Curcumin suppresses expression of low-density lipoprotein (LDL) receptor, leading to the inhibition of LDL-induced activation of hepatic stellate cells

British Journal of Pharmacology

Volumn 157, Issue 8, 2009, Pages 1354-1367

  Kang, Qiaohua ^a   Chen, Anping ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gene expression; Hepatic fibrosis; Hepatic stellate cell; Hypercholesterolemia; Low density lipoprotein; Non alcoholic steatohepatitis; Obesity

Indexed keywords

CHOLESTEROL; CURCUMIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PD 68235; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ANTAGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSFECTION; IN VITRO STUDY; LIVER CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STELLATE CELL; WESTERN BLOTTING;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHOLESTEROL; CURCUMIN; HEPATIC STELLATE CELLS; MALE; PPAR GAMMA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, LDL; SIGNAL TRANSDUCTION; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 70350341460     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2009.00261.x     Document Type: Article

References (61)

1. Amemiya-Kudo M, Shimano H, Yoshikawa T, Yahagi N, Hasty AH, Okazaki H et al. (2000). Promoter analysis of the mouse sterol regulatory element-binding protein-1c gene. J Biol Chem 275: 31078-31085.
2. Arafa HM (2005). Curcumin attenuates diet-induced hypercholester-olemia in rats. Med Sci Monit 11: BR228-BR234.
3. Asai A, Miyazawa T (2001). Dietary curcuminoids prevent high-fat diet-induced lipid accumulation in rat liver and epididymal adipose tissue. J Nutr 131: 2932-2935.
4. Babu PS, Srinivasan K (1997). Hypolipidemic action of curcumin, the active principle of turmeric (Curcuma longa) in streptozotocin induced diabetic rats. Mol Cell Biochem 166: 169-175.
5. Bilheimer DW, Goldstein JL, Grundy SM, Starzl TE, Brown MS (1984). Liver transplantation to provide low-density-lipoprotein receptors and lower plasma cholesterol in a child with homozygous familial hypercholesterolemia. N Engl J Med 311: 1658-1664.
6. Briggs MR, Yokoyama C, Wang X, Brown MS, Goldstein JL (1993). Nuclear protein that binds sterol regulatory element of low density lipoprotein receptor promoter. I. Identification of the protein and delineation of its target nucleotide sequence. J Biol Chem 268: 14490-14496.
7. Brown MS, Goldstein JL (1986). A receptor-mediated pathway for cholesterol homeostasis. Science 232: 34-47.
8. Brown MS, Goldstein JL (1997). The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340.
9. Castoreno AB, Wang Y, Stockinger W, Jarzylo LA, Du H, Pagnon JC et al. (2005). Transcriptional regulation of phagocytosis-induced membrane biogenesis by sterol regulatory element binding proteins. Proc Natl Acad Sci USA 102: 13129-13134.
10. Cave M, Deaciuc I, Mendez C, Song Z, Joshi-Barve S, Barve S et al. (2007). Nonalcoholic fatty liver disease: predisposing factors and the role of nutrition. J Nutr Biochem 18: 184-195.
11. Chen A, Davis BH (1999). UV irradiation activates JNK and increases alphaI(I) collagen gene expression in rat hepatic stellate cells. J Biol Chem 274: 158-164.
12. Chen A, Zhang L, Xu J, Tang J (2002). The antioxidant (-)-epigallocatechin-3-gallate inhibits activated hepatic stellate cell growth and suppresses acetaldehyde-induced gene expression. Biochem J 368: 695-704.
13. Clark JM (2006). The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol 40 (Suppl. 1): S5-S10.
14. Espenshade PJ, Hughes AL (2007). Regulation of sterol synthesis in eukaryotes. Annu Rev Genet 41: 401-427.
15. Fajas L, Schoonjans K, Gelman L, Kim JB, Najib J, Martin G et al. (1999). Regulation of peroxisome proliferator-activated receptor gamma expression by adipocyte differentiation and determination factor 1/sterol regulatory element binding protein 1: implications for adipocyte differentiation and metabolism. Mol Cell Biol 19: 5495-5503.
16. Fan CL, Qian Y, Wo XD, Yan J, Gao LP (2005). Effect of curcumin on the gene expression of low density lipoprotein receptors. Chin J Integr Med 11: 201-204.
17. Fiorucci S, Antonelli E, Rizzo G, Renga B, Mencarelli A, Riccardi L et al. (2004). The nuclear receptor SHP mediates inhibition of hepatic stellate cells by FXR and protects against liver fibrosis. Gastroenter-ology 127: 1497-1512.
