Hepatic lipid accumulation in apolipoprotein C-I-deficient mice is potentiated by cholesteryl ester transfer protein

Journal of Lipid Research

Volumn 48, Issue 1, 2007, Pages 30-40

  Gautier, Thomas ^a   Tietge, Uwe J F ^a   Boverhof, Renze ^a   Perton, Frank G ^a   Le Guern, Naig ^b   Masson, David ^b   Rensen, Patrick C N ^c,d   Havekes, Louis M ^c,d   Lagrost, Laurent ^b   Kuipers, Folkert ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b INSERM   (France)

^c TNO   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Bile; Cholesterol; Liver; Triglycerides

Indexed keywords

APOLIPOPROTEIN C1; BILE ACID; CHOLESTEROL; CHOLESTEROL ESTER TRANSFER PROTEIN; HIGH DENSITY LIPOPROTEIN; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL MODEL; ARTICLE; BILE SECRETION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; INSULIN METABOLISM; LIPID METABOLISM; LIPID STORAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRESS;

EID: 33845993893     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M600205-JLR200     Document Type: Article

References (63)

1. Barter, P. J., H. B. Brewer, Jr., M. J. Chapman, C. H. Hennekens, D. J. Rader, and A. R. Tall. 2003. Cholesteryl ester transfer protein: a novel target for raising HDL and inhibiting atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23: 160-167.
2. Lagrost, L. 1994. Regulation of cholesteryl ester transfer protein (CETP) activity: review of in vitro and in vivo studies. Biochim. Biophys. Acta. 1215: 209-236.
3. Schwartz, C. C., J. M. VandenBroek, and P. S. Cooper. 2004. Lipoprotein cholesteryl ester production, transfer, and output in vivo in humans. J. Lipid Res. 45: 1594-1607.
4. Jiang, X. C., L. Masucci-Magoulas, J. Mar, M. Lin, A. Walsh, J. L. Breslow, and A. Tall. 1993. Down-regulation of mRNA for the low density lipoprotein receptor in transgenic mice containing the gene for human cholesteryl ester transfer protein. Mechanism to explain accumulation of lipoprotein B particles. J. Biol. Chem. 268: 27406-27412.
5. Masson, D., B. Staels, T. Gautier, C. Desrumaux, A. Athias, N. Le Guern, M. Schneider, Z. Zak, L. Dumont, V. Deckert, et al. 2004. Cholesteryl ester transfer protein modulates the effect of liver X receptor agonists on cholesterol transport and excretion in the mouse. J. Lipid Res. 45: 543-550.
6. Lauer, S. J., D. Walker, N. A. Elshourbagy, C. A. Reardon, B. Levy-Wilson, and J. M. Taylor. 1988. Two copies of the human apolipoprotein C-I gene are linked closely to the apolipoprotein E gene. J. Biol. Chem. 263: 7277-7286.
7. Cohn, J. S., R. Batal, M. Tremblay, H. Jacques, L. Veilleux, C. Rodriguez, O. Mamer, and J. Davignon. 2003. Plasma turnover of HDL apoC-I, apoC-III, and apoE in humans: in vivo evidence for a link between HDL apoC-III and apoA-I metabolism. J. Lipid Res. 44: 1976-1983.
8. Windler, E., and R. J. Havel. 1985. 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. 26: 556-565.
9. Kowal, R. C., J. Herz, K. H. Weisgraber, R. W. Mahley, M. S. Brown, and J. L. Goldstein. 1990. Opposing effects of apolipoproteins E and C on lipoprotein binding to low density lipoprotein receptor-related protein. J. Biol. Chem. 265: 10771-10779.
