Intestinal acyl-CoA: Diacylglycerol acyltransferase 2 overexpression enhances postprandial triglyceridemic response and exacerbates high fat diet-induced hepatic triacylglycerol storage

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 8, 2013, Pages 1377-1385

  Uchida, Aki ^a,b   Slipchenko, Mikhail N ^c   Eustaquio, Trisha ^a,c   Leary, James F ^a,c,d   Cheng, Ji Xin ^a,c   Buhman, Kimberly K ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d PURDUE UNIVERSITY   (United States)

Author keywords

Acyl CoA:diacylglycerol acyltransferase; Chylomicron; Cytoplasmic lipid droplet; Dietary fat absorption; Intestine; Triacylglycerol

Indexed keywords

DIACYLGLYCEROL ACYLTRANSFERASE 2; FAT; FATTY ACID; MESSENGER RNA; TRIACYLGLYCEROL; DGAT2 PROTEIN, MOUSE; DIACYLGLYCEROL ACYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAT INTAKE; FATTY ACID OXIDATION; FATTY LIVER; GENE OVEREXPRESSION; GENE TARGETING; INTESTINE; INTESTINE CELL; INTESTINE MUCOSA; LIPID DIET; LIPID METABOLISM; LIPID STORAGE; LIVER; MALE; MOUSE; NONHUMAN; POSTPRANDIAL STATE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; BLOOD; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; TRANSGENIC MOUSE;

MUS;

ANIMALS; DIACYLGLYCEROL O-ACYLTRANSFERASE; DIETARY FATS; ENTEROCYTES; FATTY ACIDS; FATTY LIVER; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTESTINES; LIVER; MICE; MICE, TRANSGENIC; ORGAN SPECIFICITY; OXIDATION-REDUCTION; POSTPRANDIAL PERIOD; TRIGLYCERIDES;

EID: 84882993406     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.04.013     Document Type: Article

References (40)

