Intestinal CREBH overexpression prevents high-cholesterol diet-induced hypercholesterolemia by reducing Npc1l1 expression

Molecular Metabolism

Volumn 5, Issue 11, 2016, Pages 1092-1102

  Kikuchi, Takuya ^a   Orihara, Kana ^a   Oikawa, Fusaka ^a   Han, Song iee ^a   Kuba, Motoko ^a   Okuda, Kanako ^a   Satoh, Aoi ^a   Osaki, Yoshinori ^a   Takeuchi, Yoshinori ^a   Aita, Yuichi ^a   Matsuzaka, Takashi ^a   Iwasaki, Hitoshi ^a   Yatoh, Shigeru ^a   Sekiya, Motohiro ^a   Yahagi, Naoya ^a   Suzuki, Hiroaki ^a   Sone, Hirohito ^b   Nakagawa, Yoshimi ^a   Yamada, Nobuhiro ^a   Shimano, Hitoshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Cholesterol; CREBH; Intestine; Npc1l1

Indexed keywords

CHOLESTEROL; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN H; FIBROBLAST GROWTH FACTOR 21; GLUCOSE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABC TRANSPORTER G5; ABC TRANSPORTER G8; CARRIER PROTEIN; CREB3L3 PROTEIN, HUMAN; CREB3L3 PROTEIN, MOUSE; LIPOPROTEIN; MEMBRANE PROTEIN; NPC1L1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BILE LEVEL; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CHOLESTEROL METABOLISM; CONTROLLED STUDY; FECES LEVEL; GALLBLADDER; GENE; GENE EXPRESSION; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; INTESTINE; KNOCKOUT MOUSE; LIPID METABOLISM; MOUSE; NONHUMAN; NPC1/1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE LEVEL; TRIGLYCERIDE METABOLISM; WILD TYPE MOUSE; ANIMAL; CHOLESTEROL INTAKE; METABOLISM; PHYSIOLOGY;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 5; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 8; ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTEROL, DIETARY; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HUMANS; HYPERCHOLESTEROLEMIA; LIPOPROTEINS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE;

EID: 84994777338     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2016.09.004     Document Type: Article

References (49)

