Adipose triglyceride lipase is a TG hydrolase of the small intestine and regulates intestinal PPARα signaling

Journal of Lipid Research

Volumn 54, Issue 2, 2013, Pages 425-435

  Obrowsky, Sascha ^a   Chandak, Prakash G ^a   Patankar, Jay V ^a   Povoden, Silvia ^a   Schlager, Stefanie ^a   Kershaw, Erin E ^b   Bogner Strauss, Juliane G ^c   Hoefler, Gerald ^a   Levak Frank, Sanja ^a   Kratky, Dagmar ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Cholesterol absorption; Enterocytes; Peroxisome proliferator activated receptor alpha target genes; Triglyceride absorption

Indexed keywords

OLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; TRIACYLGLYCEROL LIPASE; TRIOLEIN; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BODY WEIGHT; CELL LEVEL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FECES ANALYSIS; GENE TARGETING; GENETIC REGULATION; LIPID HYDROLYSIS; LIPID METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMALL INTESTINE ABSORPTION; SYSTEMIC CIRCULATION;

ANIMALS; BIOLOGICAL TRANSPORT; CHOLESTEROL; DOWN-REGULATION; FATTY ACIDS, NONESTERIFIED; FECES; GENE KNOCKOUT TECHNIQUES; HOMEOSTASIS; INTESTINAL ABSORPTION; INTESTINE, SMALL; LIPASE; MALE; MICE; ORGAN SPECIFICITY; PPAR ALPHA; SIGNAL TRANSDUCTION; TRIGLYCERIDES;

EID: 84872475275     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M031716     Document Type: Article

References (41)