1. M.C. Carey, D.M. Small, C.M. Bliss, Lipid digestion and absorption, Annu. Rev. Physiol. 45 (1983) 651-677.
2. J.B. Zhu, B.G. Lee, K.K. Buhman, J.X. Cheng, A dynamic, cytoplasmic triacylglycerol pool in enterocytes revealed by ex vivo and in vivo coherent anti-Stokes Raman scattering imaging, J. Lipid Res. 50 (2009) 1080-1089.
3. M.D. Robertson, M. Parkes, B.F. Warren, D.J.P. Ferguson, K.G. Jackson, D.P. Jewell, K.N. Frayn, Mobilisation of enterocyte fat stores by oral glucose in humans, Gut 52 (2003) 834-839. (Pubitemid 36613490)
4. -/- mice, J. Lipid Res. 51 (2010) 1770-1780.
5. A. Uchida, M.C. Whitsitt, T. Eustaquio, M.N. Slipchenko, J.F. Leary, J.-X. Cheng, K.K. Buhman, Reduced triglyceride secretion in response to an acute dietary fat challenge in obese compared to lean mice, Front. Physiol. 3 (2012) 26.
6. C.-L.E. Yen, M.-L. Cheong, C. Grueter, P. Zhou, J. Moriwaki, J.S. Wong, B. Hubbard, S. Marmor, R.V. Farese, Deficiency of the intestinal enzyme acyl CoA: monoacylglycerol acyltransferase-2 protects mice from metabolic disorders induced by high-fat feeding, Nat. Med. 15 (2009) 442-446.
7. S. Cases, S.J. Smith, Y.W. Zheng, H.M. Myers, S.R. Lear, E. Sande, S. Novak, C. Collins, C.B. Welch, A.J. Lusis, S.K. Erickson, R.V. Farese Jr., Identification of a gene encoding an acyl CoA: diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 13018-13023. (Pubitemid 28509516)
8. K.K. Buhman, S.J. Smith, S.J. Stone, J.J. Repa, J.S. Wong, F.F. Knapp, B.J. Burri, R.L. Hamilton, N.A. Abumrad, R.V. Farese, DGAT1 is not essential for intestinal triacylglycerol absorption or chylomicron synthesis, J. Biol. Chem. 277 (2002) 25474-25479. (Pubitemid 34951861)
9. S. Cases, S.J. Stone, P. Zhou, E. Yen, B. Tow, K.D. Lardizabal, T. Voelker, R.V. Farese, Cloning of DGAT2, a second mammalian diacylglycerol acyltransferase, and related family members, J. Biol. Chem. 276 (2001) 38870-38876.
10. J.T. Haas, H.S. Winter, E. Lim, A. Kirby, B. Blumenstiel, M. DeFelice, S. Gabriel, C. Jalas, D. Branski, C.A. Grueter, M.S. Toporovski, T.C. Walther, M.J. Daly, R.V. Farese Jr., DGAT1 mutation is linked to a congenital diarrheal disorder, J. Clin. Invest. 122 (2012) 4680-4684.
11. F. Wilfling, H. Wang, J.T. Haas, N. Krahmer, T.J. Gould, A. Uchida, J.X. Cheng, M. Graham, R. Christiano, F. Frohlich, X. Liu, K.K. Buhman, R.A. Coleman, J. Bewersdorf, R.V. Farese Jr., T.C. Walther, Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets, Dev. Cell 24 (2013) 384-399.
12. S.J. Stone, M.C. Levin, P. Zhou, J.Y. Han, T.C. Walther, R.V. Farese, The endoplasmic reticulum enzyme DGAT2 is found in mitochondria-associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria, J. Biol. Chem. 284 (2009) 5352-5361.
13. C.L. Yen, S.J. Stone, S. Koliwad, C. Harris, R.V. Farese Jr., Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis, J. Lipid Res. 49 (2008) 2283-2301.
14. Q. Liu, R.M. Siloto, R. Lehner, S.J. Stone, R.J. Weselake, Acyl-CoA: diacylglycerol acyltransferase: molecular biology, biochemistry and biotechnology, Prog. Lipid Res. 51 (2012) 350-377.
15. R.L. Dow, J.C. Li, M.P. Pence, E.M. Gibbs, J.L. LaPerle, J. Litchfield, D.W. Piotrowski, M.J. Munchhof, T.B. Manion, W.J. Zavadoski, G.S. Walker, R.K. McPherson, S. Tapley, E. Sugarman, A. Guzman-Perez, P. DaSilva-Jardine, Discovery of PF-04620110, a potent, selective, and orally bioavailable inhibitor of DGAT-1, ACS Med. Chem. Lett. 2 (2011) 407-412.
16. D. Cheng, J. Iqbal, J. Devenny, C.H. Chu, L.P. Chen, J. Dong, R. Seethala, W.J. Keim, A.V. Azzara, R.M. Lawrence, M.A. Pelleymounter, M.M. Hussain, Acylation of acylglycerols by acyl coenzyme A:diacylglycerol acyltransferase 1 (DGAT1) functional importance of DGAT1 in intestinal fat absorption, J. Biol. Chem. 283 (2008) 29802-29811.
17. R.D. Jadhav, K.S. Kadam, S. Kandre, T. Guha, M.M. Reddy, M.K. Brahma, N.J. Deshmukh, A. Dixit, L. Doshi, N. Potdar, A.A. Enose, R.A. Vishwakarma, H. Sivaramakrishnan, S. Srinivasan, K.V. Nemmani, A. Gupte, A.K. Gangopadhyay, R. Sharma, Synthesis and biological evaluation of isoxazole, oxazole, and oxadiazole containing heteroaryl analogs of biaryl ureas as DGAT1 inhibitors, Eur. J. Med. Chem. 54 (2012) 324-342.
18. V.S. Yeh, D.W. Beno, S. Brodjian, M.E. Brune, S.C. Cullen, B.D. Dayton, M.K. Dhaon, H.D. Falls, J. Gao, N. Grihalde, P. Hajduk, T.M. Hansen, A.S. Judd, A.J. King, R.C. Klix, K.J. Larson, Y.Y. Lau, K.C. Marsh, S.W. Mittelstadt, D. Plata, M.J. Rozema, J.A. Segreti, E.J. Stoner, M.J. Voorbach, X. Wang, X. Xin, G. Zhao, C.A. Collins, B.F. Cox, R.M. Reilly, P.R. Kym, A.J. Souers, Identification and preliminary characterization of a potent, safe, and orally efficacious inhibitor of acyl-CoA: diacylglycerol acyltransferase 1, J. Med. Chem. 55 (2012) 1751-1757.
19. S.J. Stone, H.M. Myers, S.M. Watkins, B.E. Brown, K.R. Feingold, P.M. Elias, R.V. Farese, Lipopenia and skin barrier abnormalities in DGAT2-deficient mice, J. Biol. Chem. 279 (2004) 11767-11776. (Pubitemid 38401682)
