Direct comparison of mice null for liver or intestinal fatty acid-binding proteins reveals highly divergent phenotypic responses to high fat feeding

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30330-30344

  Gajda, Angela M ^a,b   Zhou, Yin Xiu ^a   Agellon, Luis B ^c   Fried, Susan K ^d   Kodukula, Sarala ^a   Fortson, Walter ^a   Patel, Khamoshi ^a   Storch, Judith ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COEXPRESSED; ENERGY HOMEOSTASIS; FATTY ACID-BINDING PROTEINS; LIPID METABOLISMS; PHENOTYPIC RESPONSE; WHOLE BODY;

FATTY ACIDS; MAMMALS; PROTEINS;

BINDING ENERGY;

2 ARACHIDONOYLGLYCEROL; ARACHIDONOYLETHANOLAMINE; ENDOCANNABINOID; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 2; LIVER FATTY ACID BINDING PROTEIN; LONG CHAIN FATTY ACID; MONOACYLGLYCEROL; PHOSPHOLIPID; SATURATED FATTY ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENERGY BALANCE; FATTY ACID OXIDATION; FOOD INTAKE; KNOCKOUT MOUSE; LEAN BODY WEIGHT; LIPID DIET; LIPID METABOLISM; MOUSE; NONHUMAN; OBESITY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; WEIGHT CHANGE; WILD TYPE;

FATTY ACID; FATTY ACID-BINDING PROTEIN; INTESTINE; LIPID METABOLISM; MONOACYLGLYCEROL;

ANIMALS; DIETARY FATS; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; MICE; MICE, KNOCKOUT; OXIDATION-REDUCTION; PHOSPHOLIPIDS; TRIGLYCERIDES;

EID: 84886909998     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.501676     Document Type: Article

References (84)

1. Kennedy, E. T., Bowman, S. A., and Powell, R. (1999) Dietary-fat intake in the U.S. population. J. Am. Coll. Nutr. 18, 207-212
2. Mishkin, S., Stein, L., Gatmaitan, Z., and Arias, I. M. (1972) The binding of fatty acids to cytoplasmic proteins: binding to Z protein in liver and other tissues of the rat. Biochem. Biophys. Res. Commun. 47, 997-1003
3. Ockner, R. K., Manning, J. A., Poppenhausen, R. B., and Ho, W. K. (1972) A binding protein for fatty acids in cytosol of intestinal mucosa, liver, myocardium, and other tissues. Science 177, 56-58
4. Gordon, J. I., Elshourbagy, N., Lowe, J. B., Liao, W. S., Alpers, D. H., and Taylor, J. M. (1985) Tissue specific expression and developmental regulation of two genes coding for rat fatty acid binding proteins. J. Biol. Chem. 260, 1995-1998
5. Levy, E., Ménard, D., Delvin, E., Montoudis, A., Beaulieu, J. F., Mailhot, G., Dubé, N., Sinnett, D., Seidman, E., and Bendayan, M. (2009) Localization, function and regulation of the two intestinal fatty acid-binding protein types. Histochem. Cell Biol. 132, 351-367
6. Murphy, E. J., Prows, D. R., Jefferson, J. R., and Schroeder, F. (1996) Liver fatty acid-binding protein expression in transfected fibroblasts stimulates fatty acid uptake and metabolism. Biochim. Biophys. Acta 1301, 191-198
7. Alpers, D. H., Bass, N. M., Engle, M. J., and DeSchryver-Kecskemeti, K. (2000) Intestinal fatty acid binding protein may favor differential apical fatty acid binding in the intestine. Biochim. Biophys. Acta 1483, 352-362
8. Wolfrum, C., Borchers, T., Sacchettini, J. C., and Spener, F. (2000) Binding of fatty acids and peroxisome proliferators to orthologous fatty acid binding proteins from human, murine, and bovine liver. Biochemistry 39, 14363
9. Lagakos, W. S., Guan, X., Ho, S.-Y., Sawicki, L. R., Corsico, B., Kodukula, S., Murota, K., Stark, R. E., and Storch, J. (2013) Liver fatty acid-binding protein binds monoacylglycerol in vitro and in mouse liver cytosol. J. Biol. Chem. 288, 19805-19815
