Inhibiting monoacylglycerol acyltransferase 1 ameliorates hepatic metabolic abnormalities but not inflammation and injury in mice

Journal of Biological Chemistry

Volumn 289, Issue 43, 2014, Pages 30177-30188

  Soufi, Nisreen ^a   Hall, Angela M ^a   Chen, Zhouji ^a   Yoshino, Jun ^a   Collier, Sara L ^a   Mathews, James C ^a   Brunt, Elizabeth M ^a   Albert, Carolyn J ^b   Graham, Mark J ^c   Ford, David A ^b   Finck, Brian N ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; MONOACYLGLYCEROL;

ACYLGLYCEROL PALMITOYLTRANSFERASE; ANTISENSE OLIGONUCLEOTIDE; CHOLESTEROL; DIACYLGLYCEROL; FATTY ACID; FRUCTOSE; MONOACYLGLYCEROL ACYLTRANSFERASE 1; TRANS FATTY ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; 1,2-DIACYLGLYCEROL; ACYLTRANSFERASE; BIOLOGICAL MARKER; GLUCOSE; MGAT1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE DIET; CELL ACTIVATION; CELL INFILTRATION; CHOLESTEROL DIET; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INHIBITION; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE SILENCING; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HEPATITIS; INSULIN SIGNALING; LIPID DIET; LIPID LIVER LEVEL; LIVER INJURY; LIVER METABOLISM; MACROPHAGE INFILTRATION; MALE; MOGAT1 GENE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; SIGNAL TRANSDUCTION; STELLATE CELL; WEIGHT GAIN; ADIPOSE TISSUE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DIET; DRUG EFFECTS; ENZYMOLOGY; FATTY LIVER; GENETICS; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; INFLAMMATION; LEUKOCYTE; LIPOGENESIS; LIVER; METABOLISM; MOUSE MUTANT; OBESITY; OXIDATION REDUCTION REACTION; PATHOLOGY;

ACYLTRANSFERASES; ADIPOSE TISSUE; ADIPOSITY; ANIMALS; BIOMARKERS; DIET; DIGLYCERIDES; FATTY ACIDS; FATTY LIVER; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GLUCOSE; GLUCOSE TOLERANCE TEST; HEPATIC STELLATE CELLS; HOMEOSTASIS; INFLAMMATION; LEUKOCYTES; LIPOGENESIS; LIVER; MALE; MICE, INBRED C57BL; MICE, OBESE; OLIGONUCLEOTIDES, ANTISENSE; OXIDATION-REDUCTION; TRIGLYCERIDES; WEIGHT GAIN;

EID: 84908191987     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.595850     Document Type: Article

References (45)