10. Swaney, J. B., and K. H. Weisgraber. 1994. Effect of apolipoprotein C-I peptides on the apolipoprotein E content and receptor-binding properties of beta-migrating very low density lipoproteins. J. Lipid Res. 35: 134-142.
11. Weisgraber, K. H., R. W. Mahley, R. C. Kowal, J. Herz, J. L. Goldstein, and M. S. Brown. 1990. Apolipoprotein C-I modulates the interaction of apolipoprotein E with beta-migrating very low density lipoproteins (beta-VLDL) and inhibits binding of beta-VLDL to low density lipoprotein receptor-related protein. J. Biol. Chem. 265: 22453-22459.
12. Jong, M. C., K. W. van Dijk, V. E. Dahlmans, H. van der Boom, K. Kobayashi, K. Oka, G. Siest, L. Chan, M. H. Hofker, and L. M. Havekes. 1999. Reversal of hyperlipidaemia in apolipoprotein C1 transgenic mice by adenovirus-mediated gene delivery of the low-density-lipoprotein receptor, but not by the very-low-density-lipoprotein receptor. Biochem. J. 338: 281-287.
13. Berbée, J. F., C. C. van der Hoogt, D. Sundararaman, L. M. Havekes, and P. C. Rensen. 2005. Severe hypertriglyceridemia in human APOC1 transgenic mice is caused by apoC-I-induced inhibition of LPL. J. Lipid Res. 46: 297-306.
14. Jong, M. C., M. J. Gijbels, V. E. Dahlmans, P. J. Gorp, S. J. Koopman, M. Ponec, M. H. Hofker, and L. M. Havekes. 1998. Hyperlipidemia and cutaneous abnormalities in transgenic mice overexpressing human apolipoprotein C1. J. Clin. Invest. 101: 145-152.
15. Shachter, N. S., T. Ebara, R. Ramakrishnan, G. Steiner, J. L. Breslow, H. N. Ginsberg, and J. D. Smith. 1996. Combined hyperlipidemia in transgenic mice overexpressing human apolipoprotein Cl. J. Clin. Invest. 98: 846-855.
16. Gautier, T., D. Masson, M. C. Jong, L. Duverneuil, N. Le Guern, V. Deckert, J. P. Pais De Barros, L. Dumont, A. Bataille, Z. Zak, et al. 2002. Apolipoprotein CI deficiency markedly augments plasma lipoprotein changes mediated by human cholesteryl ester transfer protein (CETP) in CETP transgenic/ApoCI-knocked out mice. J. Biol. Chem. 277: 31354-31363.
17. Jong, M. C., J. H. van Ree, V. E. Dahlmans, R. R. Frants, M. H. Hofker, and L. M. Havekes. 1997. Reduced very-low-density lipoprotein fractional catabolic rate in apolipoprotein C1-deficient mice. Biochem. J. 321: 445-450.
18. van Ree, J. H., M. H. Hofker, W. J. van den Broek, J. M. van Deursen, H. van der Boom, R. R. Frants, B. Wieringa, and L. M. Havekes. 1995. Increased response to cholesterol feeding in apolipoprotein C1-deficient mice. Biochem. J. 305: 905-911.
19. Westerterp, M., W. de Haan, J. F. Berbee, L. M. Havekes, and P. C. Rensen. 2006. Endogenous apoC-I increases hyperlipidemia in apoE-knockout mice by stimulating VLDL production and inhibiting LPL. J. Lipid Res. 47: 1203-1211.
20. Jong, M. C., P. J. Voshol, M. Muurling, V. E. Dahlmans, J. A. Romijn, H. Pijl, and L. M. Havekes. 2001. Protection from obesity and insulin resistance in mice overexpressing human apolipoprotein C1. Diabetes. 50: 2779-2785.
21. Koopmans, S. J., M. C. Jong, I. Que, V. E. Dahlmans, H. Pijl, J. K. Radder, M. Frolich, and L. M. Havekes. 2001. Hyperlipidaemia is associated with increased insulin-mediated glucose metabolism, reduced fatty acid metabolism and normal blood pressure in transgenic mice overexpressing human apolipoprotein C1. Diabetologia. 44: 437-443.