10. Hsu, K. T., and Storch, J. (1996) Fatty acid transfer from liver and intestinal fatty acid-binding proteins to membranes occurs by different mechanisms. J. Biol. Chem. 271, 13317-13323
11. Corsico, B., Cistola, D. P., Frieden, C., and Storch, J. (1998) The helical domain of intestinal fatty acid binding protein is critical for collisional transfer of fatty acids to phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 95, 12174-12178
12. Falomir-Lockhart, L. J., Franchini, G. R., Guerbi, M. X., Storch, J., and Córsico, B. (2011) Interaction of enterocyte FABPs with phospholipid membranes: clues for specific physiological roles. Biochim. Biophys. Acta 1811, 452-459
13. Richieri, G. V., Ogata, R. T., and Kleinfeld, A. M. (1994) Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte, intestine, heart, and liver measured with the fluorescent probe ADIFAB. J. Biol. Chem. 269, 23918-23930
14. Newberry, E. P., Xie, Y., Kennedy, S., Han, X., Buhman, K. K., Luo, J., Gross, R. W., and Davidson, N. O. (2003) Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 278, 51664-51672
15. Martin, G. G., Danneberg, H., Kumar, L. S., Atshaves, B. P., Erol, E., Bader, M., Schroeder, F., and Binas, B. (2003) Decreased liver fatty acid binding capacity and altered liver lipid distribution in mice lacking the liver fatty acid-binding protein gene. J. Biol. Chem. 278, 21429-21438
16. Erol, E., Kumar, L. S., Cline, G. W., Shulman, G. I., Kelly, D. P., and Binas, B. (2004) Liver fatty acid-binding protein is required for high rates of hepatic fatty acid oxidation but not for the action of PPAR- in fasting mice. FASEB J. 18, 347-349
17. Newberry, E. P., Xie, Y., Kennedy, S. M., Luo, J., and Davidson, N. O. (2006) Protection against Western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology 44, 1191-1205
18. Atshaves, B. P., McIntosh, A. L., Storey, S. M., Landrock, K. K., Kier, A. B., and Schroeder, F. (2010) High dietary fat exacerbates weight gain and obesity in female liver fatty acid binding protein gene-ablated mice. Lipids 45, 97-110
19. Martin, G. G., Atshaves, B. P., McIntosh, A. L., Payne, H. R., Mackie, J. T., Kier, A. B., and Schroeder, F. (2009) Liver fatty acid binding protein gene ablation enhances age-dependent weight gain in male mice. Mol. Cell. Biochem. 324, 101-115
20. McIntosh, A. L., Atshaves, B. P., Landrock, D., Landrock, K. K., Martin, G. G., Storey, S. M., Kier, A. B., and Schroeder, F. (2013) Liver fatty acid binding protein gene-ablation exacerbates weight gain in high fat fed female mice. Lipids 48, 435-448
21. Newberry, E. P., Kennedy, S. M., Xie, Y., Luo, J., Stanley, S. E., Semenkovich, C. F., Crooke, R. M., Graham, M. J., and Davidson, N. O. (2008) Altered hepatic triglyceride content after partial hepatectomy without impaired liver regeneration in multiple murine genetic models. Hepatology 48, 1097-1105
22. Newberry, E. P., Kennedy, S. M., Xie, Y., Luo, J., Crooke, R. M., Graham, M. J., Fu, J., Piomelli, D., and Davidson, N. O. (2012) Decreased body weight and hepatic steatosis with altered fatty acid ethanolamide metabolism in aged L-Fabp-/- mice. J. Lipid Res. 53, 744-754