1. Whitcomb, D. C., and M. E. Lowe. 2007. Human pancreatic digestive enzymes. Dig. Dis. Sci. 52: 1-17.
2. Iqbal, J., and M. M. Hussain. 2009. Intestinal lipid absorption. Am. J. Physiol. Endocrinol. Metab. 296: E1183-E1194.
3. Lee, B., J. Zhu, N. E. Wolins, J. X. Cheng, and K. K. Buhman. 2009. Differential association of adipophilin and TIP47 proteins with cytoplasmic lipid droplets in mouse enterocytes during dietary fat absorption. Biochim. Biophys. Acta. 1791: 1173-1180.
4. Storch, J., Y. X. Zhou, and W. S. Lagakos. 2008. Metabolism of apical versus basolateral sn-2-monoacylglycerol and fatty acids in rodent small intestine. J. Lipid Res. 49: 1762-1769.
5. Niot, I., H. Poirier, T. T. Tran, and P. Besnard. 2009. Intestinal absorption of long-chain fatty acids: evidence and uncertainties. Prog. Lipid Res. 48: 101-115.
6. Grober, J., S. Lucas, M. Sorhede-Winzell, I. Zaghini, A. Mairal, J. A. Contreras, P. Besnard, C. Holm, and D. Langin. 2003. Hormone-sensitive lipase is a cholesterol esterase of the intestinal mucosa. J. Biol. Chem. 278: 6510-6515. (Pubitemid 36800912)
7. Mahan, J. T., G. D. Heda, R. H. Rao, and C. M. Mansbach 2nd. 2001. The intestine expresses pancreatic triacylglycerol lipase: regulation by dietary lipid. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G1187-G1196.
8. Obrowsky, S., P. G. Chandak, J. V. Patankar, T. Pfeifer, S. Povoden, R. Schreiber, G. Haemmerle, S. Levak-Frank, and D. Kratky. 2012. Cholesteryl ester accumulation and accelerated cholesterol absorption in intestine-specific hormone sensitive lipase-null mice. Biochim. Biophys. Acta. 1821: 1406-1414.
9. Trickett, J. I., D. D. Patel, B. L. Knight, E. D. Saggerson, G. F. Gibbons, and R. J. Pease. 2001. Characterization of the rodent genes for arylacetamide deacetylase, a putative microsomal lipase, and evidence for transcriptional regulation. J. Biol. Chem. 276: 39522-39532.
10. Lass, A., R. Zimmermann, M. Oberer, and R. Zechner. 2011. Lipolysis: a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores. Prog. Lipid Res. 50: 14-27.
11. Ahmadian, M., M. J. Abbott, T. Tang, C. S. Hudak, Y. Kim, M. Bruss, M. K. Hellerstein, H. Y. Lee, V. T. Samuel, G. I. Shulman, et al. 2011. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 13: 739-748.
12. Chandak, P. G., B. Radovic, E. Aflaki, D. Kolb, M. Buchebner, E. Frohlich, C. Magnes, F. Sinner, G. Haemmerle, R. Zechner, et al. 2010. Efficient phagocytosis requires triacylglycerol hydrolysis by adipose triglyceride lipase. J. Biol. Chem. 285: 20192-20201.
13. Haemmerle, G., A. Lass, R. Zimmermann, G. Gorkiewicz, C. Meyer, J. Rozman, G. Heldmaier, R. Maier, C. Theussl, S. Eder, et al. 2006. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 312: 734-737.
14. Haemmerle, G., T. Moustafa, G. Woelkart, S. Buttner, A. Schmidt, T. van de Weijer, M. Hesselink, D. Jaeger, P. C. Kienesberger, K. Zierler, et al. 2011. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat. Med. 17: 1076-1085.
15. Ong, K. T., M. T. Mashek, S. Y. Bu, A. S. Greenberg, and D. G. Mashek. 2011. Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology. 53: 116-126.
16. Wu, J. W., S. P. Wang, S. Casavant, A. Moreau, G. S. Yang, and G. A. Mitchell. 2012. Fasting energy homeostasis in mice with adipose deficiency of desnutrin/adipose triglyceride lipase. Endocrinology. 153: 2198-2207.
17. Bunger, M., H. M. van den Bosch, J. van der Meijde, S. Kersten, G. J. Hooiveld, and M. Muller. 2007. Genome-wide analysis of PPARalpha activation in murine small intestine. Physiol. Genomics. 30: 192-204. (Pubitemid 47173282)
18. de Vogel-van den Bosch, H. M., M. Bunger, P. J. de Groot, H. Bosch-Vermeulen, G. J. Hooiveld, and M. Muller. 2008. PPARalpha-mediated effects of dietary lipids on intestinal barrier gene expression. BMC Genomics. 9: 231.
19. van den Bosch, H. M., M. Bunger, P. J. de Groot, J. van der Meijde, G. J. Hooiveld, and M. Muller. 2007. Gene expression of transporters and phase I/II metabolic enzymes in murine small intestine during fasting. BMC Genomics. 8: 267.
20. Madison, B. B., L. Dunbar, X. T. Qiao, K. Braunstein, E. Braunstein, and D. L. Gumucio. 2002. 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: 33275-33283. (Pubitemid 34984848)
21. Chandak, P. G., S. Obrowsky, B. Radovic, P. Doddapattar, E. Aflaki, A. Kratzer, L. S. Doshi, S. Povoden, H. Ahammer, G. Hoefler, et al. 2011. Lack of acyl-CoA:diacylglycerol acyltransferase 1 reduces intestinal cholesterol absorption and attenuates atherosclerosis in apolipoprotein E knockout mice. Biochim. Biophys. Acta. 1811: 1011-1020.
