Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 3, 2011, Pages 513-519

  Caron, Sandrine ^a,b,c   Verrijken, An ^d   Mertens, Ilse ^d   Samanez, Carolina Huaman ^a,b,c   Mautino, Gisèle ^a,b,c,f   Haas, Joel T ^e   Duran Sandoval, Daniel ^a,b,c   Prawitt, Janne ^a,b,c   Francque, Sven ^d   Vallez, Emmanuelle ^a,b,c   Muhr Tailleux, Anne ^a,b,c   Berard, Isabelle ^f   Kuipers, Folkert ^g   Kuivenhoven, Jan A ^h   Biddinger, Sudha B ⁱ   Taskinen, Marja Riitta ^j   Van Gaal, Luc ^d   Staels, Bart ^a,b,c  

^a UNIV LILLE   (France)

^b INSERM   (France)

^c INSTITUT PASTEUR DE LILLE   (France)

^d ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f University of California ^*

^g UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^h ACADEMIC MEDICAL CENTER   (Netherlands)

ⁱ BOSTON CHILDREN S HOSPITAL   (United States)

^j HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

more..

Author keywords

apolipoproteins; lipids; metabolism; nuclear receptors; type II diabetes

Indexed keywords

APOLIPOPROTEIN C3; CARBOHYDRATE RESPONSE ELEMENT BINDING PROTEIN; FARNESOID X RECEPTOR; GLUCOSE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DIET RESTRICTION; DYSLIPIDEMIA; FEMALE; GLUCOSE METABOLISM; HUMAN; IN VIVO STUDY; LIVER CELL; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT; TRIACYLGLYCEROL BLOOD LEVEL;

EID: 79952119879     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.220723     Document Type: Article

References (47)