23. Agellon, L. B., Drozdowski, L., Li, L., Iordache, C., Luong, L., Clandinin, M. T., Uwiera, R. R., Toth, M. J., and Thomson, A. B. (2007) Loss of intestinal fatty acid binding protein increases the susceptibility of male mice to high fat diet-induced fatty liver. Biochim. Biophys. Acta 1771, 1283-1288
24. Vassileva, G., Huwyler, L., Poirier, K., Agellon, L. B., and Toth, M. J. (2000) The intestinal fatty acid binding protein is not essential for dietary fat absorption in mice. FASEB J. 14, 2040-2046
25. Lagakos, W. S., Gajda, A. M., Agellon, L., Binas, B., Choi, V., Mandap, B., Russnak, T., Zhou, Y. X., and Storch, J. (2011) 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, G803-G814
26. McIntosh, A. L., Atshaves, B. P., Hostetler, H. A, Huang, H., Davis, J., Lyuksyutova, O. I., Landrock, D., Kier, A. B., and Schroeder, F. (2009) Liver type fatty acid binding protein (L-FABP) gene ablation reduces nuclear ligand distribution and peroxisome proliferator-activated receptor- activity in cultured primary hepatocytes. Arch. Biochem. Biophys. 485, 160-173
27. Lusk, G. (1928) The Elements of Science of Nutrition., 4th Ed., Saunders, Philadelphia
28. McLean, J., and Tobin, C. (1987) Animal and Human Calorimetry, pp. 30-32, Cambridge University Press, New York
29. Tschöp,M. H., Speakman, J. R., Arch, J. R., Auwerx, J., Brüning, J. C., Chan, L., Eckel, R. H., Farese, R. V., Galgani, J. E., Hambly, C., Herman, M. A., Horvath, T. L., Kahn, B. B., Kozma, S. C., Maratos-Flier, E., Müller, T. D., Münzberg, H., Pfluger, P. T., Plum, L., Reitman, M. L., Rahmouni, K., Shulman, G. I., Thomas, G., Kahn, C. R., and Ravussin, E. (2012)Aguide to analysis of mouse energy metabolism. Nat. Methods 9, 57-63
30. Folch, J., Lees, M., and Sloane-Stanley, G. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
31. Storch, J., Zhou, Y. X., and Lagakos, W. S. (2008) Metabolism of apical versus basolateral sn-2-monoacylglycerol and fatty acids in rodent small intestine. J. Lipid Res. 49, 1762-1769
32. Chon, S.-H., Douglass, J. D., Zhou, Y. X., Malik, N., Dixon, J. L., Brinker, A., Quadro, L., and Storch, J. (2012) Over-expression of monoacylglycerol lipase (MGL) in small intestine alters endocannabinoid levels and whole body energy balance, resulting in obesity. PLoS One 7, e43962
33. Nishiumi, S., Bessyo, H., Kubo, M., Aoki, Y., Tanaka, A., Yoshida, K., and Ashida, H. (2010) Green and black teas suppress hyperglycemia and insulin resistance by retaining the expression of glucose transporter 4 in muscle of high fat diet-fed C57BL/6J mice. J. Agric. Food Chem. 58, 12916-12923
34. Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., and Turner, R. C. (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419
35. Chon, S.-H., Zhou, Y. X., Dixon, J. L., and Storch, J. (2007) Intestinal monoacylglycerol metabolism: developmental and nutritional regulation of monoacylglycerol lipase and monoacylglycerol acyltransferase. J. Biol. Chem. 282, 33346-33357
36. Newberry, E. P., Kennedy, S. M., Xie, Y., Luo, J., and Davidson, N. O. (2009) Diet-induced alterations in intestinal and extrahepatic lipid metabolism in liver fatty acid binding protein knockout mice. Mol. Cell. Biochem. 326, 79-86
37. Storch, J. (1993) Diversity of fatty acid-binding protein structure and function: studies with fluorescent ligands. Mol. Cell. Biochem. 123, 45-53
38. Storch, J., and Herr, F. M. (2001) in Nutrient-Gene Interactions in Health and Disease (Moustaid-Moussa, N., and Berdanier, C. D., eds) pp. 101-130, CRC Press, Boca Raton, FL
