Hepatocyte-specifi c IKK- β activation enhances VLDL-triglyceride production in APOE*3-Leiden mice

Journal of Lipid Research

Volumn 52, Issue 5, 2011, Pages 942-950

  Diepen, Janna A Van ^a   Wong, Man C ^b   Guigas, Bruno ^c   Bos, Jasper ^a   Stienstra, Rinke ^e   Hodson, Leanne ^f   Shoelson, Steven E ^g   Jimmy F P Berbee ^a   Rensen, Patrick C N ^a   Romijn, Johannes A ^a   Havekes, Louis M ^a,d,h   Voshol, Peter J ^a,i  

^a Departments of General Internal Medicine Endocrinology and Metabolic Diseases   (Netherlands)

^b Departments of Pulmonology   (Netherlands)

^c Departments of Molecular Cell Biology   (Netherlands)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g HARVARD MEDICAL SCHOOL   (United States)

^h TNO   (Netherlands)

ⁱ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

I k B kinase ; Lipid metabolism; Liver; Nuclear factor kappa B; Very low density lipoprotein

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER G5; ABC TRANSPORTER G8; APOLIPOPROTEIN B; APOLIPOPROTEIN E3; BINDING PROTEIN; CARBOHYDRATE RESPONSIVE ELEMENT BINDING PROTEIN; CARNITINE PALMITOYLTRANSFERASE I; CHOLESTANETRIOL 26 MONOOXYGENASE; CHOLESTEROL 7ALPHA MONOOXYGENASE; CYTOCHROME P450; CYTOCHROME P450 8B1; DIACYLGLYCEROL ACYLTRANSFERASE; FARNESOID X RECEPTOR; FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; I KAPPA B KINASE BETA; LIPID; LIVER X RECEPTOR ALPHA; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; PERILIPIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PYRUVATE KINASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; APOLIPOPROTEIN E; I KAPPA B KINASE; VERY LOW DENSITY LIPOPROTEIN TRIGLYCERIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR RISK; CONTROLLED STUDY; ENZYME ACTIVATION; FATTY ACID OXIDATION; GENE EXPRESSION PROFILING; HYPERLIPIDEMIA; HYPERTRIGLYCERIDEMIA; IN VITRO STUDY; IN VIVO STUDY; LIPID ANALYSIS; LIPID METABOLISM; LIPOGENESIS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; ANIMAL; BIOSYNTHESIS; CELL CULTURE; GENETICS; HUMAN; LIVER; MALE; METABOLISM; WESTERN BLOTTING;

ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEINS E; BLOTTING, WESTERN; CELLS, CULTURED; HEPATOCYTES; HUMANS; HYPERTRIGLYCERIDEMIA; I-KAPPA B KINASE; LIPOPROTEINS, VLDL; LIVER; MALE; MICE; TRIGLYCERIDES;

EID: 79955037346     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M010405     Document Type: Article

References (38)

