Activation of Liver X receptors in the heart leads to accumulation of intracellular lipids and attenuation of ischemia-reperfusion injury

Basic Research in Cardiology

Volumn 108, Issue 1, 2013, Pages

  Lei, Peng ^a,b,d   Baysa, Anton ^b,d   Nebb, Hilde Irene ^b   Valen, Guro ^b,d   Skomedal, Tor ^c,d   Osnes, Jan Bjørn ^c,d   Yang, Zaiqing ^a   Haugen, Fred ^b,d  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d Center for Heart Failure Research   (Norway)

Author keywords

GW3965; Lipid droplets; Liver X receptor; Myocardial infarction

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; FAT DROPLET; LIPID; LIVER X RECEPTOR ALPHA; LIVER X RECEPTOR BETA; MESSENGER RNA; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL STRAIN HL 1 CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORONARY ARTERY LIGATION; GENE EXPRESSION; HEART; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HOMEOSTASIS; HYPOXIA; ISCHEMIA; LIPID ANALYSIS; LIPOGENESIS; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REOXYGENATION; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

EID: 84871397031     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0323-z     Document Type: Article

References (57)

1. 2+ and cell death during ischaemia-reperfusion injury in cardiomyocytes. J Physiol 587:1331-1341. doi: 10.1113/jphysiol.2008.163311
2. Bilet L, van de Weijer T, Hesselink MK, Glatz JF, Lamb HJ, Wildberger J, Kooi ME, Schrauwen P, Schrauwen-Hinderling VB (2011) Exercise-induced modulation of cardiac lipid content in healthy lean young men. Basic Res Cardiol 106:307-315. doi: 10.1007/s00395-010-0144-x
3. Boergesen M, Pedersen TA, Gross B, van Heeringen SJ, Hagenbeek D, Bindesboll C, Caron S, Lalloyer F, Steffensen KR, Nebb HI, Gustafsson JA, Stunnenberg HG, Staels B, Mandrup S (2012) Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol Cell Biol 32:852-867. doi: 10.1128/MCB.06175-11
4. Borradaile NM, Schaffer JE (2005) Lipotoxicity in the heart. Curr Hypertens Rep 7:412-417 (Pubitemid 43136936)
5. Brindley DN, Kok BP, Kienesberger PC, Lehner R, Dyck JR (2010) Shedding light on the enigma of myocardial lipotoxicity: the involvement of known and putative regulators of fatty acid storage and mobilization. Am J Physiol Endocrinol Metab 298:E897-E908. doi: 10.1152/ajpendo.00509.2009
6. Broderick TL, Currie RW, Paulson DJ (1997) Heat stress induces rapid recovery of mechanical function of ischemic fatty acid perfused hearts by stimulating glucose oxidation during reperfusion. Can J Physiol Pharmacol 75:1273-1279 (Pubitemid 28130366)
7. Calkin AC, Tontonoz P (2012) Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol 13:213-224. doi: 10.1038/nrm3312
8. Chawla A, Boisvert WA, Lee CH, Laffitte BA, Barak Y, Joseph SB, Liao D, Nagy L, Edwards PA, Curtiss LK, Evans RM, Tontonoz P (2001) A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol Cell 7:161-171. doi: 10.1016/S1097-2765(01)00164-2 (Pubitemid 32162909)
9. Chisholm JW, Hong J, Mills SA, Lawn RM (2003) The LXR ligand T0901317 induces severe lipogenesis in the db/db diabetic mouse. J Lipid Res 44:2039-2048. doi: 10.1194/jlr.M300135-JLR200 (Pubitemid 37509619)
10. Chokshi A, Drosatos K, Cheema FH, Ji R, Khawaja T, Yu S, Kato T, Khan R, Takayama H, Knoll R, Milting H, Chung CS, Jorde U, Naka Y, Mancini DM, Goldberg IJ, Schulze PC (2012) Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure. Circulation 125:2844-2853. doi: 10.1161/CIRCULATIONAHA.111.060889
11. Chu K, Miyazaki M, Man WC, Ntambi JM (2006) Stearoyl-coenzyme A desaturase 1 deficiency protects against hypertriglyceridemia and increases plasma high-density lipoprotein cholesterol induced by liver X receptor activation. Mol Cell Biol 26:6786-6798. doi: 10.1128/MCB.00077-06 (Pubitemid 44387629)
12. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr (1998) HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 95:2979-2984 (Pubitemid 28135840)
13. Cole MA, Murray AJ, Cochlin LE, Heather LC, McAleese S, Knight NS, Sutton E, Jamil AA, Parassol N, Clarke K (2011) A high fat diet increases mitochondrial fatty acid oxidation and uncoupling to decrease efficiency in rat heart. Basic Res Cardiol 106:447-457. doi: 10.1007/s00395-011-0156-1
14. Collins JL, Fivush AM, Watson MA, Galardi CM, Lewis MC, Moore LB, Parks DJ, Wilson JG, Tippin TK, Binz JG, Plunket KD, Morgan DG, Beaudet EJ, Whitney KD, Kliewer SA, Willson TM (2002) Identification of a nonsteroidal liver X receptor agonist through parallel array synthesis of tertiary amines. J Med Chem 45:1963-1966 (Pubitemid 34477709)
15. Crisafulli C, Di Paola R, Mazzon E, Paterniti I, Galuppo M, Genovese T, Bramanti P, Cappellani A, Cuzzocrea S (2010) Liver X receptor agonist treatment reduced splanchnic ischemia and reperfusion injury. J Leukoc Biol 87:309-321. doi: 10.1189/jlb.0609438
16. Czibik G, Gravning J, Martinov V, Ishaq B, Knudsen E, Attramadal H, Valen G (2011) Gene therapy with hypoxia-inducible factor 1 alpha in skeletal muscle is cardioprotective in vivo. Life Sci 88:543-550. doi: 10.1016/j.lfs.2011.01.006
17. Flowers MT, Ntambi JM (2008) Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism. Curr Opin Lipidol 19:248-256. doi: 10.1097/MOL.0b013e3282f9b54d (Pubitemid 351653562)
18. Haugen F, Drevon CA (2007) The interplay between nutrients and the adipose tissue. Proc Nutr Soc 66:171-182. doi: 10.1017/S0029665107005423 (Pubitemid 46684971)
19. Haugen F, Zahid N, Dalen KT, Hollung K, Nebb HI, Drevon CA (2005) Resistin expression in 3T3-L1 adipocytes is reduced by arachidonic acid. J Lipid Res 46:143-153. doi: 10.1194/jlr.M400348-JLR200 (Pubitemid 40066680)
20. Heather LC, Clarke K (2011) Metabolism, hypoxia and the diabetic heart. J Mol Cell Cardiol 50:598-605. doi: 10.1016/j.yjmcc.2011.01.007
21. Hessvik NP, Boekschoten MV, Baltzersen MA, Kersten S, Xu X, Andersen H, Rustan AC, Thoresen GH (2010) LXRβ is the dominant LXR subtype in skeletal muscle regulating lipogenesis and cholesterol efflux. Am J Physiol Endocrinol Metab 298:E602-E613. doi: 10.1152/ajpendo.00553.2009
22. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118:1915-1919. doi: 10.1161/CIRCULATIONAHA.108.805242
23. Janowski BA, Willy PJ, Devi TR, Falck JR, Mangelsdorf DJ (1996) An oxysterol signalling pathway mediated by the nuclear receptor LXRα. Nature 383:728-731. doi: 10.1038/383728a0 (Pubitemid 26360651)
24. Jodalen H, Stangeland L, Grong K, Vik-Mo H, Lekven J (1985) Lipid accumulation in the myocardium during acute regional ischaemia in cats. J Mol Cell Cardiol 17:973-980 pii:S0022-2828(85)80077-8 (Pubitemid 16228238)
25. Juvet LK, Andresen SM, Schuster GU, Dalen KT, Tobin KA, Hollung K, Haugen F, Jacinto S, Ulven SM, Bamberg K, Gustafsson JA, Nebb HI (2003) On the role of liver X receptors in lipid accumulation in adipocytes. Mol Endocrinol 17:172-182 (Pubitemid 36187394)
26. King LM, Opie LH (1998) Glucose and glycogen utilisation in myocardial ischemia-changes in metabolism and consequences for the myocyte. Mol Cell Biochem 180:3-26 (Pubitemid 28118799)
27. Kotokorpi P, Venteclef N, Ellis E, Gustafsson JA, Mode A (2010) The human ADFP gene is a direct liver-X-receptor (LXR) target gene and differentially regulated by synthetic LXR ligands. Mol Pharmacol 77:79-86. doi: 10.1124/mol.109.059063