39. Cao, J., Hawkins, E., Brozinick, J., Liu, X., Zhang, H., Burn, P., and Shi, Y. (2004) 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. 279, 18878-18886
40. Hostetler, H. A., McIntosh, A. L., Atshaves, B. P., Storey, S. M., Payne, H. R., Kier, A. B., and Schroeder, F. (2009) L-FABP directly interacts with PPARα in cultured primary hepatocytes. J. Lipid Res. 50, 1663-1675
41. Kaczocha, M., Glaser, S. T., and Deutsch, D. G. (2009) Identification of intracellular carriers for the endocannabinoid anandamide. Proc. Natl. Acad. Sci. U.S.A. 106, 6375-6380
42. Kaczocha, M., Vivieca, S., Sun, J., Glaser, S. T., and Deutsch, D. G. (2012) Fatty acid-binding proteins transport N-acylethanolamines to nuclear receptors and are targets of endocannabinoid transport inhibitors. J. Biol. Chem. 287, 3415-3424
43. Fu, J., Gaetani, S., Oveisi, F., Lo Verme, J., Serrano, A., Rodríguez De Fonseca, F., Rosengarth, A., Luecke, H., Di Giacomo, B., Tarzia, G., and Piomelli, D. (2003) Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-α. Nature 425, 90-93
44. Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., and Piomelli, D. (2005) The nuclear receptor peroxisome proliferator- activated receptor-α mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19
45. Labonté, E. D., Li, Q., Kay, C. M., and Agellon, L. B. (2003) The relative ligand binding preference of the murine ileal lipid binding protein. Protein Expr. Purif. 28, 25-33
46. Sacchettini, J. C., Hauft, S. M., Van Camp, S. L., Cistola, D. P., and Gordon, J. I. (1990) Developmental and structural studies of an intracellular lipid binding protein expressed in the ileal epithelium. J. Biol. Chem. 265, 19199-19207
47. Storch, J., and Corsico, B. (2008) The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu. Rev. Nutr. 28, 73-95
48. Richieri, G. V., Ogata, R. T., Zimmerman, A. W., Veerkamp, J. H., and Kleinfeld, A. M. (2000) Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions. Biochemistry 39, 7197-7204
49. Martin, G. G., Atshaves, B. P., McIntosh, A. L., Mackie, J. T., Kier, A. B., and Schroeder, F. (2008) Liver fatty acid-binding protein gene-ablated female mice exhibit increased age-dependent obesity. J. Nutr. 138, 1859-1865
50. Newberry, E. P., Kennedy, S. M., Xie, Y., Sternard, B. T., Luo, J., and Davidson, N. O. (2008) Diet-induced obesity and hepatic steatosis in LFabp/ mice is abrogated with SF, but not PUFA, feeding and attenuated after cholesterol supplementation. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G307-G314
51. Atshaves, B. P., McIntosh, A. M., Lyuksyutova, O. I., Zipfel, W., Webb, W. W., and Schroeder, F. (2004) Liver fatty acid-binding protein gene ablation inhibits branched chain fatty acid metabolism in cultured primary hepatocytes. J. Biol. Chem. 279, 30954-30965
52. Xie, Y., Newberry, E. P., Kennedy, S. M., Luo, J., and Davidson, N. O. (2009) Increased susceptibility to diet-induced gallstones in liver fatty acid binding protein knockout mice. J. Lipid Res. 50, 977-987
53. Stubbins, R. E., Holcomb, V. B., Hong, J., and Núñez, N. P. (2012) Estrogen modulates abdominal adiposity and protects female mice from obesity and impaired glucose tolerance. Eur. J. Nutr. 51, 861-870