1. Cai, D., M. Yuan, D. F. Frantz, P. A. Melendez, L. Hansen, J. Lee, and S. E. Shoelson. 2005. Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat. Med. 11 : 183-190. (Pubitemid 40321354)
2. Arkan, M. C., A. L. Hevener, F. R. Greten, S. Maeda, Z. W. Li, J. M. Long, A. Wynshaw-Boris, G. Poli, J. Olefsky, and M. Karin. 2005. IKK-beta links infl ammation to obesity-induced insulin resistance. Nat. Med. 11 : 191-198. (Pubitemid 40321355)
3. Feingold, K. R., M. Soued, S. Adi, I. Staprans, J. Shigenaga, W. Doerrler, A. Moser, and C. Grunfeld. 1990. Tumor necrosis factor-increased hepatic very-low-density lipoprotein production and increased serum triglyceride levels in diabetic rats. Diabetes. 39 : 1569-1574.
4. Goldfi ne, A. B., R. Silver, W. Aldhahi, D. Cai, E. Tatro, J. Lee, and S. E. Shoelson. 2008. Use of salsalate to target infl ammation in the treatment of insulin resistance and type 2 diabetes. Clin. Transl. Sci. 1 : 36-43.
5. Feingold, K. R., I. Staprans, R. A. Memon, A. H. Moser, J. K. Shigenaga, W. Doerrler, C. A. Dinarello, and C. Grunfeld. 1992. Endotoxin rapidly induces changes in lipid metabolism that produce hypertriglyceridemia: Low doses stimulate hepatic triglyceride production while high doses inhibit clearance. J. Lipid Res. 33 : 1765-1776. (Pubitemid 23006653)
6. van den Maagdenberg, A. M., M. H. Hofker, P. J. Krimpenfort, I. de Bruijn, B. J. van Vlijmen, H. van der Boom, L. M. Havekes, and R. R. Frants. 1993. Transgenic mice carrying the apolipoprotein E3-Leiden gene exhibit hyperlipoproteinemia. J. Biol. Chem. 268 : 10540-10545. (Pubitemid 23150242)
7. Zadelaar, S., R. Kleemann, L. Verschuren, J. de Vries-van der Weij, J. van der Hoorn, H. M. Princen, and T. Kooistra. 2007. Mouse models for atherosclerosis and pharmaceutical modifi ers. Arterioscler. Thromb. Vasc. Biol. 27 : 1706-1721. (Pubitemid 47207165)
8. Zambon, A., S. I. Hashimoto, and J. D. Brunzell. 1993. Analysis of techniques to obtain plasma for measurement of levels of free fatty acids. J. Lipid Res. 34 : 1021-1028. (Pubitemid 23182699)
9. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purifi cation. Can. J. Biochem. Physiol. 37 : 911-917.
10. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purifi cation of total lipides from animal tissues. J. Biol. Chem. 226 : 497-509.
11. Rensen, P. C., M. C. van Dijk, E. C. Havenaar, M. K. Bijsterbosch, J. K. Kruijt, and T. J. van Berkel. 1995. Selective liver targeting of antivirals by recombinant chylomicrons-a new therapeutic approach to hepatitis B. Nat. Med. 1 : 221-225.
12. Rensen, P. C., N. Herijgers, M. H. Netscher, S. C. Meskers, M. van Eck, and T. J. van Berkel. 1997. Particle size determines the specifi city of apolipoprotein E-containing triglyceride-rich emulsions for the LDL receptor versus hepatic remnant receptor in vivo. J. Lipid Res. 38 : 1070-1084. (Pubitemid 27281803)
13. Jong, M. C., P. C. Rensen, V. E. Dahlmans, H. van der Boom, T. J. van Berkel, and L. M. Havekes. 2001. Apolipoprotein C-III defi ciency accelerates triglyceride hydrolysis by lipoprotein lipase in wild-type and apoE knockout mice. J. Lipid Res. 42 : 1578-1585. (Pubitemid 33026056)
14. Redgrave, T. G., D. C. Roberts, and C. E. West. 1975. Separation of plasma lipoproteins by density-gradient ultracentrifugation. Anal. Biochem. 65 : 42-49.
15. Berry, M. N., and D. S. Friend. 1969. High-yield preparation of isolated rat liver parenchymal cells: A biochemical and fi ne structural study. J. Cell Biol. 43 : 506-520.
16. Groen, A. K., C. W. van Roermund, R. C. Vervoorn, and J. M. Tager. 1986. Control of gluconeogenesis in rat liver cells. Flux control coeffi cients of the enzymes in the gluconeogenic pathway in the absence and presence of glucagon. Biochem. J. 237 : 379-389. (Pubitemid 16043695)
17. Kuipers, F., M. C. Jong, Y. Lin, M. Eck, R. Havinga, V. Bloks, H. J. Verkade, M. H. Hofker, H. Moshage, T. J. Berkel, et al. 1997. Impaired secretion of very low density lipoprotein-triglycerides by apolipoprotein E- defi cient mouse hepatocytes. J. Clin. Invest. 100 : 2915-2922. (Pubitemid 28007563)
18. Powell, E. E., J. R. Jonsson, and A. D. Clouston. 2005. Steatosis: Cofactor in other liver diseases. Hepatology. 42 : 5-13. (Pubitemid 40911303)