22. Jonas, A., S. A. Sweeny, and P. N. Herbert. 1984. Discoidal complexes of A and C apolipoproteins with lipids and their reactions with lecithin:cholesterol acyltransferase. J. Biol. Chem. 259: 6369-6375.
23. Gautier, T., D. Masson, J. P. de Barros, A. Athias, P. Gambert, D. Aunis, M. H. Metz-Boutigue, and L. Lagrost. 2000. Human apolipoprotein C-I accounts for the ability of plasma high density lipoproteins to inhibit the cholesteryl ester transfer protein activity. J. Biol. Chem. 275: 37504-37509.
24. Dietschy, J. M., and S. D. Turley. 2002. Control of cholesterol turnover in the mouse. J. Biol. Chem. 277: 3801-3804.
25. Hogarth, C. A., A. Roy, and D. L. Ebert. 2003. Genomic evidence for the absence of a functional cholesteryl ester transfer protein gene in mice and rats. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 135: 219-229.
26. Jiang, X. C., L. B. Agellon, A. Walsh, J. L. Breslow, and A. Tall. 1992. Dietary cholesterol increases transcription of the human cholesteryl ester transfer protein gene in transgenic mice. Dependence on natural flanking sequences. J. Clin. Invest. 90: 1290-1295.
27. Voshol, P. J., R. Havinga, H. Wolters, R. Ottenhoff, H. M. Princen, R. P. Oude Elferink, A. K. Groen, and F. Kuipers. 1998. Reduced plasma cholesterol and increased fecal sterol loss in multidrug resistance gene 2 P-glycoprotein-deficient mice. Gastroenterology. 114: 1024-1034.
28. Matthews, D. R., J. P. Hosker, A. S. Rudenski, B. A. Naylor, D. F. Treacher, and R. C. Turner. 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 28: 412-419.
29. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
30. Böttcher, C. F. J., C. M. van Gent, and C. Pries. 1961. A rapid and sensitive sub-micro-phosphorus determination. Anal. Chim. Acta. 24: 203-204.
31. Gamble, W., M. Vaughan, H. S. Kruth, and J. Avigan. 1978. Procedure for determination of free and total cholesterol in micro- or nanogram amounts suitable for studies with cultured cells. J. Lipid Res. 19: 1068-1070.
32. Murphy, G. M., B. H. Billing, and D. N. Baron. 1970. A fluorimetric and enzymatic method for the estimation of serum total bile acids. J. Clin. Pathol. 23: 594-598.
33. Setchell, K. D., A. M. Lawson, N. Tanida, and J. Sjovall. 1983. General methods for the analysis of metabolic profiles of bile acids and related compounds in feces. J. Lipid Res. 24: 1085-1100.
34. Bloks, V. W., T. Plosch, H. van Goor, H. Roelofsen, J. Baller, R. Havinga, H. J. Verkade, A. van Tol, P. L. Jansen, and F. Kuipers. 2001. Hyperlipidemia and atherosclerosis associated with liver disease in ferrochelatase-deficient mice. J. Lipid Res. 42: 41-50.
35. Heid, C. A., J. Stevens, K. J. Livak, and P. M. Williams. 1996. Real time quantitative PCR. Genome Res. 6: 986-994.
36. Plosch, T., T. Kok, V. W. Bloks, M. J. Smit, R. Havinga, G. Chimini, A. K. Groen, and F. Kuipers. 2002. Increased hepatobiliary and fecal cholesterol excretion upon activation of the liver X receptor is independent of ABCA1. J. Biol. Chem. 277: 33870-33877.
37. Grefhorst, A., B. M. Elzinga, P. J. Voshol, T. Plosch, T. Kok, V. W. Bloks, F. H. van der Sluijs, L. M. Havekes, J. A. Romijn, H. J. Verkade, et al. 2002. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 277: 34182-34190.