28. Kuramoto K, Okamura T, Yamaguchi T, Nakamura TY, Wakabayashi S, Morinaga H, Nomura M, Yanase T, Otsu K, Usuda N, Matsumura S, Inoue K, Fushiki T, Kojima Y, Hashimoto T, Sakai F, Hirose F, Osumi T (2012) Perilipin 5, a lipid droplet-binding protein, protects heart from oxidative burden by sequestering fatty acid from excessive oxidation. J Biol Chem 287:23852-23863. doi: 10.1074/jbc.M111.328708
29. Lopaschuk GD, Ussher JR, Folmes CD, Jaswal JS, Stanley WC (2010) Myocardial fatty acid metabolism in health and disease. Physiol Rev 90:207-258. doi: 10.1152/physrev.00015.2009
30. Matsui H, Yokoyama T, Sekiguchi K, Iijima D, Sunaga H, Maniwa M, Ueno M, Iso T, Arai M, Kurabayashi M (2012) Stearoyl-CoA desaturase-1 (SCD1) augments saturated fatty acid-induced lipid accumulation and inhibits apoptosis in cardiac myocytes. PLoS ONE 7:e33283. doi: 10.1371/journal.pone.0033283
31. McGavock JM, Victor RG, Unger RH, Szczepaniak LS, American College of P, the American Physiological S, (2006) Adiposity of the heart, revisited. Ann Intern Med 144:517-524. pii:144/7/517 (Pubitemid 46780675)
32. Menendez JA, Colomer R, Lupu R (2004) Inhibition of tumor-associated fatty acid synthase activity enhances vinorelbine (Navelbine)-induced cytotoxicity and apoptotic cell death in human breast cancer cells. Oncol Rep 12:411-422
33. Mitro N, Vargas L, Romeo R, Koder A, Saez E (2007) T0901317 is a potent PXR ligand: implications for the biology ascribed to LXR. FEBS Lett 581:1721-1726. doi: 10.1016/j.febslet.2007.03.047 (Pubitemid 46602262)
34. Miyazaki M, Ntambi JM (2003) Role of stearoyl-coenzyme A desaturase in lipid metabolism. Prostaglandins Leukot Essent Fatty Acids 68:113-121 (Pubitemid 36216475)
35. Montessuit C, Papageorgiou I, Campos L, Lerch R (2006) Retinoic acids increase expression of GLUT4 in dedifferentiated and hypertrophied cardiac myocytes. Basic Res Cardiol 101:27-35. doi: 10.1007/s00395-005-0567-y (Pubitemid 43323429)
36. O'Connell TD, Rodrigo MC, Simpson PC (2007) Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 357:271-296. doi: 10.1385/1-59745-214-9:271 (Pubitemid 350183253)
37. Ouvrier A, Cadet R, Vernet P, Laillet B, Chardigny JM, Lobaccaro JM, Drevet JR, Saez F (2009) LXR and ABCA1 control cholesterol homeostasis in the proximal mouse epididymis in a cell-specific manner. J Lipid Res 50:1766-1775. doi: 10.1194/jlr.M800657-JLR200
38. Peter A, Weigert C, Staiger H, Rittig K, Cegan A, Lutz P, Machicao F, Haring HU, Schleicher E (2008) Induction of stearoyl-CoA desaturase protects human arterial endothelial cells against lipotoxicity. Am J Physiol Endocrinol Metab 295:E339-E349. doi: 10.1152/ajpendo.00022.2008
39. Phelan CA, Weaver JM, Steger DJ, Joshi S, Maslany JT, Collins JL, Zuercher WJ, Willson TM, Walker M, Jaye M, Lazar MA (2008) Selective partial agonism of liver X receptor alpha is related to differential corepressor recruitment. Mol Endocrinol 22:2241-2249. doi: 10.1210/me.2008-0041
40. Reue K (2011) A thematic review series: lipid droplet storage and metabolism: from yeast to man. J Lipid Res 52:1865-1868. doi: 10.1194/jlr.E020602
41. Ruusalepp A, Czibik G, Flatebo T, Vaage J, Valen G (2007) Myocardial protection evoked by hyperoxic exposure involves signaling through nitric oxide and mitogen activated protein kinases. Basic Res Cardiol 102:318-326. doi: 10.1007/s00395-007-0644-5 (Pubitemid 46909710)
42. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, Li L, Schwendner S, Wang S, Thoolen M, Mangelsdorf DJ, Lustig KD, Shan B (2000) Role of LXRs in control of lipogenesis. Genes Dev 14:2831-2838. doi: 10.1101/Gad.850400