54. Stubbins, R. E., Najjar, K., Holcomb, V. B., Hong, J., and Núñez, N. P. (2012) Oestrogen alters adipocyte biology and protects female mice from adipocyte inflammation and insulin resistance. Diabetes Obes. Metab. 14, 58-66
55. Bass, N. M., Manning, J. A, Ockner, R. K., Gordon, J. I., Seetharam, S., and Alpers, D. H. (1985) Regulation of the biosynthesis of two distinct fatty acid-binding proteins in rat liver and intestine. Influences of sex difference and of clofibrate. J. Biol. Chem. 260, 1432-1436
56. Bach, A. C., Ingenbleek, Y., and Frey, A. (1996) The usefulness of dietary medium chain triglycerides in body weight control: fact or fancy? J. Lipid Res. 37, 708-726
57. Omar, B., Pacini, G., and Ahrén, B. (2012) Differential development of glucose intolerance and pancreatic islet adaptation in multiple diet induced obesity models. Nutrients 4, 1367-1381
58. Buettner, R., Parhofer, K. G., Woenckhaus, M., Wrede, C. E., Kunz- Schughart, L. A., Schölmerich, J., and Bollheimer, L. C. (2006) Defining high fat-diet rat models: metabolic and molecular effects of different fat types. J. Mol. Endocrinol. 36, 485-501
59. Papamandjaris, A. A., MacDougall, D. E., and Jones, P. J. (1998) Medium chain fatty acid metabolism and energy expenditure: obesity treatment implications. Life Sci. 62, 1203-1215
60. Atshaves, B. P., Martin, G. G., Hostetler, H. A., McIntosh, A. L., Kier, A. B., and Schroeder, F. (2010) Liver fatty acid-binding protein and obesity. J. Nutr. Biochem. 21, 1015-1032
61. Kahn, C. R., Bezy, O., Usar, S., Griffin, N. W., and Gordon, J. I. (2013) Keystone Symposia: Diabetes-New Insights into Mechanisms of Disease and its Treatment p. 42, Keystone Symposia, Keystone, CO
62. Agellon, L. B., Li, L., Luong, L., and Uwiera, R. R. (2006) Adaptations to the loss of intestinal fatty acid binding protein in mice. Mol. Cell. Biochem. 284, 159-166
63. Sugiyama, M. G., Hobson, L., Agellon, A. B., and Agellon, L. B. (2012) Visualization of sex-dimorphic changes in the intestinal transcriptome of Fabp2 gene-ablated mice. J. Nutrigenet. Nutrigenomics 5, 45-55
64. Krempler, F., Hell, E., Winkler, C., Breban, D., and Patsch, W. (1998) Plasma leptin levels: Interaction of obesity with a common variant of insulin receptor substrate-1. Arterioscler. Thromb. Vasc. Biol. 18, 1686-1690
65. Considine, R. V., Sinha, M. K., Heiman, M. L., Kriauciunas, A., Stephens, T. W., Nyce, M. R., Ohannesian, J. P., Marco, C. C., McKee, L. J., and Bauer, T. L. (1996) Serum immunoreactive-leptin concentrations in normalweight and obese humans. N. Engl. J. Med. 334, 292-295
66. Van Heek, M., Compton, D. S., France, C. F., Tedesco, R. P., Fawzi, A. B., Graziano, M. P., Sybertz, E. J., Strader, C. D., and Davis, H. R., Jr. (1997) Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J. Clin. Invest. 99, 385-390
67. Neeli, I., Siddiqi, S. A, Siddiqi, S., Mahan, J., Lagakos, W. S., Binas, B., Gheyi, T., Storch, J., and Mansbach, C. M., 2nd (2007) Liver fatty acidbinding protein initiates budding of pre-chylomicron transport vesicles from intestinal endoplasmic reticulum. J. Biol. Chem. 282, 17974-17984
68. Siddiqi, S., Saleem, U., Abumrad, N. A, Davidson, N. O., Storch, J., Siddiqi, S. A, and Mansbach, C. M., 2nd (2010) A novel multiprotein complex is required to generate the prechylomicron transport vesicle from intestinal ER. J. Lipid Res. 51, 1918-1928