1. [1] Patel, A., Barzi, F., Jamrozik, K., Lam, T.H., Ueshima, H., Whitlock, G., et al. Serum triglycerides as a risk factor for cardiovascular diseases in the Asia-Pacific region. Circulation 110:17 (2004), 2678–2686.
2. [2] Xie, P., Zhu, H., Jia, L., Ma, Y., Tang, W., Wang, Y., et al. Genetic demonstration of intestinal NPC1L1 as a major determinant of hepatic cholesterol and blood atherogenic lipoprotein levels. Atherosclerosis 237:2 (2014), 609–617.
3. [3] Iqbal, J., Hussain, M.M., Intestinal lipid absorption. American Journal of Physiology. Endocrinology and Metabolism 296:6 (2009), E1183–E1194.
4. [4] Temel, R.E., Brown, J.M., A new model of reverse cholesterol transport: enTICEing strategies to stimulate intestinal cholesterol excretion. Trends in Pharmacological Sciences 36:7 (2015), 440–451.
5. [5] van der Velde, A.E., Vrins, C.L., van den Oever, K., Kunne, C., Oude Elferink, R.P., Kuipers, F., et al. Direct intestinal cholesterol secretion contributes significantly to total fecal neutral sterol excretion in mice. Gastroenterology 133:3 (2007), 967–975.
6. [6] Engelking, L.J., McFarlane, M.R., Li, C.K., Liang, G., Blockade of cholesterol absorption by ezetimibe reveals a complex homeostatic network in enterocytes. Journal of Lipid Research 53:7 (2012), 1359–1368.
7. [7] Davis, H.R. Jr., Zhu, L.J., Hoos, L.M., Tetzloff, G., Maguire, M., Liu, J., et al. Niemann-Pick C1 Like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis. The Journal of Biological Chemistry 279:32 (2004), 33586–33592.
8. [8] Altmann, S.W., Davis, H.R. Jr., Zhu, L.J., Yao, X., Hoos, L.M., Tetzloff, G., et al. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303:5661 (2004), 1201–1204.
9. [9] Cannon, C.P., Blazing, M.A., Giugliano, R.P., McCagg, A., White, J.A., Theroux, P., et al. Ezetimibe added to statin therapy after acute coronary syndromes. New England Journal of Medicine 372:25 (2015), 2387–2397.
10. [10] Jakulj, L., Vissers, M.N., van Roomen, C.P., van der Veen, J.N., Vrins, C.L., Kunne, C., et al. Ezetimibe stimulates faecal neutral sterol excretion depending on abcg8 function in mice. FEBS Letters 584:16 (2010), 3625–3628.
11. [11] Graf, G.A., Cohen, J.C., Hobbs, H.H., Missense mutations in ABCG5 and ABCG8 disrupt heterodimerization and trafficking. The Journal of Biological Chemistry 279:23 (2004), 24881–24888.
12. [12] Temel, R.E., Gebre, A.K., Parks, J.S., Rudel, L.L., Compared with Acyl-CoA:cholesterol O-acyltransferase (ACAT) 1 and lecithin:cholesterol acyltransferase, ACAT2 displays the greatest capacity to differentiate cholesterol from sitosterol. The Journal of Biological Chemistry 278:48 (2003), 47594–47601.
13. [13] Graf, G.A., Li, W.P., Gerard, R.D., Gelissen, I., White, A., Cohen, J.C., et al. Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface. The Journal of Clinical Investigation 110:5 (2002), 659–669.
14. [14] Yu, L., Hammer, R.E., Li-Hawkins, J., Von Bergmann, K., Lutjohann, D., Cohen, J.C., et al. Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proceedings of the National Academy of Sciences of the United States of America 99:25 (2002), 16237–16242.
15. [15] Yu, L., Li-Hawkins, J., Hammer, R.E., Berge, K.E., Horton, J.D., Cohen, J.C., et al. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. The Journal of Clinical Investigation 110:5 (2002), 671–680.
16. [16] Tachibana, S., Hirano, M., Hirata, T., Matsuo, M., Ikeda, I., Ueda, K., et al. Cholesterol and plant sterol efflux from cultured intestinal epithelial cells is mediated by ATP-binding cassette transporters. Bioscience Biotechnology and Biochemistry 71:8 (2007), 1886–1895.
17. [17] Omori, Y., Imai, J., Watanabe, M., Komatsu, T., Suzuki, Y., Kataoka, K., et al. CREB-H: a novel mammalian transcription factor belonging to the CREB/ATF family and functioning via the box-B element with a liver-specific expression. Nucleic Acids Research 29:10 (2001), 2154–2162.