20. J.D. Douglass, N. Malik, S.H. Chon, K. Wells, Y.X. Zhou, A.S. Choi, L.B. Joseph, J. Storch, Intestinal mucosal triacylglycerol accumulation secondary to decreased lipid secretion in obese and high fat fed mice, Front. Physiol. 3 (2012) 25.
21. K. Wakimoto, H. Chiba, H. Michibata, M. Seishima, S. Kawasaki, K. Okubo, H. Mitsui, H. Torii, Y. Imai, A novel diacylglycerol acyltransferase (DGAT2) is decreased in human psoriatic skin and increased in diabetic mice, Biochem. Biophys. Res. Commun. 310 (2003) 296-302. (Pubitemid 37163663)
22. A. Werner, R. Havinga, F. Perton, F. Kuipers, H.J. Verkade, Lymphatic chylomicron size is inversely related to biliary phospholipid secretion in mice, Am. J. Physiol. Gastrointest. Liver Physiol. 290 (2006) G1177-G1185. (Pubitemid 43788300)
23. T. Sakurai, S. Trirongjitmoah, Y. Nishibata, T. Namita, M. Tsuji, S.-P. Hui, S. Jin, K. Shimizu, H. Chiba, Measurement of lipoprotein particle sizes using dynamic light scattering, Ann. Clin. Biochem. 47 (2010) 476-481.
24. B.B. Madison, L. Dunbar, X.T. Qiao, K. Braunstein, E. Braunstein, D.L. Gumucio, Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine, J. Biol. Chem. 277 (2002) 33275-33283. (Pubitemid 34984848)
25. E.M. van Schothorst, P. Flachs, N.L. Franssen-van Hal, O. Kuda, A. Bunschoten, J. Molthoff, C. Vink, G.J. Hooiveld, J. Kopecky, J. Keijer, Induction of lipid oxidation by polyunsaturated fatty acids of marine origin in small intestine of mice fed a high-fat diet, BMC Genomics 10 (2009) 110.
26. A. Uchida, M.N. Slipchenko, J.X. Cheng, K.K. Buhman, Fenofibrate, a peroxisome proliferator-activated receptor a agonist, alters triglyceride metabolism in enterocytes of mice, Biochim. Biophys. Acta, Mol. Cell. Biol. Lipids 1811 (2011) 170-176.
27. J. Storch, Y.X. Zhou, W.S. Lagakos, Metabolism of apical versus basolateral sn-2-monoacylglycerol and fatty acids in rodent small intestine, J. Lipid Res. 49 (2008) 1762-1769.
28. M. Owen, V.A. Zammit, Evidence for overt and latent forms of DGAT in rat liver microsomes. Implications for the pathways of triacylglycerol incorporation into VLDL, Biochem. Soc. Trans. 25 (1997) 21S.
29. M.R. Owen, C.C. Corstorphine, V.A. Zammit, Overt and latent activities of diacylglycerol acytransferase in rat liver microsomes: possible roles in very-low-density lipoprotein triacylglycerol secretion, Biochem. J. 323 (Pt 1) (1997) 17-21. (Pubitemid 27153869)
30. S.L. Sturley, M.M. Hussain, Lipid droplet formation on opposing sides of the endoplasmic reticulum, J. Lipid Res. 53 (2012) 1800-1810.
31. D. Cheng, R.L. Meegalla, B. He, D.A. Cromley, J.T. Billheimer, P.R. Young, Human acyl-CoA: diacylglycerol acyltransferase is a tetrameric protein, Biochem. J. 359 (2001) 707-714. (Pubitemid 33063396)
32. C. Yu, J. Chen, S. Lin, J. Liu, C.C. Chang, T.Y. Chang, Human acyl-CoA: cholesterol acyltransferase-1 is a homotetrameric enzyme in intact cells and in vitro, J. Biol. Chem. 274 (1999) 36139-36145.
33. S.J. Stone, M.C. Levin, R.V. Farese Jr., Membrane topology and identification of key functional amino acid residues of murine acyl-CoA:diacylglycerol acyltransferase-2, J. Biol. Chem. 281 (2006) 40273-40282. (Pubitemid 46041832)
34. H.R. Wurie, L. Buckett, V.A. Zammit, Evidence that diacylglycerol acyltransferase 1 (DGAT1) has dual membrane topology in the endoplasmic reticulum of HepG2 cells, J. Biol. Chem. 286 (2011) 36238-36247.
35. L. Kuerschner, C. Moessinger, C. Thiele, Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets, Traffic 9 (2008) 338-352. (Pubitemid 351188994)
36. H.G. Windmueller, A.E. Spaeth, Identification of ketone bodies and glutamine as the major respiratory fuels in vivo for postabsorptive rat small intestine, J. Biol. Chem. 253 (1978) 69-76.
37. W.S. Lagakos, A.M. Gajda, L. Agellon, B. Binas, V. Choi, B. Mandap, T. Russnak, Y.X. Zhou, J. Storch, Different functions of intestinal and liver-type fatty acid-binding proteins in intestine and in whole body energy homeostasis, Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011) G803-G814.
38. H.M. de Vogel-van, M. den Bosch, P.J. de Bunger, H. Groot, G. Bosch-Vermeulen, M. Muller Hooiveld, PPARalpha-mediated effects of dietary lipids on intestinal barrier gene expression, BMC Genomics 9 (2008) 231.
39. T. Mori, H. Kondo, T. Hase, I. Tokimitsu, T. Murase, Dietary fish oil upregulates intestinal lipid metabolism and reduces body weight gain in C57BL/6J mice, J. Nutr. 137 (2007) 2629-2634. (Pubitemid 350255289)
40. R. Kimura, N. Takahashi, K. Murota, Y. Yamada, S. Niiya, N. Kanzaki, Y. Murakami, T. Moriyama, T. Goto, T. Kawada, Activation of peroxisome proliferator-activated receptor-alpha (PPAR alpha) suppresses postprandial lipidemia through fatty acid oxidation in enterocytes, Biochem. Biophys. Res. Commun. 410 (2011) 1-6.