Niemann-pick C1-like 1 deletion in mice prevents high-fat diet-induced fatty liver by reducing lipogenesis

Journal of Lipid Research

Volumn 51, Issue 11, 2010, Pages 3135-3144

  Jia, Lin ^a   Ma, Yinyan ^a   Rong, Shunxing ^a   Betters, Jenna L ^a   Xie, Ping ^a   Chung, Soonkyu ^a   Wang, Nanping ^a   Tang, Weiqing ^a   Yu, Liqing ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Ezetimibe; Insulin resistance; Intestinal cholesterol absorption; Nonalcoholic fatty liver disease; Obesity

Indexed keywords

LIPOPROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; NIEMANN PICK C1 LIKE 1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DIET RESTRICTION; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FATTY LIVER; GENE DELETION; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HYPERINSULINEMIA; INSULIN SENSITIVITY; KNOCKOUT MOUSE; LIPID DIET; LIPID HYDROLYSIS; LIPOGENESIS; LIVER LEVEL; LIVER METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; WILD TYPE;

ANIMALS; CHOLESTEROL; DIETARY FATS; FATTY ACIDS; FATTY LIVER; GENE DELETION; GENE KNOCKOUT TECHNIQUES; INSULIN RESISTANCE; LIPOGENESIS; LIVER; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; OBESITY; OXIDATIVE STRESS;

EID: 78149348442     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M006353     Document Type: Article

References (52)