18. [18] Luebke-Wheeler, J., Zhang, K., Battle, M., Si-Tayeb, K., Garrison, W., Chhinder, S., et al. Hepatocyte nuclear factor 4alpha is implicated in endoplasmic reticulum stress-induced acute phase response by regulating expression of cyclic adenosine monophosphate responsive element binding protein H. Hepatology 48:4 (2008), 1242–1250.
19. [19] Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., Rutkowski, D.T., et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124:3 (2006), 587–599.
20. [20] Kim, H., Mendez, R., Zheng, Z., Chang, L., Cai, J., Zhang, R., et al. Liver-enriched transcription factor CREBH interacts with peroxisome proliferator-activated receptor alpha to regulate metabolic hormone FGF21. Endocrinology 155:3 (2014), 769–782.
21. [21] Nakagawa, Y., Satoh, A., Yabe, S., Furusawa, M., Tokushige, N., Tezuka, H., et al. Hepatic CREB3L3 controls whole-body energy homeostasis and improves obesity and diabetes. Endocrinology 155:12 (2014), 4706–4719.
22. [22] Kuba, M., Matsuzaka, T., Matsumori, R., Saito, R., Kaga, N., Taka, H., et al. Absence of Elovl6 attenuates steatohepatitis but promotes gallstone formation in a lithogenic diet-fed Ldlr(-/-) mouse model. Scientific Reports, 5, 2015, 17604.
23. [23] Nakagawa, Y., Shimano, H., Yoshikawa, T., Ide, T., Tamura, M., Furusawa, M., et al. TFE3 transcriptionally activates hepatic IRS-2, participates in insulin signaling and ameliorates diabetes. Nature Medicine 12:1 (2006), 107–113.
24. [24] Kobayashi, M., Ikegami, H., Fujisawa, T., Nojima, K., Kawabata, Y., Noso, S., et al. Prevention and treatment of obesity, insulin resistance, and diabetes by bile acid-binding resin. Diabetes 56:1 (2007), 239–247.
25. [25] Folch, J., Lees, M., Sloane Stanley, G.H., A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 226:1 (1957), 497–509.
26. [26] Short, M.K., Clouthier, D.E., Schaefer, I.M., Hammer, R.E., Magnuson, M.A., Beale, E.G., Tissue-specific, developmental, hormonal, and dietary regulation of rat phosphoenolpyruvate carboxykinase-human growth hormone fusion genes in transgenic mice. Molecular and Cellular Biology 12:3 (1992), 1007–1020.
27. [27] Reihner, E., Stahlberg, D., Lithogenic diet and gallstone formation in mice: integrated response of activities of regulatory enzymes in hepatic cholesterol metabolism. British Journal of Nutrition 76:5 (1996), 765–772.
28. [28] Tepperman, J., Caldwell, F.T., Tepperman, H.M., Induction of gallstones in mice by feeding a cholesterol-cholic acid containing diet. American Journal of Physiology 206 (1964), 628–634.
29. [29] Brunham, L.R., Kruit, J.K., Iqbal, J., Fievet, C., Timmins, J.M., Pape, T.D., et al. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. The Journal of Clinical Investigation 116:4 (2006), 1052–1062.
30. [30] Iqbal, J., Parks, J.S., Hussain, M.M., Lipid absorption defects in intestine-specific microsomal triglyceride transfer protein and ATP-binding cassette transporter A1-deficient mice. The Journal of Biological Chemistry 288:42 (2013), 30432–30444.
31. [31] Alrefai, W.A., Annaba, F., Sarwar, Z., Dwivedi, A., Saksena, S., Singla, A., et al. Modulation of human Niemann-Pick C1-like 1 gene expression by sterol: role of sterol regulatory element binding protein 2. American Journal of Physiology. Gastrointestinal and Liver Physiology 292:1 (2007), G369–G376.
32. [32] Lee, J.H., Giannikopoulos, P., Duncan, S.A., Wang, J., Johansen, C.T., Brown, J.D., et al. The transcription factor cyclic AMP-responsive element-binding protein H regulates triglyceride metabolism. Nature Medicine 17:7 (2011), 812–815.
33. [33] Zhang, C., Wang, G., Zheng, Z., Maddipati, K.R., Zhang, X., Dyson, G., et al. Endoplasmic reticulum-tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology 55:4 (2012), 1070–1082.