1. Vernon, G., Baranova, A., and Younossi, Z. M. (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment. Pharmacol. Ther. 34, 274-285
2. Fan, J. G., and Cao, H. X. (2013) Role of diet and nutritional management in non-alcoholic fatty liver disease. J. Gastroenterol. Hepatol. 28, 81-87
3. Sookoian, S., and Pirola, C. J. (2011) Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology 53, 1883-1894
4. Zhu, L., Baker, S. S., Gill, C., Liu, W., Alkhouri, R., Baker, R. D., and Gill, S. R. (2013) Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 57, 601-609
5. Yue, Y. G., Chen, Y. Q., Zhang, Y., Wang, H., Qian, Y. W., Arnold, J. S., Calley, J. N., Li, S. D., Perry, W. L., 3rd, Zhang, H. Y., Konrad, R. J., and Cao, G. (2011) The acyl coenzyme A:monoacylglycerol acyltransferase 3 (MGAT3) gene is a pseudogene in mice but encodes a functional enzyme in rats. Lipids 46, 513-520
6. Cao, J., Cheng, L., and Shi, Y. (2007) Catalytic properties of MGAT3, a putative triacylgycerol synthase. J. Lipid Res. 48, 583-591
7. Shi, Y., and Cheng, D. (2009) Beyond triglyceride synthesis: the dynamic functional roles of MGAT and DGAT enzymes in energy metabolism. Am. J. Physiol. Endocrinol. Metab. 297, E10-E18
8. Xia, T., Mostafa, N., Bhat, B. G., Florant, G. L., and Coleman, R. A. (1993) Selective retention of essential fatty acids: the role of hepatic monoacylglycerol acyltransferase. Am. J. Physiol. 265, R414-R419
9. Bhat, B. G., Wang, P., and Coleman, R. A. (1994) Hepatic monoacylglycerol acyltransferase is regulated by sn-1,2-diacylglycerol and by specific lipids in Triton X-100/phospholipid-mixed micelles. J. Biol. Chem. 269, 13172-13178
10. Hall, A. M., Kou, K., Chen, Z., Pietka, T. A., Kumar, M., Korenblat, K. M., Lee, K., Ahn, K., Fabbrini, E., Klein, S., Goodwin, B., and Finck, B. N. (2012) Evidence for regulated monoacylglycerol acyltransferase expression and activity in human liver. J. Lipid Res. 53, 990-999
11. Cortés, V. A., Curtis, D. E., Sukumaran, S., Shao, X., Parameswara, V., Rashid, S., Smith, A. R., Ren, J., Esser, V., Hammer, R. E., Agarwal, A. K., Horton, J. D., and Garg, A. (2009) Molecular mechanisms of hepatic steatosis and insulin resistance in the AGPAT2-deficient mouse model of congenital generalized lipodystrophy. Cell Metab. 9, 165-176
12. Lee, Y. J., Ko, E. H., Kim, J. E., Kim, E., Lee, H., Choi, H., Yu, J. H., Kim, H. J., Seong, J. K., Kim, K. S., and Kim, J. W. (2012) Nuclear receptor PPARγ-regulated monoacylglycerol O-acyltransferase 1 (MGAT1) expression is responsible for the lipid accumulation in diet-induced hepatic steatosis. Proc. Natl. Acad. Sci. U.S.A. 109, 13656-13661
13. Hall, A. M., Soufi, N., Chambers, K. T., Chen, Z., Schweitzer, G. G., Mc-Commis, K. S., Erion, D. M., Graham, M. J., Su, X., and Finck, B. N. (2014) Abrogating monoacylglycerol acyltransferase activity in liver improves glucose tolerance and hepatic insulin signaling in obese mice. Diabetes 63, 2284-2296
14. Clapper, J. R., Hendricks, M. D., Gu, G., Wittmer, C., Dolman, C. S., Herich, J., Athanacio, J., Villescaz, C., Ghosh, S. S., Heilig, J. S., Lowe, C., and Roth, J. D. (2013) Diet-induced mouse model of fatty liver disease and nonalcoholic steatohepatitis reflecting clinical disease progression and methods of assessment. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G483-G495
15. Trevaskis, J. L., Griffin, P. S., Wittmer, C., Neuschwander-Tetri, B. A., Brunt, E. M., Dolman, C. S., Erickson, M. R., Napora, J., Parkes, D. G., and Roth, J. D. (2012) Glucagon-like peptide-1 receptor agonism improves metabolic, biochemical, and histopathological indices of nonalcoholic steatohepatitis in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G762-G772