1. Davies, J. P., B. Levy, and Y. A. Ioannou. 2000. Evidence for a Niemann-pick C (NPC) gene family: identification and characterization of NPC1L1. Genomics. 65: 137-145.
2. Altmann, S. W., H. R. Davis, Jr., L. J. Zhu, X. Yao, L. M. Hoos, G. Tetzloff, S. P. Iyer, M. Maguire, A. Golovko, M. Zeng, et al. 2004. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science. 303: 1201-1204.
3. Davies, J. P., C. Scott, K. Oishi, A. Liapis, and Y. A. Ioannou. 2005. Inactivation of NPC1L1 causes multiple lipid transport defects and protects against diet-induced hypercholesterolemia. J. Biol. Chem. 280: 12710-12720.
4. Temel, R. E., W. Tang, Y. Ma, L. L. Rudel, M. C. Willingham, Y. A. Ioannou, J. P. Davies, L. M. Nilsson, and L. Yu. 2007. Hepatic Niemann-Pick C1-like 1 regulates biliary cholesterol concentration and is a target of ezetimibe. J. Clin. Invest. 117: 1968-1978.
5. Davis, H. R., Jr., L. J. Zhu, L. M. Hoos, G. Tetzloff, M. Maguire, J. Liu, X. Yao, S. P. Iyer, M. H. Lam, E. G. Lund, et al. 2004. Niemann-Pick C1 Like 1 (NPC1L1) is the intestinal phytosterol and cholesterol transporter and a key modulator of whole-body cholesterol homeostasis. J. Biol. Chem. 279: 33586-33592.
6. Davis, H. R., Jr., L. M. Hoos, G. Tetzloff, M. Maguire, L. J. Zhu, M. P. Graziano, and S. W. Altmann. 2007. Deficiency of Niemann-Pick C1 Like 1 prevents atherosclerosis in ApoE -/- mice. Arterioscler. Thromb. Vasc. Biol. 27: 841-849.
7. Garcia-Calvo, M., J. Lisnock, H. G. Bull, B. E. Hawes, D. A. Burnett, M. P. Braun, J. H. Crona, H. R. Davis, Jr., D. C. Dean, P. A. Detmers, et al. 2005. The target of ezetimibe is Niemann-Pick C1-Like 1 (NPC1L1). Proc. Natl. Acad. Sci. USA. 102: 8132-8137.
8. Weinglass, A. B., M. Kohler, U. Schulte, J. Liu, E. O. Nketiah, A. Thomas, W. Schmalhofer, B. Williams, W. Bildl, D. R. McMasters, et al. 2008. Extracellular loop C of NPC1L1 is important for binding to ezetimibe. Proc. Natl. Acad. Sci. USA. 105: 11140-11145.
9. Davis, H. R., and E. P. Veltri. 2007. Zetia: inhibition of Niemann-Pick C1 Like 1 (NPC1L1) to reduce intestinal cholesterol absorption and treat hyperlipidemia. J. Atheroscler. Thromb. 14: 99-108.
10. Chan, D. C., G. F. Watts, S. K. Gan, E. M. Ooi, and P. H. Barrett. 2010. Effect of ezetimibe on hepatic fat, inflammatory markers, and apolipoprotein B-100 kinetics in insulin-resistant obese subjects on a weight loss diet. Diabetes Care. 33: 1134-1139.
11. Yagi, S., M. Akaike, K. Aihara, T. Iwase, K. Ishikawa, S. Yoshida, Y. Sumitomo-Ueda, K. Kusunose, T. Niki, K. Yamaguchi, et al. 2010. Ezetimibe ameliorates metabolic disorders and microalbuminuria in patients with hypercholesterolemia. J. Atheroscler. Thromb. 17: 173-180.
12. Deushi, M., M. Nomura, A. Kawakami, M. Haraguchi, M. Ito, M. Okazaki, H. Ishii, and M. Yoshida. 2007. Ezetimibe improves liver steatosis and insulin resistance in obese rat model of metabolic syndrome. FEBS Lett. 581: 5664-5670. (Pubitemid 350179776)
13. Nomura, M., H. Ishii, A. Kawakami, and M. Yoshida. 2009. Inhibition of hepatic Neiman-Pick C1-Like 1 improves hepatic insulin resistance. Am. J. Physiol. Endocrinol. Metab. Epub ahead of print. August 4, 2009.
14. Assy, N., M. Grozovski, I. Bersudsky, S. Szvalb, and O. Hussein. 2006. Effect of insulin-sensitizing agents in combination with ezetimibe, and valsartan in rats with non-alcoholic fatty liver disease. World J. Gastroenterol. 12: 4369-4376.
15. Zheng, S., L. Hoos, J. Cook, G. Tetzloff, H. Davis, Jr., M. van Heek, and J. J. Hwa. 2008. Ezetimibe improves high fat and cholesterol diet-induced non-alcoholic fatty liver disease in mice. Eur. J. Pharmacol. 584: 118-124.