22. Zhu, J., B. Lee, K. K. Buhman, and J. X. Cheng. 2009. A dynamic, cytoplasmic triacylglycerol pool in enterocytes revealed by ex vivo and in vivo coherent anti-Stokes Raman scattering imaging. J. Lipid Res. 50: 1080-1089.
23. Jenkins, C. M., D. J. Mancuso, W. Yan, H. F. Sims, B. Gibson, and R. W. Gross. 2004. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279: 48968-48975. (Pubitemid 39625778)
24. Villena, J. A., S. Roy, E. Sarkadi-Nagy, K. H. Kim, and H. S. Sul. 2004. Desnutrin, an adipocyte gene encoding a novel patatin domain- containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J. Biol. Chem. 279: 47066-47075. (Pubitemid 39518362)
25. Zimmermann, R., J. G. Strauss, G. Haemmerle, G. Schoiswohl, R. Birner-Gruenberger, M. Riederer, A. Lass, G. Neuberger, F. Eisenhaber, A. Hermetter, et al. 2004. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science. 306: 1383-1386. (Pubitemid 39532517)
26. Etschmaier, K., T. Becker, T. O. Eichmann, C. Schweinzer, M. Scholler, C. Tam-Amersdorfer, M. Poeckl, R. Schuligoi, A. Kober, A. P. Chirackal Manavalan, et al. 2011. Adipose triglyceride lipase affects triacylglycerol metabolism at brain barriers. J. Neurochem. 119: 1016-1028.
27. Quiroga, A. D., and R. Lehner. 2012. Liver triacylglycerol lipases. Biochim. Biophys. Acta. 1821: 762-769.
28. Wu, J. W., S. P. Wang, F. Alvarez, S. Casavant, N. Gauthier, L. Abed, K. G. Soni, G. Yang, and G. A. Mitchell. 2011. Deficiency of liver adipose triglyceride lipase in mice causes progressive hepatic steatosis. Hepatology. 54: 122-132.
29. Temel, R. E., and J. M. Brown. 2012. Biliary and nonbiliary contributions to reverse cholesterol transport. Curr. Opin. Lipidol. 23: 85-90.
30. Mansbach 2nd, C. M., and R. F. Dowell. 1995. Role of the intestine in chylomicron remnant clearance. Am. J. Physiol. 269: G144-G152.
31. Soued, M., and C. M. Mansbach 2nd. 1996. Chylomicron remnant uptake by enterocytes is receptor dependent. Am. J. Physiol. 270: G203-G212.
32. Franck, P., J. L. Sallerin, H. Schroeder, M. A. Gelot, and P. Nabet. 1996. Rapid determination of fecal fat by Fourier transform infrared analysis (FTIR) with partial least-squares regression and an attenuated total reflectance accessory. Clin. Chem. 42: 2015-2020. (Pubitemid 26415355)
33. Tsuboi, K. K., L. K. Kwong, P. Sunshine, and R. O. Castillo. 1992. Mechanism of maturational decline of rat intestinal lactase-phlorizin hydrolase. Biochem. J. 282: 107-113.
34. Kaminsky, L. S., and Q. Y. Zhang. 2003. The small intestine as a xenobiotic-metabolizing organ. Drug Metab. Dispos. 31: 1520-1525. (Pubitemid 37466920)
35. Xie, Y., E. P. Newberry, S. G. Young, S. Robine, R. L. Hamilton, J. S. Wong, J. Luo, S. Kennedy, and N. O. Davidson. 2006. Compensatory increase in hepatic lipogenesis in mice with conditional intestine-specific Mttp deficiency. J. Biol. Chem. 281: 4075-4086. (Pubitemid 43847833)
36. Knight, B. L., D. D. Patel, S. M. Humphreys, D. Wiggins, and G. F. Gibbons. 2003. Inhibition of cholesterol absorption associated with a PPAR alpha-dependent increase in ABC binding cassette transporter A1 in mice. J. Lipid Res. 44: 2049-2058. (Pubitemid 37509620)
37. Kimura, R., N. Takahashi, K. Murota, Y. Yamada, S. Niiya, N. Kanzaki, Y. Murakami, T. Moriyama, T. Goto, and T. Kawada. 2011. Activation of peroxisome proliferator-activated receptor-alpha (PPARalpha) suppresses postprandial lipidemia through fatty acid oxidation in enterocytes. Biochem. Biophys. Res. Commun. 410: 1-6.
38. Uchida, A., M. N. Slipchenko, J. X. Cheng, and K. K. Buhman. 2011. Fenofibrate, a peroxisome proliferator-activated receptor alpha agonist, alters triglyceride metabolism in enterocytes of mice. Biochim. Biophys. Acta. 1811: 170-176.
39. Nauli, A. M., F. Nassir, S. Zheng, Q. Yang, C. M. Lo, S. B. Vonlehmden, D. Lee, R. J. Jandacek, N. A. Abumrad, and P. Tso. 2006. CD36 is important for chylomicron formation and secretion and may mediate cholesterol uptake in the proximal intestine. Gastroenterology. 131: 1197-1207.
40. Brunham, L. R., J. K. Kruit, J. Iqbal, C. Fievet, J. M. Timmins, T. D. Pape, B. A. Coburn, N. Bissada, B. Staels, A. K. Groen, et al. 2006. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 116 : 1052-1062.
41. Colin, S., O. Briand, V. Touche, K. Wouters, M. Baron, F. Pattou, R. Hanf, A. Tailleux, G. Chinetti, B. Staels, et al. 2012. Activation of intestinal peroxisome proliferator-activated receptor-alpha increases high-density lipoprotein production. Eur. Heart J. In press.