Abrogating monoacylglycerol acyltransferase activity in liver improves glucose tolerance and hepatic insulin signaling in obese mice

Diabetes

Volumn 63, Issue 7, 2014, Pages 2284-2296

  Hall, Angela M ^a   Soufi, Nisreen ^a   Chambers, Kari T ^a   Chen, Zhouji ^a   Schweitzer, George G ^a   McCommis, Kyle S ^a   Erion, Derek M ^b   Graham, Mark J ^c   Su, Xiong ^a,d   Finck, Brian N ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

^c ISIS PHARMACEUTICALS   (United States)

^d MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLGLYCEROL PALMITOYLTRANSFERASE; ACYLGLYCEROL PALMITOYLTRANSFERASE 1; ANTISENSE OLIGONUCLEOTIDE; DIACYLGLYCEROL; GLUCOSE; INSULIN; MOGAT1 PROTEIN; PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXPERIMENTAL OBESITY; GENE SILENCING; GLUCOSE TOLERANCE; MALE; MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ACYLTRANSFERASES; ANIMALS; DIET, HIGH-FAT; DIGLYCERIDES; GENE EXPRESSION; GLUCOSE; INSULIN; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; MICE, TRANSGENIC; OBESITY; OLIGONUCLEOTIDES, ANTISENSE; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

EID: 84903179316     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1502     Document Type: Article

References (46)