16. Labonte, E. D., L. M. Camarota, J. C. Rojas, R. J. Jandacek, D. E. Gilham, J. P. Davies, Y. A. Ioannou, P. Tso, D. Y. Hui, and P. N. Howles. 2008. Reduced absorption of saturated fatty acids and resistance to diet-induced obesity and diabetes by ezetimibe-treated and Npc1l1 -/- mice. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G776-G783.
17. Browning, J. D., and J. D. Horton. 2004. Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114: 147-152.
18. Clark, J. M. 2006. The epidemiology of nonalcoholic fatty liver disease in adults. J. Clin. Gastroenterol. 40 ( Suppl 1 ): S5-S10.
19. Browning, J. D., L. S. Szczepaniak, R. Dobbins, P. Nuremberg, J. D. Horton, J. C. Cohen, S. M. Grundy, and H. H. Hobbs. 2004. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 40: 1387-1395.
20. Janowski, B. A., P. J. Willy, T. R. Devi, J. R. Falck, and D. J. Mangelsdorf. 1996. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature. 383: 728-731.
21. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
22. Tang, W., Y. Ma, L. Jia, Y. A. Ioannou, J. P. Davies, and L. Yu. 2008. Niemann-Pick C1-Like 1 is required for an LXR agonist to raise plasma HDL cholesterol in mice. Arterioscler. Thromb. Vasc. Biol. 28: 448-454.
23. Chen, G., G. Liang, J. Ou, J. L. Goldstein, and M. S. Brown. 2004. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc. Natl. Acad. Sci. USA. 101: 11245-11250.
24. Horton, J. D., J. L. Goldstein, and M. S. Brown. 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109: 1125-1131.
25. Brown, M. S., and J. L. Goldstein. 2008. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 7: 95-96.
26. Shulman, G. I. 2000. Cellular mechanisms of insulin resistance. J. Clin. Invest. 106: 171-176.
27. Biddinger, S. B., K. Almind, M. Miyazaki, E. Kokkotou, J. M. Ntambi, and C. R. Kahn. 2005. Effects of diet and genetic background on sterol regulatory element-binding protein-1c, stearoyl-CoA desaturase 1, and the development of the metabolic syndrome. Diabetes. 54: 1314-1323.
28. Tang, W., Y. Ma, L. Jia, Y. A. Ioannou, J. P. Davies, and L. Yu. 2009. Genetic inactivation of NPC1L1 protects against sitosterolemia in mice lacking ABCG5/ABCG8. J. Lipid Res. 50: 293-300.
29. Jandacek, R. J., J. E. Heubi, and P. Tso. 2004. A novel, noninvasive method for the measurement of intestinal fat absorption. Gastroenterology. 127: 139-144.
30. Mulvihill, E. E., E. M. Allister, B. G. Sutherland, D. E. Telford, C. G. Sawyez, J. Y. Edwards, J. M. Markle, R. A. Hegele, and M. W. Huff. 2009. Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes. 58: 2198-2210.
31. Linden, D., L. William-Olsson, A. Ahnmark, K. Ekroos, C. Hallberg, H. P. Sjogren, B. Becker, L. Svensson, J. C. Clapham, J. Oscarsson, et al. 2006. Liver-directed overexpression of mitochondrial glycerol-3-phosphate acyltransferase results in hepatic steatosis, increased triacylglycerol secretion and reduced fatty acid oxidation. FASEB J. 20: 434-443.
32. 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.
33. Schweiger, M., G. Schoiswohl, A. Lass, F. P. Radner, G. Haemmerle, R. Malli, W. Graier, I. Cornaciu, M. Oberer, R. Salvayre, et al. 2008. The C-terminal region of human adipose triglyceride lipase affects enzyme activity and lipid droplet binding. J. Biol. Chem. 283: 17211-17220.
34. Radner, F. P., I. E. Streith, G. Schoiswohl, M. Schweiger, M. Kumari, T. O. Eichmann, G. Rechberger, H. C. Koefeler, S. Eder, S. Schauer, et al. 2010. Growth retardation, impaired triacylglycerol catabolism, hepatic steatosis, and lethal skin barrier defect in mice lacking comparative gene identification-58 (CGI-58). J. Biol. Chem. 285: 7300-7311.
35. Norris, A. W., L. Chen, S. J. Fisher, I. Szanto, M. Ristow, A. C. Jozsi, M. F. Hirshman, E. D. Rosen, L. J. Goodyear, F. J. Gonzalez, et al. 2003. Muscle-specific PPARgamma-deficient mice develop increased adiposity and insulin resistance but respond to thiazolidinediones. J. Clin. Invest. 112: 608-618.