69. Douglass, J. D., Malik, N., Chon, S.-H., Wells, K., Zhou, Y. X., Choi, A. S., Joseph, L. B., and Storch, J. (2012) Intestinal mucosal triacylglycerol accumulation secondary to decreased lipid secretion in obese and high fat fed mice. Front. Physiol. 3, 25
70. Uchida, A., Whitsitt, M. C., Eustaquio, T., Slipchenko, M. N., Leary, J. F., Cheng, J.-X., and Buhman, K. K. (2012) Reduced triglyceride secretion in response to an acute dietary fat challenge in obese compared with lean mice. Front. Physiol. 3, 26
71. Gangl, A., and Ockner, R. K. (1975) Intestinal metabolism of plasma free fatty acids. Intracellular compartmentation and mechanisms of control. J. Clin. Invest. 55, 803-813
72. Praslickova, D., Torchia, E. C., Sugiyama, M. G., Magrane, E. J., Zwicker, B. L., Kolodzieyski, L., and Agellon, L. B. (2012) The ileal lipid binding protein is required for efficient absorption and transport of bile acids in the distal portion of the murine small intestine. PLoS One 7, e50810
73. Lambert, D. M., and Fowler, C. J. (2005) The endocannabinoid system: drug targets, lead compounds, and potential therapeutic applications. J. Med. Chem. 48, 5059-5087
74. Storr, M. A., and Sharkey, K. A. (2007) The endocannabinoid system and gut-brain signalling. Curr. Opin. Pharmacol. 7, 575-582
75. Di Marzo, V., and Matias, I. (2005) Endocannabinoid control of food intake and energy balance. Nat. Neurosci. 8, 585-589
76. Burdyga, G., Lal, S., Varro, A., Dimaline, R., Thompson, D. G., and Dockray, G. J. (2004) Expression of cannabinoid CB1 receptors by vagal afferent neurons is inhibited by cholecystokinin. J. Neurosci. 24, 2708-2715
77. Izzo, A. A., Piscitelli, F., Capasso, R., Aviello, G., Romano, B., Borrelli, F., Petrosino, S., and Di Marzo, V. (2009) Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding. Br. J. Pharmacol. 158, 451-461
78. DiPatrizio, N. V., Astarita, G., Schwartz, G., Li, X., and Piomelli, D. (2011) Endocannabinoid signal in the gut controls dietary fat intake. Proc. Natl. Acad. Sci. U.S.A. 108, 12904-12908
79. DiPatrizio, N. V., Joslin, A., Jung, K.-M., and Piomelli, D. (2013) Endocannabinoid signaling in the gut mediates preference for dietary unsaturated fats. FASEB J. 27, 2513-2520
80. Leamy, L. J., Kelly, S. A., Hua, K., and Pomp, D. (2012) Exercise and diet affect quantitative trait loci for body weight and composition traits in an advanced intercross population of mice. Physiol. Genomics 44, 1141-1153
81. Primeau, V., Coderre, L., Karelis, a D., Brochu, M., Lavoie, M.-E., Messier, V., Sladek, R., and Rabasa-Lhoret, R. (2011) Characterizing the profile of obese patients who are metabolically healthy. Int. J. Obes. 35, 971-981
82. Yen, C.-L., Cheong, M.-L., Grueter, C., Zhou, P., Moriwaki, J., Wong, J. S., Hubbard, B., Marmor, S., and Farese, R. V., Jr. (2009) Deficiency of the intestinal enzyme acyl CoA:monoacylglycerol acyltransferase-2 protects mice from metabolic disorders induced by high fat feeding. Nat. Med. 15, 442-446
83. Smith, S. J., Cases, S., Jensen, D. R., Chen, H. C., Sande, E., Tow, B., Sanan, D. A., Raber, J., Eckel, R. H., and Farese, R. V., Jr. (2000) Obesity resistance and multiple mechanisms of triglyceride synthesis in mice lacking Dgat. Nat. Genetics 25, 87-90
84. Chen, H. C., Ladha, Z., Smith, S. J., and Farese, R. V. (2003) Analysis of energy expenditure at different ambient temperatures in mice lacking DGAT1. Am. J. Physiol. Endocrinol. Metab. 284, E213-E218