38. Grefhorst, A., J. Hoekstra, T. G. Derks, D. M. Ouwens, J. F. Baller, R. Havinga, L. M. Havekes, J. A. Romijn, and F. Kuipers. 2005. Acute hepatic steatosis in mice by blocking beta-oxidation does not reduce insulin sensitivity of very-low-density lipoprotein production. Am. J. Physiol. Gastrointest. Liver Physiol. 289: G592-G598.
39. Werner, A., R. Havinga, T. Bos, V. W. Bloks, F. Kuipers, and H. J. Verkade. 2005. Essential fatty acid deficiency in mice is associated with hepatic steatosis and secretion of large VLDL particles. Am. J. Physiol. Gastrointest. Liver Physiol. 288: G1150-G1158.
40. Millar, J. S., D. A. Cromley, M. G. McCoy, D. J. Rader, and J. T. Billheimer. 2005. Determining hepatic triglyceride production in mice: comparison of poloxamer 407 with Triton WR-1339. J. Lipid Res. 46: 2023-2028.
41. Plump, A. S., N. Azrolan, H. Odaka, L. Wu, X. Jiang, A. Tall, S. Eisenberg, and J. L. Breslow. 1997. ApoA-I knockout mice: characterization of HDL metabolism in homozygotes and identification of a post-RNA mechanism of apoA-I up-regulation in heterozygotes. J. Lipid Res. 38: 1033-1047.
42. Shimano, H., N. Yamada, M. Katsuki, M. Shimada, T. Gotoda, K. Harada, T. Murase, C. Fukazawa, F. Takaku, and Y. Yazaki. 1992. Overexpression of apolipoprotein E in transgenic mice: marked reduction in plasma lipoproteins except high density lipoprotein and resistance against diet-induced hypercholesterolemia. Proc. Natl. Acad. Sci. USA. 89: 1750-1754.
43. Shimano, H., N. Yamada, M. Katsuki, K. Yamamoto, T. Gotoda, K. Harada, M. Shimada, and Y. Yazaki. 1992. Plasma lipoprotein metabolism in transgenic mice overexpressing apolipoprotein E. Accelerated clearance of lipoproteins containing apolipoprotein B. J. Clin. Invest. 90: 2084-2091.
44. Hofmann, S. L., D. W. Russell, M. S. Brown, J. L. Goldstein, and R. E. Hammer. 1988. Overexpression of low density lipoprotein (LDL) receptor eliminates LDL from plasma in transgenic mice. Science. 239: 1277-1281.
45. Yokode, M., R. E. Hammer, S. Ishibashi, M. S. Brown, and J. L. Goldstein. 1990. Diet-induced hypercholesterolemia in mice: prevention by overexpression of LDL receptors. Science. 250: 1273-1275.
46. Wang, N., T. Arai, Y. Ji, F. Rinninger, and A. R. Tall. 1998. Liverspecific overexpression of scavenger receptor BI decreases levels of very low density lipoprotein ApoB, low density lipoprotein ApoB, and high density lipoprotein in transgenic mice. J. Biol. Chem. 273: 32920-32926.
47. Kuipers, F., J. M. van Ree, M. H. Hofker, H. Wolters, G. In't Veld, R. Havinga, R. J. Vonk, H. M. Princen, and L. M. Havekes. 1996. Altered lipid metabolism in apolipoprotein E-deficient mice does not affect cholesterol balance across the liver. Hepatology. 24: 241-247.
48. Verkade, H. J., R. J. Vonk, and F. Kuipers. 1995. New insights into the mechanism of bile acid-induced biliary lipid secretion. Hepatology. 21: 1174-1189.
49. Kok, T., H. Wolters, V. W. Bloks, R. Havinga, P. L. Jansen, B. Staels, and F. Kuipers. 2003. Induction of hepatic ABC transporter expression is part of the PPARalpha-mediated fasting response in the mouse. Gastroenterology. 124: 160-171.
50. Kok, T., V. W. Bloks, H. Wolters, R. Havinga, P. L. Jansen, B. Staels, and F. Kuipers. 2003. Peroxisome proliferator-activated receptor alpha (PPARalpha)-mediated regulation of multidrug resistance 2 (Mdr2) expression and function in mice. Biochem. J. 369: 539-547.