1. Sarwar N, Danesh J, Eiriksdottir G, Sigurdsson G, Wareham N, Bingham S, Boekholdt SM, Khaw K, Gudnason V. Triglycerides and the risk of coronary heart disease: 10,158 incident cases among 262,525 participants in 29 Western prospective studies. Circulation. 2007;115:450-458. (Pubitemid 46184196)
2. Adiels M, Olofsson S, Taskinen M, Borén J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol. 2008;28:1225-1236.
3. Zannis VI, Cole FS, Jackson CL, Kurnit DM, Karathanasis SK. Distribution of apolipoprotein A-I, C-II, C-III, and E mRNA in fetal human tissues. Time-dependent induction of apolipoprotein E mRNA by cultures of human monocyte-macrophages. Biochemistry. 1985;24:4450-4455. (Pubitemid 15228451)
4. Ginsberg HN, Le NA, Goldberg IJ, Gibson JC, Rubinstein A, Wang-Iverson P, Norum R, Brown WV. Apolipoprotein B metabolism in subjects with deficiency of apolipoproteins CIII and AI: evidence that apolipoprotein CIII inhibits catabolism of triglyceride-rich lipoproteins by lipoprotein lipase in vivo. J Clin Invest. 1986;78:1287-1295. (Pubitemid 17181567)
5. Maeda N, Li H, Lee D, Oliver P, Quarfordt SH, Osada J. Targeted disruption of the apolipoprotein C-III gene in mice results in hypotriglyceridemia and protection from postprandial hypertriglyceridemia. J Biol Chem. 1994;269:23610-23616. (Pubitemid 24293564)
6. Mendivil CO, Zheng C, Furtado J, Lel J, Sacks FM. Metabolism of very-low-density lipoprotein and low-density lipoprotein containing apolipoprotein C-III and not other small apolipoproteins. Arterioscler Thromb Vasc Biol. 2010;30:239-245.
7. Batal R, Tremblay M, Barrett PH, Jacques H, Fredenrich A, Mamer O, Davignon J, Cohn JS. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. J Lipid Res. 2000;41: 706-718. (Pubitemid 30314126)
8. Le NA, Gibson JC, Ginsberg HN. Independent regulation of plasma apolipoprotein C-II and C-III concentrations in very low density and high density lipoproteins: implications for the regulation of the catabolism of these lipoproteins. J Lipid Res. 1988;29:669-677.
9. Schonfeld G, George PK, Miller J, Reilly P, Witztum J. Apolipoprotein C-II and C-III levels in hyperlipoproteinemia. Metab Clin Exp. 1979;28: 1001-1010. (Pubitemid 10201198)
10. Stocks J, Holdsworth G, Galton D. Hypertriglyceridaemia associated with an abnormal triglyceride-rich lipoprotein carrying excess apolipoprotein C-III-2. Lancet. 1979;2:667-671. (Pubitemid 10236973)
11. Ito Y, Azrolan N, O'Connell A, Walsh A, Breslow JL. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science. 1990;249:790-793.
12. Jong MC, Rensen PC, Dahlmans VE, van der Boom H, van Berkel TJ, Havekes LM. Apolipoprotein C-III deficiency accelerates triglyceride hydrolysis by lipoprotein lipase in wild-type and apoE knockout mice. J Lipid Res. 2001;42:1578-1585. (Pubitemid 33026056)
13. Wang CS, McConathy WJ, Kloer HU, Alaupovic P. Modulation of lipoprotein lipase activity by apolipoproteins: effect of apolipoprotein C-III. J Clin Invest. 1985;75:384-390. (Pubitemid 15143476)
14. Mann CJ, Troussard AA, Yen FT, Hannouche N, Najib J, Fruchart JC, Lotteau V, André P, Bihain BE. Inhibitory effects of specific apolipoprotein C-III isoforms on the binding of triglyceride-rich lipoproteins to the lipolysis-stimulated receptor. J Biol Chem. 1997; 272:31348-31354. (Pubitemid 28013269)
15. Windler E, Havel RJ. Inhibitory effects of C apolipoproteins from rats and humans on the uptake of triglyceride-rich lipoproteins and their remnants by the perfused rat liver. J Lipid Res. 1985;26:556-565. (Pubitemid 15073727)
16. Cohn JS, Patterson BW, Uffelman KD, Davignon J, Steiner G. Rate of production of plasma and very-low-density lipoprotein (VLDL) apolipoprotein C-III is strongly related to the concentration and level of production of VLDL triglyceride in male subjects with different body weights and levels of insulin sensitivity. J Clin Endocrinol Metab. 2004; 89:3949-3955. (Pubitemid 39071498)
17. Petersen KF, Dufour S, Hariri A, Nelson-Williams C, Foo JN, Zhang X, Dziura J, Lifton RP, Shulman GI. Apolipoprotein C3 gene variants in nonalcoholic fatty liver disease. N Engl J Med. 2010;362:1082-1089.
18. Sacks FM, Alaupovic P, Moye LA, Cole TG, Sussex B, Stampfer MJ, Pfeffer MA, Braunwald E. VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation. 2000;102:1886-1892.
19. Chen X, Tian H, Liu R. Association of serum apolipoprotein C III levels and apolipoprotein C III gene Sst I polymorphism with carotid intima-media thickness in Chinese type 2 diabetic patients. Diabetes Res Clin Pract. 2004;66:41-47. (Pubitemid 39201370)
20. Florez H, Mendez A, Casanova-Romero P, Larreal-Urdaneta C, Castillo-Florez S, Lee D, Goldberg R. Increased apolipoprotein C-III levels associated with insulin resistance contribute to dyslipidemia in normoglycemic and diabetic subjects from a triethnic population. Atherosclerosis. 2006;188: 134-141. (Pubitemid 44142528)
21. Kawakami A, Aikawa M, Alcaide P, Luscinskas FW, Libby P, Sacks FM. Apolipoprotein CIII induces expression of vascular cell adhesion molecule-1 in vascular endothelial cells and increases adhesion of monocytic cells. Circulation. 2006;114:681-687. (Pubitemid 44252310)
22. Pollin TI, Damcott CM, Shen H, Ott SH, Shelton J, Horenstein RB, Post W, McLenithan JC, Bielak LF, Peyser PA, Mitchell BD, Miller M, O'Connell JR, Shuldiner AR. A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science. 2008;322:1702-1705.