1. Jornayvaz FR, Birkenfeld AL, Jurczak MJ, et al. Hepatic insulin resistance in mice with hepatic overexpression of diacylglycerol acyltransferase 2. Proc Natl Acad Sci U S A 2011;108:5748-5752
2. Jornayvaz FR, Lee HY, Jurczak MJ, et al. Thyroid hormone receptor-α gene knockout mice are protected from diet-induced hepatic insulin resistance. Endocrinology 2012;153:583-591
3. Jornayvaz FR, Shulman GI. Diacylglycerol activation of protein kinase Cε and hepatic insulin resistance. Cell Metab 2012;15:574-584
4. Wendel AA, Li LO, Li Y, Cline GW, Shulman GI, Coleman RA. Glycerol-3-phosphate acyltransferase 1 defi ciency in ob/ob mice diminishes hepatic steatosis but does not protect against insulin resistance or obesity. Diabetes 2010;59:1321-1329
5. Neschen S, Morino K, Hammond LE, et al. Prevention of hepatic steatosis and hepatic insulin resistance in mitochondrial acyl-CoA:glycerol-sn-3-phosphate acyltransferase 1 knockout mice. Cell Metab 2005;2:55-65 (Pubitemid 43239825)
6. Summers SA. Sphingolipids and insulin resistance: the five Ws. Curr Opin Lipidol 2010;21:128-135
7. Farese RV Jr, Zechner R, Newgard CB, Walther TC. The problem of establishing relationships between hepatic steatosis and hepatic insulin resistance. Cell Metab 2012;15:570-573
8. Shi Y, Cheng D. Beyond triglyceride synthesis: the dynamic functional roles of MGAT and DGAT enzymes in energy metabolism. Am J Physiol Endocrinol Metab 2009;297:E10-E18
9. Cao J, Hawkins E, Brozinick J, et al. A predominant role of acyl-CoA: monoacylglycerol acyltransferase-2 in dietary fat absorption implicated by tissue distribution, subcellular localization, and up-regulation by high fat diet. J Biol Chem 2004;279:18878-18886 (Pubitemid 38623315)
10. Yue YG, Chen YQ, Zhang Y, et al. The acyl coenzymeA:monoacylglycerol acyltransferase 3 (MGAT3) gene is a pseudogene in mice but encodes a functional enzyme in rats. Lipids 2011;46:513-520
11. Hall AM, Kou K, Chen Z, et al. Evidence for regulated monoacylglycerol acyltransferase expression and activity in human liver. J Lipid Res 2012;53:990-999
12. Yen CL, Stone SJ, Cases S, Zhou P, Farese RV Jr. Identification of a gene encoding MGAT1, a monoacylglycerol acyltransferase. Proc Natl Acad Sci U S A 2002;99:8512-8517 (Pubitemid 34693593)
13. Yen CL, Farese RV Jr. MGAT2, a monoacylglycerol acyltransferase expressed in the small intestine. J Biol Chem 2003;278:18532-18537
14. Mostafa N, Bhat BG, Coleman RA. Increased hepatic monoacylglycerol acyltransferase activity in streptozotocin-induced diabetes: characterization and comparison with activities from adult and neonatal rat liver. Biochim Biophys Acta 1993;1169:189-195 (Pubitemid 23234596)
15. Xia T, Mostafa N, Bhat BG, Florant GL, Coleman RA. Selective retention of essential fatty acids: the role of hepatic monoacylglycerol acyltransferase. Am J Physiol 1993;265:R414-R419 (Pubitemid 23275085)
16. Lee YJ, Ko EH, Kim JE, et al. 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 2012;109:13656-13661
17. Yen CL, Cheong ML, Grueter C, et al. Deficiency of the intestinal enzyme acyl CoA:monoacylglycerol acyltransferase-2 protects mice from metabolic disorders induced by high-fat feeding. Nat Med 2009;15:442-446
18. Chen Z, Vigueira PA, Chambers KT, et al. Insulin resistance and metabolic derangements in obese mice are ameliorated by a novel peroxisome proliferator-activated receptor γ-sparing thiazolidinedione. J Biol Chem 2012;287:23537-23548
19. Finck BN, Bernal-Mizrachi C, Han DH, et al. A potential link between muscle peroxisome proliferator- activated receptor-alpha signaling and obesity-related diabetes. Cell Metab 2005;1:133-144 (Pubitemid 43960595)
20. Chen Z, Gropler MC, Norris J, Lawrence JC Jr, Harris TE, Finck BN. Alterations in hepatic metabolism in fld mice reveal a role for lipin 1 in regulating VLDL-triacylglyceride secretion. Arterioscler Thromb Vasc Biol 2008;28:1738-1744
21. Harris LA, Shew TM, Skinner JR, Wolins NE. A single centrifugation method for isolating fat droplets from cells and tissues. J Lipid Res 2012;53:1021-1025
22. Cantley JL, Yoshimura T, Camporez JP, et al. CGI-58 knockdown sequesters diacylglycerols in lipid droplets/ER-preventing diacylglycerol-mediated hepatic insulin resistance. Proc Natl Acad Sci U S A 2013;110:1869-1874
23. Magkos F, Su X, Bradley D, et al. Intrahepatic diacylglycerol content is associated with hepatic insulin resistance in obese subjects. Gastroenterology 2012;142:1444-1446
24. Leiker TJ, Barkley RM, Murphy RC. Analysis of diacylglycerol molecular species in cellular lipid extracts by normal-phase LC-electrospray mass spectrometry. Int J Mass Spectrom 2011;305:103-109
25. Boni LT, Rando RR. The nature of protein kinase C activation by physically defined phospholipid vesicles and diacylglycerols. J Biol Chem 1985;260:10819-10825 (Pubitemid 16252268)
26. Rando RR, Young N. The stereospecific activation of protein kinase C. Biochem Biophys Res Commun 1984;122:818-823
27. Nomura H, Ase K, Sekiguchi K, et al. Stereospecificity of diacylglycerol for stimulus-response coupling in platelets. Biochem Biophys Res Commun 1986;140:1143-1151 (Pubitemid 17207809)
28. Choi CS, Savage DB, Abu-Elheiga L, et al. Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Proc Natl Acad Sci U S A 2007;104:16480-16485 (Pubitemid 350211044)
29. Jornayvaz FR, Jurczak MJ, Lee HY, et al. A high-fat, ketogenic diet causes hepatic insulin resistance in mice, despite increasing energy expenditure and preventing weight gain. Am J Physiol Endocrinol Metab 2010;299:E808-E815
30. Samuel VT, Liu ZX, Wang A, et al. Inhibition of protein kinase Cepsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest 2007;117:739-745 (Pubitemid 46348532)
31. Bezy O, Tran TT, Pihlajamäki J, et al. PKCd regulates hepatic insulin sensitivity and hepatosteatosis in mice and humans. J Clin Invest 2011;121:2504-2517
32. Frangioudakis G, Burchfield JG, Narasimhan S, et al. Diverse roles for protein kinase C delta and protein kinase C epsilon in the generation of high-fat-diet-induced glucose intolerance in mice: regulation of lipogenesis by protein kinase C delta. Diabetologia 2009;52:2616-2620
33. Abdeen MB, Chowdhury NA, Hayden MR, Ibdah JA. Nonalcoholic steatohepatitis and the cardiometabolic syndrome. J Cardiometab Syndr 2006;1:36-40
34. Petersen KF, Shulman GI. Etiology of insulin resistance. Am J Med 2006;119(Suppl. 1):S10-S16
35. Samuel VT, Liu ZX, Qu X, et al. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 2004;279:32345-32353 (Pubitemid 39014687)
36. Choi CS, Savage DB, Kulkarni A, et al. Suppression of diacylglycerol acyltransferase-2 (DGAT2), but not DGAT1, with antisense oligonucleotides reverses diet-induced hepatic steatosis and insulin resistance. J Biol Chem 2007;282:22678-22688 (Pubitemid 47267336)
37. Nagai Y, Yonemitsu S, Erion DM, et al. The role of peroxisome proliferator-activated receptor gamma coactivator-1 beta in the pathogenesis of fructose-induced insulin resistance. Cell Metab 2009;9:252-264
38. Monetti M, Levin MC, Watt MJ, et al. Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver. Cell Metab 2007;6:69-78 (Pubitemid 46995777)
39. Timmers S, de Vogel-van den Bosch J, Hesselink MK, et al. Paradoxical increase in TAG and DAG content parallel the insulin sensitizing effect of unilateral DGAT1 overexpression in rat skeletal muscle. PLoS One 2011;6:e14503
40. Ong KT, Mashek MT, Bu SY, Mashek DG. Hepatic ATGL knockdown uncouples glucose intolerance from liver TAG accumulation. FASEB J 2013;27:313-321
41. Brown JM, Betters JL, Lord C, et al. CGI-58 knockdown in mice causes hepatic steatosis but prevents diet-induced obesity and glucose intolerance. J Lipid Res 2010;51:3306-3315
42. Voshol PJ, Haemmerle G, Ouwens DM, et al. Increased hepatic insulin sensitivity together with decreased hepatic triglyceride stores in hormone-sensitive lipase-deficient mice. Endocrinology 2003;144:3456-3462 (Pubitemid 36904422)
43. Monetti M, Canavesi M, Camera M, et al. Rosuvastatin displays anti-atherothrombotic and anti-infl ammatory properties in apoE-deficient mice. Pharmacol Res 2007;55:441-449 (Pubitemid 46560397)
44. Kumashiro N, Erion DM, Zhang D, et al. Cellular mechanism of insulin resistance in nonalcoholic fatty liver disease. Proc Natl Acad Sci U S A 2011;108:16381-16385
45. Bergman BC, Hunerdosse DM, Kerege A, Playdon MC, Perreault L. Localisation and composition of skeletal muscle diacylglycerol predicts insulin resistance in humans. Diabetologia 2012;55:1140-1150
46. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 2005;54:603-608 (Pubitemid 40322060)