34. [34] Nakagawa, Y., Oikawa, F., Mizuno, S., Ohno, H., Yagishita, Y., Satoh, A., et al. Hyperlipidemia and hepatitis in liver-specific CREB3L3 knockout mice generated using a one-step CRISPR/Cas9 system. Scientific Reports, 6, 2016, 27857.
35. [35] Garcia-Calvo, M., Lisnock, J., Bull, H.G., Hawes, B.E., Burnett, D.A., Braun, M.P., et al. The target of ezetimibe is Niemann-Pick C1-Like 1 (NPC1L1). Proceedings of the National Academy of Sciences of the United States of America 102:23 (2005), 8132–8137.
36. [36] Buhman, K.K., Accad, M., Novak, S., Choi, R.S., Wong, J.S., Hamilton, R.L., et al. Resistance to diet-induced hypercholesterolemia and gallstone formation in ACAT2-deficient mice. Nature Medicine 6:12 (2000), 1341–1347.
37. [37] Jia, L., Ma, Y., Liu, G., Yu, L., Dietary cholesterol reverses resistance to diet-induced weight gain in mice lacking Niemann-Pick C1-Like 1. Journal of Lipid Research 51:10 (2010), 3024–3033.
38. [38] Wang, X., Sugimoto, K., Fujisawa, T., Shindo, N., Minato, S., Kamada, Y., et al. Novel effect of ezetimibe to inhibit the development of non-alcoholic fatty liver disease in Fatty Liver Shionogi mouse. Hepatology Research 44:1 (2014), 102–113.
39. [39] Davies, J.P., Scott, C., Oishi, K., Liapis, A., Ioannou, Y.A., Inactivation of NPC1L1 causes multiple lipid transport defects and protects against diet-induced hypercholesterolemia. The Journal of Biological Chemistry 280:13 (2005), 12710–12720.
40. [40] Yu, L., York, J., von Bergmann, K., Lutjohann, D., Cohen, J.C., Hobbs, H.H., Stimulation of cholesterol excretion by the liver X receptor agonist requires ATP-binding cassette transporters G5 and G8. The Journal of Biological Chemistry 278:18 (2003), 15565–15570.
41. [41] Lino, M., Farr, S., Baker, C., Fuller, M., Trigatti, B., Adeli, K., Intestinal scavenger receptor class B type I as a novel regulator of chylomicron production in healthy and diet-induced obese states. American Journal of Physiology. Gastrointestinal and Liver Physiology 309:5 (2015), G350–G359.
42. [42] Nguyen, D.V., Drover, V.A., Knopfel, M., Dhanasekaran, P., Hauser, H., Phillips, M.C., Influence of class B scavenger receptors on cholesterol flux across the brush border membrane and intestinal absorption. Journal of Lipid Research 50:11 (2009), 2235–2244.
43. [43] Bietrix, F., Yan, D., Nauze, M., Rolland, C., Bertrand-Michel, J., Comera, C., et al. Accelerated lipid absorption in mice overexpressing intestinal SR-BI. The Journal of Biological Chemistry 281:11 (2006), 7214–7219.
44. [44] van der Veen, J.N., van Dijk, T.H., Vrins, C.L., van Meer, H., Havinga, R., Bijsterveld, K., et al. Activation of the liver X receptor stimulates trans-intestinal excretion of plasma cholesterol. The Journal of Biological Chemistry 284:29 (2009), 19211–19219.
45. [45] Repa, J.J., Berge, K.E., Pomajzl, C., Richardson, J.A., Hobbs, H., Mangelsdorf, D.J., Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. The Journal of Biological Chemistry 277:21 (2002), 18793–18800.
46. [46] Repa, J.J., Turley, S.D., Lobaccaro, J.A., Medina, J., Li, L., Lustig, K., et al. Regulation of absorption and ABC1-mediated efflux of cholesterol by RXR heterodimers. Science 289:5484 (2000), 1524–1529.
47. [47] Malerod, L., Juvet, L.K., Hanssen-Bauer, A., Eskild, W., Berg, T., Oxysterol-activated LXRalpha/RXR induces hSR-BI-promoter activity in hepatoma cells and preadipocytes. Biochemical and Biophysical Research Communications 299:5 (2002), 916–923.
48. [48] Repa, J.J., Liang, G., Ou, J., Bashmakov, Y., Lobaccaro, J.M., Shimomura, I., et al. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes & Development 14:22 (2000), 2819–2830.
49. [49] Valasek, M.A., Clarke, S.L., Repa, J.J., Fenofibrate reduces intestinal cholesterol absorption via PPARalpha-dependent modulation of NPC1L1 expression in mouse. Journal of Lipid Research 48:12 (2007), 2725–2735.