23. Dallinga-Thie GM, Berk-Planken IIL, Bootsma AH, Jansen H. Atorvastatin decreases apolipoprotein C-III in apolipoprotein B-containing lipoprotein and HDL in type 2 diabetes: a potential mechanism to lower plasma triglycerides. Diabetes Care. 2004;27:1358-1364. (Pubitemid 38679983)
24. Hertz R, Bishara-Shieban J, Bar-Tana J. Mode of action of peroxisome proliferators as hypolipidemic drugs: suppression of apolipoprotein C-III. J Biol Chem. 1995;270:13470-13475.
25. Malmendier CL, Lontie JF, Delcroix C, Dubois DY, Magot T, De Roy L. Apolipoproteins C-II and C-III metabolism in hypertriglyceridemic patients: effect of a drastic triglyceride reduction by combined diet restriction and fenofibrate administration. Atherosclerosis. 1989;77: 139-149. (Pubitemid 19136714)
26. Pavlic M, Valéro R, Duez H, Xiao C, Szeto L, Patterson BW, Lewis GF. Triglyceride-rich lipoprotein-associated apolipoprotein C-III production is stimulated by plasma free fatty acids in humans. Arterioscler Thromb Vasc Biol. 2008;28:1660-1665.
27. Altomonte J, Cong L, Harbaran S, Richter A, Xu J, Meseck M, Dong HH. Foxo1 mediates insulin action on apoC-III and triglyceride metabolism. J Clin Invest. 2004;114:1493-1503. (Pubitemid 40385579)
28. Chen M, Breslow JL, Li W, Leff T. Transcriptional regulation of the apoC-III gene by insulin in diabetic mice: correlation with changes in plasma triglyceride levels. J Lipid Res. 1994;35:1918-1924. (Pubitemid 24353064)
29. Towle HC. Glucose as a regulator of eukaryotic gene transcription. Trends Endocrinol Metab. 2005;16:489-494. (Pubitemid 41660865)
30. Shih HM, Liu Z, Towle HC. Two CACGTG motifs with proper spacing dictate the carbohydrate regulation of hepatic gene transcription. J Biol Chem. 1995;270:21991-21997.
31. Iizuka K, Bruick RK, Liang G, Horton JD, Uyeda K. Deficiency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis. Proc Natl Acad Sci U S A. 2004;101: 7281-7286. (Pubitemid 38638024)
32. Yamashita H, Takenoshita M, Sakurai M, Bruick RK, Henzel WJ, Shillinglaw W, Arnot D, Uyeda K. A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc Natl Acad Sci U S A. 2001;98:9116-9121. (Pubitemid 32743878)
33. Adamson AW, Suchankova G, Rufo C, Nakamura MT, Teran-Garcia M, Clarke SD, Gettys TW. Hepatocyte nuclear factor-4α contributes to carbohydrate-induced transcriptional activation of hepatic fatty acid synthase. Biochem J. 2006;399:285-295. (Pubitemid 44570291)
34. Cha J, Repa JJ. The liver X receptor (LXR) and hepatic lipogenesis. The carbohydrate-response element-binding protein is a target gene of LXR. J Biol Chem. 2007;282:743-751. (Pubitemid 47076632)
35. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, Kahn CR. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell. 2000;6: 87-97.
36. Schippers IJ, Moshage H, Roelofsen H, Müller M, Heymans HS, Ruiters M, Kuipers F. Immortalized human hepatocytes as a tool for the study of hepatocytic (de-)differentiation. Cell Biol Toxicol. 1997;13:375-386. (Pubitemid 27373408)
37. Unwin N, Shaw J, Zimmet P, Alberti KG. Impaired glucose tolerance and impaired fasting glycaemia: the current status on definition and intervention. Diabet Med. 2002;19:708-723. (Pubitemid 35013848)
38. Lavrentiadou SN, Hadzopoulou-Cladaras M, Kardassis D, Zannis VI. Binding specificity and modulation of the human ApoCIII promoter activity by heterodimers of ligand-dependent nuclear receptors. Biochemistry. 1999;38:964-975.
39. Diaz Guerra MJ, Bergot MO, Martinez A, Cuif MH, Kahn A, Raymondjean M. Functional characterization of the L-type pyruvate kinase gene glucose response complex. Mol Cell Biol. 1993;13:7725-7733. (Pubitemid 23354297)
40. Mitro N, Mak PA, Vargas L, Godio C, Hampton E, Molteni V, Kreusch A, Saez E. The nuclear receptor LXR is a glucose sensor. Nature. 2007;445:219-223. (Pubitemid 46095727)
41. Claudel T, Inoue Y, Barbier O, Duran-Sandoval D, Kosykh V, Fruchart J, Fruchart J, Gonzalez FJ, Staels B. Farnesoid X receptor agonists suppress hepatic apolipoprotein CIII expression. Gastroenterology. 2003; 125:544-555. (Pubitemid 36929436)
42. Duivenvoorden I, Teusink B, Rensen PC, Romijn JA, Havekes LM, Voshol PJ. Apolipoprotein C3 deficiency results in diet-induced obesity and aggravated insulin resistance in mice. Diabetes. 2005;54:664-671. (Pubitemid 40322068)
43. Li WW, Dammerman MM, Smith JD, Metzger S, Breslow JL, Leff T. Common genetic variation in the promoter of the human apo CIII gene abolishes regulation by insulin and may contribute to hypertriglyceridemia. J Clin Invest. 1995;96:2601-2605.
44. Shin M, Blanche PJ, Rawlings RS, Fernstrom HS, Krauss RM. Increased plasma concentrations of lipoprotein(a) during a low-fat, highcarbohydrate diet are associated with increased plasma concentrations of apolipoprotein C-III bound to apolipoprotein B-containing lipoproteins. Am J Clin Nutr. 2007;85:1527-1532. (Pubitemid 46890419)
45. Yamamoto T, Shimano H, Nakagawa Y, Ide T, Yahagi N, Matsuzaka T, Nakakuki M, Takahashi A, Suzuki H, Sone H, Toyoshima H, Sato R, Yamada N. SREBP-1 interacts with hepatocyte nuclear factor-4α and interferes with PGC-1 recruitment to suppress hepatic gluconeogenic genes. J Biol Chem. 2004;279:12027-12035. (Pubitemid 38445764)
46. Coste H, Rodríguez JC. Orphan nuclear hormone receptor Rev-erbα regulates the human apolipoprotein CIII promoter. J Biol Chem. 2002; 277:27120-27129. (Pubitemid 34951726)
47. Qu S, Su D, Altomonte J, Kamagate A, He J, Perdomo G, Tse T, Jiang Y, Dong HH. PPARγ mediates the hypolipidemic action of fibrates by antagonizing FoxO1. Am J Physiol Endocrinol Metab. 2007;292: E421-E434. (Pubitemid 46220566)