36. Yang, J., J. L. Goldstein, R. E. Hammer, Y. A. Moon, M. S. Brown, and J. D. Horton. 2001. Decreased lipid synthesis in livers of mice with disrupted Site-1 protease gene. Proc. Natl. Acad. Sci. USA. 98: 13607-13612.
37. Kruit, J. K., T. Plosch, R. Havinga, R. Boverhof, P. H. Groot, A. K. Groen, and F. Kuipers. 2005. Increased fecal neutral sterol loss upon liver X receptor activation is independent of biliary sterol secretion in mice. Gastroenterology. 128: 147-156.
38. van der Velde, A. E., C. L. Vrins, K. van den Oever, C. Kunne, R. P. Oude Elferink, F. Kuipers, and A. K. Groen. 2007. Direct intestinal cholesterol secretion contributes significantly to total fecal neutral sterol excretion in mice. Gastroenterology. 133: 967-975.
39. Xue, B., Y. B. Kim, A. Lee, E. Toschi, S. Bonner-Weir, C. R. Kahn, B. G. Neel, and B. B. Kahn. 2007. Protein-tyrosine phosphatase 1B deficiency reduces insulin resistance and the diabetic phenotype in mice with polygenic insulin resistance. J. Biol. Chem. 282: 23829-23840.
40. Iynedjian, P. B., A. Gjinovci, and A. E. Renold. 1988. Stimulation by insulin of glucokinase gene transcription in liver of diabetic rats. J. Biol. Chem. 263: 740-744.
41. Magnuson, M. A., T. L. Andreone, R. L. Printz, S. Koch, and D. K. Granner. 1989. Rat glucokinase gene: structure and regulation by insulin. Proc. Natl. Acad. Sci. USA. 86: 4838-4842.
42. Uyeda, K., and J. J. Repa. 2006. Carbohydrate response element binding protein, ChREBP, a transcription factor coupling hepatic glucose utilization and lipid synthesis. Cell Metab. 4: 107-110.
43. Dentin, R., J. P. Pegorier, F. Benhamed, F. Foufelle, P. Ferre, V. Fauveau, M. A. Magnuson, J. Girard, and C. Postic. 2004. Hepatic glucokinase is required for the synergistic action of ChREBP and SREBP-1c on glycolytic and lipogenic gene expression. J. Biol. Chem. 279: 20314-20326.
44. Ogawa, T., H. Fujii, K. Yoshizato, and N. Kawada. 2010. A human-type nonalcoholic steatohepatitis model with advanced fibrosis in rabbits. Am. J. Pathol. 177: 153-165.
45. Horvath, E. M., L. Tackett, and J. S. Elmendorf. 2008. A novel membrane-based anti-diabetic action of atorvastatin. Biochem. Biophys. Res. Commun. 372: 639-643.
46. Liu, P., B. J. Leffler, L. K. Weeks, G. Chen, C. M. Bouchard, A. B. Strawbridge, and J. S. Elmendorf. 2004. Sphingomyelinase activates GLUT4 translocation via a cholesterol-dependent mechanism. Am. J. Physiol. Cell Physiol. 286: C317-C329.
47. Guclu, F., B. Ozmen, Z. Hekimsoy, and C. Kirmaz. 2004. Effects of a statin group drug, pravastatin, on the insulin resistance in patients with metabolic syndrome. Biomed. Pharmacother. 58: 614-618.
48. Huptas, S., H. C. Geiss, C. Otto, and K. G. Parhofer. 2006. Effect of atorvastatin (10 mg/day) on glucose metabolism in patients with the metabolic syndrome. Am. J. Cardiol. 98: 66-69.
49. Jia, L., Y. Ma, G. Liu, and L. Yu. 2010. Dietary cholesterol reverses resistance to diet-induced weight gain in mice lacking Niemann-Pick C1-Like 1. J. Lipid Res. Epub ahead of print. July 2, 2010; doi: 10.1194/jlr.M008599.
50. Kalaany, N. Y., K. C. Gauthier, A. M. Zavacki, P. P. Mammen, T. Kitazume, J. A. Peterson, J. D. Horton, D. J. Garry, A. C. Bianco, and D. J. Mangelsdorf. 2005. LXRs regulate the balance between fat storage and oxidation. Cell Metab. 1: 231-244.
51. Repa, J. J., G. Liang, J. Ou, Y. Bashmakov, J. M. Lobaccaro, I. Shimomura, B. Shan, M. S. Brown, J. L. Goldstein, and D. J. Mangelsdorf. 2000. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14: 2819-2830.
52. Donnelly, K. L., C. I. Smith, S. J. Schwarzenberg, J. Jessurun, M. D. Boldt, and E. J. Parks. 2005. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J. Clin. Invest. 115: 1343-1351.