18. Fiorucci S, Rizzo G, Antonelli E, Renga B, Mencarelli A, Riccardi L et al. (2005). Cross-talk between farnesoid-X-receptor (FXR) and peroxi-some proliferator-activated receptor gamma contributes to the anti-fibrotic activity of FXR ligands in rodent models of liver cirrhosis. J Pharmacol Exp Ther 315: 58-68.
19. Forman BM, Goode E, Chen J, Oro AE, Bradley DJ, Perlmann T et al. (1995). Identification of a nuclear receptor that is activated by farnesol metabolites. Cell 81: 687-693.
20. Friedman SL (2008). Mechanisms of hepatic fibrogenesis. Gastroenter-ology 134: 1655-1669.
21. Fu Y, Zheng S, Lin J, Ryerse J, Chen A (2008). Curcumin protects the rat liver from CCl4-caused injury and fibrogenesis by attenuating oxidative stress and suppressing inflammation. Mol Pharmacol 73: 399-409.
22. Galli A, Crabb D, Price D, Ceni E, Salzano R, Surrenti C et al. (2000). Peroxisome proliferator-activated receptor gamma transcriptional regulation is involved in platelet-derived growth factor-induced proliferation of human hepatic stellate cells. Hepatology 31: 101-108.
23. Goldstein JL, DeBose-Boyd RA, Brown MS (2006). Protein sensors for membrane sterols. Cell 124: 35-46.
24. Horton JD, Goldstein JL, Brown MS (2002). SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109: 1125-1131.
25. Jang EM, Choi MS, Jung UJ, Kim MJ, Kim HJ, Jeon SM et al. (2008). Beneficial effects of curcumin on hyperlipidemia and insulin resistance in high-fat-fed hamsters. Metabolism 57: 1576-1583.
26. Kapoor GS, Atkins BA, Mehta KD (2002). Activation of Raf-1/MEK-1/ 2/p42/44(MAPK) cascade alone is sufficient to uncouple LDL receptor expression from cell growth. Mol Cell Biochem 236: 13-22.
27. Kisseleva T, Brenner DA (2006). Hepatic stellate cells and the reversal of fibrosis. J Gastroenterol Hepatol 21 (Suppl. 3): S84-S87.
28. Kong B, Luyendyk JP, Tawfik O, Guo GL (2009). Farnesoid X receptor deficiency induces nonalcoholic steatohepatitis in low-density lipo-protein receptor-knockout mice fed a high-fat diet. J Pharmacol Exp Ther 328: 116-122.
29. Liu Y, Hong XQ (2006). Effect of three different curcumin pigmens on the prdiferation of vascular smooth muscle cells by ox-LDL and the expression of LDL-R. Zhongguo Zhong Yao Za Zhi 31: 500-503.
30. Lopez D, Ness GC (2006). Characterization of the rat LDL receptor 5′-flanking region. Biochim Biophys Acta 1761: 492-500.
31. Marra F, Efsen E, Romanelli RG, Caligiuri A, Pastacaldi S, Batignani G et al. (2000). Ligands of peroxisome proliferator-activated receptor gamma modulate profibrogenic and proinflammatory actions in hepatic stellate cells. Gastroenterology 119: 466-478.
32. Miyahara T, Schrum L, Rippe R, Xiong S, Yee HF Jr, Motomura K et al. (2000). Peroxisome proliferator-activated receptors and hepatic stellate cell activation. J Biol Chem 275: 35715-35722.
33. Moon YA, Shah NA, Mohapatra S, Warrington JA, Horton JD (2001). Identification of a mammalian long chain fatty acyl elongase regulated by sterol regulatory element-binding proteins. J Biol Chem 276: 45358-45366.
34. Nanji AA, Jokelainen K, Tipoe GL, Rahemtulla A, Thomas P, Dannen-berg AJ (2003). Curcumin prevents alcohol-induced liver disease in rats by inhibiting the expression of NF-kappa B-dependent genes. Am J Physiol Gastrointest Liver Physiol 284: G321-G327.
35. Neuschwander-Tetri BA (2001). Fatty liver and nonalcoholic steato-hepatitis. Clin Cornerstone 3: 47-57.
36. O'Brien PE, Dixon JB (2002). The extent of the problem of obesity. Am J Surg 184: 4S-8S.
37. O'Connell MA, Rushworth SA (2008). Curcumin: potential for hepatic fibrosis therapy? Br J Pharmacol 153: 403-405.
38. Osborne TF (2000). Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J Biol Chem 275: 32379-32382.
39. Park EJ, Jeon CH, Ko G, Kim J, Sohn DH (2000). Protective effect of curcumin in rat liver injury induced by carbon tetrachloride. J Pharm Pharmacol 52: 437-440.
40. Peschel D, Koerting R, Nass N (2007). Curcumin induces changes in expression of genes involved in cholesterol homeostasis. J Nutr Biochem 18: 113-119.
41. Ramirez-Tortosa MC, Mesa MD, Aguilera MC, Quiles JL, Baro L, Ramirez-Tortosa CL et al. (1999). Oral administration of a turmeric extract inhibits LDL oxidation and has hypocholesterolemic effects in rabbits with experimental atherosclerosis. Atherosclerosis 147: 371-378.