19. Khovidhunkit, W., M. S. Kim, R. A. Memon, J. K. Shigenaga, A. H. Moser, K. R. Feingold, and C. Grunfeld. 2004. Effects of infection and infl ammation on lipid and lipoprotein metabolism: Mechanisms and consequences to the host. J. Lipid Res. 45 : 1169-1196. (Pubitemid 38802622)
20. Hotamisligil, G. S. 2006. Infl ammation and metabolic disorders. Nature. 444 : 860-867.
21. Rensen, P. C., M. Oosten, E. Bilt, M. Eck, J. Kuiper, and T. J. Berkel. 1997. Human recombinant apolipoprotein E redirects lipopolysaccharide from Kupffer cells to liver parenchymal cells in rats in vivo. J. Clin. Invest. 99 : 2438-2445. (Pubitemid 27227722)
22. Nonogaki, K., G. M. Fuller, N. L. Fuentes, A. H. Moser, I. Staprans, C. Grunfeld, and K. R. Feingold. 1995. Interleukin-6 stimulates hepatic triglyceride secretion in rats. Endocrinology. 136 : 2143-2149.
23. Tsai, J., R. Zhang, W. Qiu, Q. Su, M. Naples, and K. Adeli. 2009. Infl ammatory NF-kappaB activation promotes hepatic apolipoprotein B100 secretion: Evidence for a link between hepatic infl ammation and lipoprotein production. Am. J. Physiol. Gastrointest. Liver Physiol. 296 : G1287-G1298.
24. Lewis, G. F., and G. Steiner. 1996. Acute effects of insulin in the control of VLDL production in humans. Implications for the insulin- resistant state. Diabetes Care. 19 : 390-393. (Pubitemid 26115468)
25. Huang, W., A. Metlakunta, N. Dedousis, P. Zhang, I. Sipula, J. J. Dube, D. K. Scott, and R. M. O'Doherty. 2010. Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance. Diabetes. 59 : 347-357.
26. Stienstra, R., F. Saudale, C. Duval, S. Keshtkar, J. E. Groener, N. van Rooijen, B. Staels, S. Kersten, and M. Muller. 2010. Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity. Hepatology. 51 : 511-522.
27. Glass, C. K., and S. Ogawa. 2006. Combinatorial roles of nuclear receptors in infl ammation and immunity. Nat. Rev. Immunol. 6 : 44-55. (Pubitemid 43279752)
28. Stienstra, R., S. Mandard, N. S. Tan, W. Wahli, C. Trautwein, T. A. Richardson, E. Lichtenauer-Kaligis, S. Kersten, and M. Muller. 2007. The Interleukin-1 receptor antagonist is a direct target gene of PPARalpha in liver. J. Hepatol. 46 : 869-877. (Pubitemid 46529035)
29. Watanabe, M., S. M. Houten, L. Wang, A. Moschetta, D. J. Mangelsdorf, R. A. Heyman, D. D. Moore, and J. Auwerx. 2004. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c. J. Clin. Invest. 113 : 1408-1418. (Pubitemid 39071696)
30. Feingold, K. R., M. Soued, M. K. Serio, A. H. Moser, C. A. Dinarello, and C. Grunfeld. 1989. Multiple cytokines stimulate hepatic lipid synthesis in vivo. Endocrinology. 125 : 267-274. (Pubitemid 19182669)
31. Grunfeld, C., J. A. Verdier, R. Neese, A. H. Moser, and K. R. Feingold. 1988. Mechanisms by which tumor necrosis factor stimulates hepatic fatty acid synthesis in vivo. J. Lipid Res. 29 : 1327-1335. (Pubitemid 18261055)
32. Joseph, S. B., B. A. Laffi tte, P. H. Patel, M. A. Watson, K. E. Matsukuma, R. Walczak, J. L. Collins, T. F. Osborne, and P. Tontonoz. 2002. Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors. J. Biol. Chem. 277 : 11019-11025. (Pubitemid 34952859)
33. Iizuka, K., R. K. Bruick, G. Liang, J. D. Horton, and K. Uyeda. 2004. Defi ciency of carbohydrate response element-binding protein (ChREBP) reduces lipogenesis as well as glycolysis. Proc. Natl. Acad. Sci. USA. 101 : 7281-7286. (Pubitemid 38638024)
34. Kawaguchi, T., M. Takenoshita, T. Kabashima, and K. Uyeda. 2001. Glucose and cAMP regulate the L-type pyruvate kinase gene by phosphorylation/ dephosphorylation of the carbohydrate response element binding protein. Proc. Natl. Acad. Sci. USA. 98 : 13710-13715. (Pubitemid 33115963)
35. Yamashita, H., M. Takenoshita, M. Sakurai, R. K. Bruick, W. J. Henzel, W. Shillinglaw, D. Arnot, and K. Uyeda. 2001. A glucoseresponsive transcription factor that regulates carbohydrate metabolism in the liver. Proc. Natl. Acad. Sci. USA. 98 : 9116-9121. (Pubitemid 32743878)
36. Morral, N., H. J. Edenberg, S. R. Witting, J. Altomonte, T. Chu, and M. Brown. 2007. Effects of glucose metabolism on the regulation of genes of fatty acid synthesis and triglyceride secretion in the liver. J. Lipid Res. 48 : 1499-1510. (Pubitemid 47312012)
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. Chakravarthy, M. V., Z. Pan, Y. Zhu, K. Tordjman, J. G. Schneider, T. Coleman, J. Turk, and C. F. Semenkovich. 2005. "New" hepatic fat activates PPARalpha to maintain glucose, lipid, and cholesterol homeostasis. Cell Metab. 1 : 309-322. (Pubitemid 43977168)