen GH. LXR{beta} is the dominant LXR subtype in skeletal muscle regulating lipogenesis and cholesterol efflux. Am J Physiol Endocrinol Metab. 2010;298:E602-E613.
22. Spyridon M, Moraes LA, Jones CI, Sage T, Sasikumar P, Bucci G, Gibbins JM. LXR as a novel antithrombotic target. Blood. 2011;117: 5751-5761.
23. Faulds MH, Zhao C, Dahlman-Wright K. Molecular biology and functional genomics of liver X receptors (LXR) in relationship to metabolic diseases. Curr Opin Pharmacol. 2010;10:692-697.
24. ElAli A, Hermann DM. Liver X receptor activation enhances blood-brain barrier integrity in the ischemic brain and increases the abundance of ATP-binding cassette transporters ABCB1 and ABCC1 on brain capillary cells. Brain Pathol. 2012;22:175-187.
25. 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. 2010;87:309-321.
26. 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. 2010;11:19.
27. El Roz A, Bard JM, Huvelin JM, Nazih H. LXR agonists and ABCG1-dependent cholesterol efflux in MCF-7 breast cancer cells: relation to proliferation and apoptosis. Anticancer Res. 2012;32:3007-3013.
28. Lo Sasso G, Bovenga F, Murzilli S, Salvatore L, Di Tullio G, Martelli N, D'Orazio A, Rainaldi S, Vacca M, Mangia A, Palasciano G, Moschetta A. Liver X receptors inhibit proliferation of human colorectal cancer cells and growth of intestinal tumors in mice. Gastroenterology. 2013;144:1497-1507, 1507.e1.
29. Pommier AJ, Alves G, Viennois E, Bernard S, Communal Y, Sion B, Marceau G, Damon C, Mouzat K, Caira F, Baron S, Lobaccaro JM. Liver X Receptor activation downregulates AKT survival signaling in lipid rafts and induces apoptosis of prostate cancer cells. Oncogene. 2010;29:2712-2723.
30. Lin J, Steenbergen C, Murphy E, Sun J. Estrogen receptor-beta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation. 2009;120:245-254.
31. Tsang S, Wu S, Liu J, Wong TM. Testosterone protects rat hearts against ischaemic insults by enhancing the effects of alpha(1)-adrenoceptor stimulation. Br J Pharmacol. 2008;153:693-709.
32. Laffitte BA, Joseph SB, Walczak R, Pei L, Wilpitz DC, Collins JL, Tontonoz P. Autoregulation of the human liver X receptor alpha promoter. Mol Cell Biol. 2001;21:7558-7568.
33. Seo JB, Moon HM, Kim WS, Lee YS, Jeong HW, Yoo EJ, Ham J, Kang H, Park MG, Steffensen KR, Stulnig TM, Gustafsson JA, Park SD, Kim JB. Activated liver X receptors stimulate adipocyte differentiation through induction of peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol. 2004;24:3430-3444.