16. Chen, Z., Gropler, M. C., Norris, J., Lawrence, J. C., Jr., Harris, T. E., and Finck, B. N. (2008) Alterations in hepatic metabolism in fld mice reveal a role for lipin 1 in regulating VLDL-triacylglyceride secretion. Arterioscler. Thromb. Vasc. Biol. 28, 1738-1744
17. Burgess, S. C., Leone, T. C., Wende, A. R., Croce, M. A., Chen, Z., Sherry, A. D., Malloy, C. R., and Finck, B. N. (2006) Diminished hepatic gluconeogenesis via defects in tricarboxylic acid cycle flux in peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α)-deficient mice. J. Biol. Chem. 281, 19000-19008
18. Lin, X., Schonfeld, G., Yue, P., and Chen, Z. (2002) Hepatic fatty acid synthesis is suppressed in mice with fatty livers due to targeted apolipoprotein B38.9 mutation. Arterioscler. Thromb. Vasc. Biol. 22, 476-482
19. Chen, Z., Norris, J. Y., and Finck, B. N. (2010) Peroxisome proliferatoractivated receptor-γ coactivator-1α (PGC-1α) stimulates VLDL assembly through activation of cell death-inducing DFFA-like effector B (CideB). J. Biol. Chem. 285, 25996-26004
20. Kim, S. Y., and Volsky, D. J. (2005) PAGE: parametric analysis of gene set enrichment. BMC Bioinformatics 6, 144
21. + intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 14, 528-536
22. Hjelkrem, M., Stauch, C., Shaw, J., and Harrison, S. A. (2011) Validation of the non-alcoholic fatty liver disease activity score. Aliment. Pharmacol. Ther. 34, 214-218
23. Kleiner, D. E., Brunt, E. M., Van Natta, M., Behling, C., Contos, M. J., Cummings, O. W., Ferrell, L. D., Liu, Y. C., Torbenson, M. S., Unalp-Arida, A., Yeh, M., McCullough, A. J., Sanyal, A. J., and Nonalcoholic Steatohepatitis Clinical Research Network (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321
24. Bowden, J. A., Albert, C. J., Barnaby, O. S., and Ford, D. A. (2011) Analysis of cholesteryl esters and diacylglycerols using lithiated adducts and electrospray ionization-tandem mass spectrometry. Anal. Biochem. 417, 202-210
25. Brown, R. J., Shao, F., Baldán, A., Albert, C. J., and Ford, D. A. (2013) Cholesterol efflux analyses using stable isotopes and mass spectrometry. Anal. Biochem. 433, 56-64
26. Yang, Y., Kuwano, T., Lagor, W. R., Albert, C. J., Brenton, S., Rader, D. J., Ford, D. A., and Brown, R. J. (2014) Lipidomic analyses of female mice lacking hepatic lipase and endothelial lipase indicate selective modulation of plasma lipid species. Lipids 49, 505-515
27. Hammond, L. E., Gallagher, P. A., Wang, S., Hiller, S., Kluckman, K. D., Posey-Marcos, E. L., Maeda, N., and Coleman, R. A. (2002) Mitochondrial glycerol-3-phosphate acyltransferase-deficient mice have reduced weight and liver triacylglycerol content and altered glycerolipid fatty acid composition. Mol. Cell. Biol. 22, 8204-8214
28. Chang, B. H., Li, L., Paul, A., Taniguchi, S., Nannegari, V., Heird, W. C., and Chan, L. (2006) Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol. Cell. Biol. 26, 1063-1076
29. McManaman, J. L., Bales, E. S., Orlicky, D. J., Jackman, M., MacLean, P. S., Cain, S., Crunk, A. E., Mansur, A., Graham, C. E., Bowman, T. A., and Greenberg, A. S. (2013) Perilipin-2-null mice are protected against diet-induced obesity, adipose inflammation, and fatty liver disease. J. Lipid Res. 54, 1346-1359
30. Zhou, L., Xu, L., Ye, J., Li, D., Wang, W., Li, X., Wu, L., Wang, H., Guan, F., and Li, P. (2012) Cidea promotes hepatic steatosis by sensing dietary fatty acids. Hepatology 56, 95-107
31. Li, J. Z., Ye, J., Xue, B., Qi, J., Zhang, J., Zhou, Z., Li, Q., Wen, Z., and Li, P. (2007) Cideb regulates diet-induced obesity, liver steatosis, and insulin sensitivity by controlling lipogenesis and fatty acid oxidation. Diabetes 56, 2523-2532