42. Rao DS, Sekhara NC, Satyanarayana MN, Srinivasan M (1970). Effect of curcumin on serum and liver cholesterol levels in the rat. J Nutr 100: 1307-1315.
43. Rothblat GH, Phillips MC (1982). Mechanism of cholesterol efflux from cells. Effects of acceptor structure and concentration. J Biol Chem 257: 4775-4782.
44. Sato R, Okamoto A, Inoue J, Miyamoto W, Sakai Y, Emoto N et al. (2000). Transcriptional regulation of the ATP citrate-lyase gene by sterol regulatory element-binding proteins. J Biol Chem 275: 12497-12502.
45. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW (2000). Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and realtime methods. Anal Biochem 285: 194-204.
46. Sharma AM, Staels B (2007). Review: peroxisome proliferator-activated receptor gamma and adipose tissue-understanding obesity-related changes in regulation of lipid and glucose metabolism. J Clin Endocrinol Metab 92: 386-395.
47. Shimomura I, Shimano H, Horton JD, Goldstein JL, Brown MS (1997). Differential expression of exons 1a and 1c in mRNAs for sterol regulatory element binding protein-1 in human and mouse organs and cultured cells. J Clin Invest 99: 838-845.
48. Shin DJ, Osborne TF (2003). Thyroid hormone regulation and cholesterol metabolism are connected through sterol regulatory element-binding protein-2 (SREBP-2). J Biol Chem 278: 34114-34118.
49. Shishodia S, Sethi G, Aggarwal BB (2005). Curcumin: getting back to the roots. Ann N Y Acad Sci 1056: 206-217.
50. Tomita K, Azuma T, Kitamura N, Nishida J, Tamiya G, Oka A et al. (2004). Pioglitazone prevents alcohol-induced fatty liver in rats through up-regulation of c-Met. Gastroenterology 126: 873-885.
51. Wong J, Quinn CM, Brown AJ (2006). SREBP-2 positively regulates transcription of the cholesterol efflux gene, ABCA1, by generating oxysterol ligands for LXR. Biochem J 400: 485-491.
52. Xu J, Fu Y, Chen A (2003). Activation of peroxisome proliferator- activated receptor-gamma contributes to the inhibitory effects of curcumin on rat hepatic stellate cell growth. Am J Physiol Gastrointest Liver Physiol 285: G20-G30.
53. Yasni S, Imaizumi K, Nakamura M, Aimoto J, Sugano M (1993). Effects of Curcuma xanthorrhiza Roxb. and curcuminoids on the level of serum and liver lipids, serum apolipoprotein A-I and lipogenic enzymes in rats. Food Chem Toxicol 31: 213-218.
54. Yeh M, Cole AL, Choi J, Liu Y, Tulchinsky D, Qiao JH et al. (2004). Role for sterol regulatory element-binding protein in activation of endothelial cells by phospholipid oxidation products. Circ Res 95: 780-788.
55. Yumei F, Zhou Y, Zheng S, Chen A (2006). The antifibrogenic effect of (-)-epigallocatechin gallate results from the induction of de novo synthesis of glutathione in passaged rat hepatic stellate cells. Lab Invest 86: 697-709.
56. Zhang W, Liu D, Wo X, Zhang Y, Jin M, Ding Z (1999). Effects of Curcuma Longa on proliferation of cultured bovine smooth muscle cells and on expression of low density lipoprotein receptor in cells. Chin Med J (Engl) 112: 308-311.
57. Zheng S, Chen A (2004). Activation of PPARgamma is required for curcumin to induce apoptosis and to inhibit the expression of extracellular matrix genes in hepatic stellate cells in vitro. Biochem J 384: 149-157.
58. Zheng S, Chen A (2006). Curcumin suppresses the expression of extracellular matrix genes in activated hepatic stellate cells by inhibiting gene expression of connective tissue growth factor. Am J Physiol Gastrointest Liver Physiol 290: G883-G893.
59. Zheng S, Chen A (2007). Disruption of transforming growth factor-beta signaling by curcumin induces gene expression of peroxisome proliferator- activated receptor-gamma in rat hepatic stellate cells. Am J Physiol Gastrointest Liver Physiol 292: G113-G123.
60. Zheng S, Yumei F, Chen A (2007). De novo synthesis of glutathione is a prerequisite for curcumin to inhibit hepatic stellate cell (HSC) activation. Free Radic Biol Med 43: 444-453.
61. Zhou Y, Zheng S, Lin J, Zhang QJ, Chen A (2007). The interruption of the PDGF and EGF signaling pathways by curcumin stimulates gene expression of PPARgamma in rat activated hepatic stellate cell in vitro. Lab Invest 87: 488-498.