43. Sironi L, Mitro N, Cimino M, Gelosa P, Guerrini U, Tremoli E, Saez E (2008) Treatment with LXR agonists after focal cerebral ischemia prevents brain damage. FEBS Lett 582:3396-3400. doi: 10.1016/j.febslet.2008.08.035
44. Skyschally A, Schulz R, Heusch G (2008) Pathophysiology of myocardial infarction: protection by ischemic pre- and postconditioning. Herz 33:88-100. doi: 10.1007/s00059-008-3101-9 (Pubitemid 351437850)
45. Son NH, Yu S, Tuinei J, Arai K, Hamai H, Homma S, Shulman GI, Abel ED, Goldberg IJ (2010) PPARγ-induced cardiolipotoxicity in mice is ameliorated by PPARα deficiency despite increases in fatty acid oxidation. J Clin Invest 120:3443-3454. doi: 10.1172/JCI40905
46. Sparrow CP, Baffic J, Lam MH, Lund EG, Adams AD, Fu X, Hayes N, Jones AB, Macnaul KL, Ondeyka J, Singh S, Wang J, Zhou G, Moller DE, Wright SD, Menke JG (2002) A potent synthetic LXR agonist is more effective than cholesterol loading at inducing ABCA1 mRNA and stimulating cholesterol efflux. J Biol Chem 277:10021-10027. doi: 10.1074/jbc.M108225200 (Pubitemid 34968111)
47. Stanley WC, Lopaschuk GD, Hall JL, McCormack JG (1997) Regulation of myocardial carbohydrate metabolism under normal and ischaemic conditions. Potential for pharmacological interventions. Cardiovasc Res 33:243-257 (Pubitemid 27072627)
48. Straeter-Knowlen IM, Evanochko WT, den Hollander JA, Wolkowicz PE, Balschi JA, Caulfield JB, Ku DD, Pohost GM (1996) 1H NMR spectroscopic imaging of myocardial triglycerides in excised dog hearts subjected to 24 hours of coronary occlusion. Circulation 93:1464-1470 (Pubitemid 26099359)
49. Suzuki J, Shen WJ, Nelson BD, Patel S, Veerkamp JH, Selwood SP, Murphy GM Jr, Reaven E, Kraemer FB (2001) Absence of cardiac lipid accumulation in transgenic mice with heart-specific HSL overexpression. Am J Physiol Endocrinol Metab 281:E857-E866
50. Tontonoz P, Kim JB, Graves RA, Spiegelman BM (1993) ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol Cell Biol 13:4753-4759
51. Vary TC, Reibel DK, Neely JR (1981) Control of energy metabolism of heart muscle. Annu Rev Physiol 43:419-430. doi: 10.1146/annurev.ph.43.030181.002223
52. Wagner BL, Valledor AF, Shao G, Daige CL, Bischoff ED, Petrowski M, Jepsen K, Baek SH, Heyman RA, Rosenfeld MG, Schulman IG, Glass CK (2003) Promoter-specific roles for liver X receptor/corepressor complexes in the regulation of ABCA1 and SREBP1 gene expression. Mol Cell Biol 23:5780-5789 (Pubitemid 36951340)
53. Wang H, Sreenevasan U, Hu H, Saladino A, Polster BM, Lund LM, Gong DW, Stanley WC, Sztalryd C (2011) Perilipin 5, a lipid droplet-associated protein, provides physical and metabolic linkage to mitochondria. J Lipid Res 52:2159-2168. doi: 10.1194/jlr.M017939
54. Weedon-Fekjaer MS, Dalen KT, Solaas K, Staff AC, Duttaroy AK, Nebb HI (2010) Activation of LXR increases acyl-CoA synthetase activity through direct regulation of ACSL3 in human placental trophoblast cells. J Lipid Res 51:1886-1896. doi: 10.1194/jlr.M004978
55. Wende AR, Abel ED (2010) Lipotoxicity in the heart. Biochim Biophys Acta 1801:311-319. doi: 10.1016/j.bbalip.2009.09.023
56. Williams S, Bledsoe RK, Collins JL, Boggs S, Lambert MH, Miller AB, Moore J, McKee DD, Moore L, Nichols J, Parks D, Watson M, Wisely B, Willson TM (2003) X-ray crystal structure of the liver X receptor beta ligand binding domain: regulation by a histidine-tryptophan switch. J Biol Chem 278:27138-27143. doi: 10.1074/jbc.M302260200 (Pubitemid 36876869)
57. Wu S, Yin R, Ernest R, Li Y, Zhelyabovska O, Luo J, Yang Y, Yang Q (2009) Liver X receptors are negative regulators of cardiac hypertrophy via suppressing NF-κB signalling. Cardiovasc Res 84:119-126. doi: 10.1093/cvr/cvp180