32. Yamaguchi, K., Yang, L., McCall, S., Huang, J., Yu, X. X., Pandey, S. K., Bhanot, S., Monia, B. P., Li, Y. X., and Diehl, A. M. (2007) Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 45, 1366-1374
33. Anderson, N., and Borlak, J. (2008) Molecular mechanisms and therapeutic targets in steatosis and steatohepatitis. Pharmacol. Rev. 60, 311-357
34. Cheung, O., and Sanyal, A. J. (2008) Abnormalities of lipid metabolism in nonalcoholic fatty liver disease. Semin. Liver Dis. 28, 351-359
35. Nagarajan, P., Mahesh Kumar, M. J., Venkatesan, R., Majundar, S. S., and Juyal, R. C. (2012) Genetically modified mouse models for the study of nonalcoholic fatty liver disease. World J. Gastroenterol. 18, 1141-1153
36. Kubota, N., Kado, S., Kano, M., Masuoka, N., Nagata, Y., Kobayashi, T., Miyazaki, K., and Ishikawa, F. (2013) A high-fat diet and multiple administration of carbon tetrachloride induces liver injury and pathological features associated with non-alcoholic steatohepatitis in mice. Clin. Exp. Pharmacol. Physiol. 40, 422-430
37. Kita, Y., Takamura, T., Misu, H., Ota, T., Kurita, S., Takeshita, Y., Uno, M., Matsuzawa-Nagata, N., Kato, K., Ando, H., Fujimura, A., Hayashi, K., Kimura, T., Ni, Y., Otoda, T., Miyamoto, K., Zen, Y., Nakanuma, Y., and Kaneko, S. (2012) Metformin prevents and reverses inflammation in a non-diabetic mouse model of nonalcoholic steatohepatitis. PloS One 7, e43056
38. Fukunishi, S., Nishio, H., Fukuda, A., Takeshita, A., Hanafusa, T., Higuchi, K., and Suzuki, K. (2009) Development of fibrosis in nonalcoholic steatosis through combination of a synthetic diet rich in disaccharide and low-dose lipopolysaccharides in the livers of Zucker (fa/fa) rats. J. Clin. Biochem. Nutr. 45, 322-328
39. Yang, S. Q., Lin, H. Z., Lane, M. D., Clemens, M., and Diehl, A. M. (1997) Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc. Natl. Acad. Sci. U. S. A. 94, 2557-2562
40. Sato, W., Horie, Y., Kataoka, E., Ohshima, S., Dohmen, T., Iizuka, M., Sasaki, J., Sasaki, T., Hamada, K., Kishimoto, H., Suzuki, A., and Watanabe, S. (2006) Hepatic gene expression in hepatocyte-specific Pten deficient mice showing steatohepatitis without ethanol challenge. Hepatol. Res. 34, 256-265
41. Svegliati-Baroni, G., Candelaresi, C., Saccomanno, S., Ferretti, G., Bachetti, T., Marzioni, M., De Minicis, S., Nobili, L., Salzano, R., Omenetti, A., Pacetti, D., Sigmund, S., Benedetti, A., and Casini, A. (2006) Amodel of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptor-α and n-3 polyunsaturated fatty acid treatment on liver injury. Am. J. Pathol. 169, 846-860
42. Kohli, R., Kirby, M., Xanthakos, S. A., Softic, S., Feldstein, A. E., Saxena, V., Tang, P. H., Miles, L., Miles, M. V., Balistreri, W. F., Woods, S. C., and Seeley, R. J. (2010) High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis. Hepatology 52, 934-944
43. Matsuzawa, N., Takamura, T., Kurita, S., Misu, H., Ota, T., Ando, H., Yokoyama, M., Honda, M., Zen, Y., Nakanuma, Y., Miyamoto, K., and Kaneko, S. (2007) Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46, 1392-1403
44. Rinella, M. E., and Green, R. M. (2004) The methionine-choline deficient dietary model of steatohepatitis does not exhibit insulin resistance. J. Hepatol. 40, 47-51
45. Rizki, G., Arnaboldi, L., Gabrielli, B., Yan, J., Lee, G. S., Ng, R. K., Turner, S. M., Badger, T. M., Pitas, R. E., and Maher, J. J. (2006) Mice fed a lipogenic methionine-choline-deficient diet develop hypermetabolism coincident with hepatic suppression of SCD-1. J. Lipid Res. 47, 2280-2290