51. Huang, L., A. Zhao, J. L. Lew, T. Zhang, Y. Hrywna, J. R. Thompson, N. De Pedro, I. Royo, R. A. Blevins, F. Pelaez, et al. 2003. Farnesoid X receptor activates transcription of the phospholipid pump MDR3. J. Biol. Chem. 278: 51085-51090.
52. Liu, Y., J. Binz, M. J. Numerick, S. Dennis, G. Luo, B. Desai, K. I. MacKenzie, T. A. Mansfield, S. A. Kliewer, B. Goodwin, et al. 2003. Hepatoprotection by the farnesoid X receptor agonist GW4064 in rat models of intra- and extrahepatic cholestasis. J. Clin. Invest. 112: 1678-1687.
53. Moschetta, A., A. L. Bookout, and D. J. Mangelsdorf. 2004. Prevention of cholesterol gallstone disease by FXR agonists in a mouse model. Nat. Med. 10: 1352-1358.
54. Windler, E., Y. Chao, and R. J. Havel. 1980. Regulation of the hepatic uptake of triglyceride-rich lipoproteins in the rat. Opposing effects of homologous apolipoprotein E and individual C apoproteins. J. Biol. Chem. 255: 8303-8307.
55. Clavey, V., S. Lestavel-Delattre, C. Copin, J. M. Bard, and J. C. Fruchart. 1995. Modulation of lipoprotein B binding to the LDL receptor by exogenous lipids and apolipoproteins CI, CII, CIII, and E. Arterioscler. Thromb. Vasc. Biol. 15: 963-971.
56. Sehayek, E., and S. Eisenberg. 1991. Mechanisms of inhibition by apolipoprotein C of apolipoprotein E-dependent cellular metabolism of human triglyceride-rich lipoproteins through the low density lipoprotein receptor pathway. J. Biol. Chem. 266: 18259-18267.
57. Conde-Knape, K., A. Bensadoun, J. H. Sobel, J. S. Cohn, and N. S. Shachter. 2002. Overexpression of apoC-I in apoE-null mice: severe hypertriglyceridemia due to inhibition of hepatic lipase. J. Lipid Res. 43: 2136-2145.
58. Shinomiya, M., N. Sasaki, R. L. Barnhart, K. Shirai, and R. L. Jackson. 1982. Effect of apolipoproteins on the hepatic lipase-catalyzed hydrolysis of human plasma high density lipoprotein2-triacylglycerols. Biochim. Biophys. Acta. 713: 292-299.
59. Dichek, H. L., W. Brecht, J. Fan, Z. S. Ji, S. P. McCormick, H. Akeefe, L. Conzo, D. A. Sanan, K. H. Weisgraber, S. G. Young, et al. 1998. Overexpression of hepatic lipase in transgenic mice decreases apolipoprotein B-containing and high density lipoproteins. Evidence that hepatic lipase acts as a ligand for lipoprotein uptake. J. Biol. Chem. 273: 1896-1903.
60. Thuren, T. 2000. Hepatic lipase and HDL metabolism. Curr. Opin. Lipidol. 11: 277-283.
61. Collet, X., A. R. Tall, H. Serajuddin, K. Guendouzi, L. Royer, H. Oliveira, R. Barbaras, X. C. Jiang, and O. L. Francone. 1999. Remodeling of HDL by CETP in vivo and by CETP and hepatic lipase in vitro results in enhanced uptake of HDL CE by cells expressing scavenger receptor B-I. J. Lipid Res. 40: 1185-1193.
62. Gautier, T., D. Masson, M. C. Jong, J. P. Pais De Barros, L. Duverneuil, N. Le Guern, V. Deckert, L. Dumont, A. Bataille, Z. Zak, et al. 2005. Apolipoprotein CI overexpression is not a relevant strategy to block cholesteryl ester transfer protein (CETP) activity in CETP transgenic mice. Biochem. J. 385: 189-195.
63. Gauthier, A., P. Lau, X. Zha, R. Milne, and R. McPherson. 2005. Cholesteryl ester transfer protein directly mediates selective uptake of high density lipoprotein cholesteryl esters by the liver. Arterioscler. Thromb. Vasc. Biol. 25: 2177-2184.