Short term palmitate supply impairs intestinal insulin signaling via ceramide production

Journal of Biological Chemistry

Volumn 291, Issue 31, 2016, Pages 16328-16338

  Tran, Thi Thu Trang ^a   Postal, Bárbara Graziela ^a   Demignot, Sylvie ^a   Ribeiro, Agnès ^a   Osinski, Céline ^a   De Barros, Jean Paul Pais ^b   Blachnio Zabielska, Agnieszka ^c   Leturque, Armelle ^a   Rousset, Monique ^a   Ferré, Pascal ^d   Hajduch, Eric ^d   Carrière, Véronique ^a  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; CERAMIDES; FATTY ACIDS; INSULIN; MAMMALS; MONOUNSATURATED FATTY ACIDS; OIL SHALE; OLIVE OIL; PALM OIL; PROTEINS; SATURATED FATTY ACIDS;

AKT PHOSPHORYLATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SIGNALING; INTESTINAL CELLS; METABOLIC DISEASE; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEINS; PROTEIN PHOSPHATASE;

PALMITIC ACID;

APOLIPOPROTEIN B48; CERAMIDE; INSULIN; MESSENGER RNA; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; MONOUNSATURATED FATTY ACID; OLIVE OIL; PALM OIL; PALMITIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE B; PROTEIN KINASE C; SATURATED FATTY ACID; TRIACYLGLYCEROL; VEGETABLE OIL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE CELL; INTESTINE EPITHELIUM CELL; LIPID ABSORPTION; LIPOGENESIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BIOSYNTHESIS; CACO-2 CELL LINE; DRUG EFFECTS; INTESTINE; METABOLISM; PHOSPHORYLATION;

ANIMALS; CACO-2 CELLS; CERAMIDES; ENTEROCYTES; HUMANS; INSULIN; INTESTINES; MICE; PALMITIC ACID; PHOSPHORYLATION; PLANT OILS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84979783988     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.709626     Document Type: Article

References (52)

1. Bansal, S., Buring, J. E., Rifai, N., Mora, S., Sacks, F. M., and Ridker, P. M. (2007) Fasting compared with nonfasting triglycerides and risk of cardiovascular events in women. JAMA 298, 309-316
2. Nordestgaard, B. G., Benn, M., Schnohr, P., and Tybjaerg-Hansen, A. (2007) Nonfasting triglycerides and risk of myocardial infarction, ischemic heart disease, and death in men and women. JAMA 298, 299-308
3. Duez, H., Pavlic, M., and Lewis, G. F. (2008) Mechanism of intestinal lipoprotein overproduction in insulin resistant humans. Atherosclerosis 9, 33-38
4. Phillips, C., Madigan, C., Owens, D., Collins, P., and Tomkin, G. H. (2002) Defective chylomicron synthesis as a cause of delayed particle clearance in diabetes? Int. J. Exp. Diabetes Res. 3, 171-178
5. Adeli, K., and Lewis, G. F. (2008) Intestinal lipoprotein overproduction in insulin-resistant states. Curr. Opin. Lipidol. 19, 221-228
6. Hussain, M. M., Nijstad, N., and Franceschini, L. (2011) Regulation of microsomal triglyceride transfer protein. Clin. Lipidol. 6, 293-303
7. Hooper, A. J., Burnett, J. R., and Watts, G. F. (2015) Contemporary aspects of the biology and therapeutic regulation of the microsomal triglyceride transfer protein. Circ. Res. 116, 193-205
8. Allister, E. M., Borradaile, N. M., Edwards, J. Y., and Huff, M. W. (2005) Inhibition of microsomal triglyceride transfer protein expression and apolipoprotein B100 secretion by the citrus flavonoid naringenin and by insulin involves activation of the mitogen-activated protein kinase pathway in hepatocytes. Diabetes 54, 1676-1683
9. Haas, M. E., Attie, A. D., and Biddinger, S. B. (2013) The regulation of ApoB metabolism by insulin. Trends Endocrinol. Metab. 24, 391-397
10. Lewis, G. F., Uffelman, K. D., Szeto, L. W., Weller, B., and Steiner, G. (1995) Interaction between free fatty acids and insulin in the acute control of very low density lipoprotein production in humans. J. Clin. Invest. 95, 158-166
11. Pavlic, M., Xiao, C., Szeto, L., Patterson, B. W., and Lewis, G. F. (2010) Insulin acutely inhibits intestinal lipoprotein secretion in humans in part by suppressing plasma free fatty acids. Diabetes 59, 580-587
12. Federico, L. M., Naples, M., Taylor, D., and Adeli, K. (2006) Intestinal insulin resistance and aberrant production of apolipoprotein B48 lipoproteins in an animal model of insulin resistance and metabolic dyslipidemia: evidence for activation of protein tyrosine phosphatase-1B, extracellular signal-related kinase, and sterol regulatory element-binding protein-1c in the fructose-fed hamster intestine. Diabetes 55, 1316-1326
13. Haidari, M., Leung, N., Mahbub, F., Uffelman, K. D., Kohen-Avramoglu, R., Lewis, G. F., and Adeli, K. (2002) Fasting and postprandial overproduction of intestinally derived lipoproteins in an animal model of insulin resistance. Evidence that chronic fructose feeding in the hamster is accompanied by enhanced intestinal de novo lipogenesis and ApoB48-containing lipoprotein overproduction. J. Biol. Chem. 277, 31646-31655
14. Qin, B., Qiu, W., Avramoglu, R. K., and Adeli, K. (2007) Tumor necrosis factor-α induces intestinal insulin resistance and stimulates the overproduction of intestinal apolipoprotein B48-containing lipoproteins. Diabetes 56, 450-461
15. Leung, N., Naples, M., Uffelman, K., Szeto, L., Adeli, K., and Lewis, G. F. (2004) Rosiglitazone improves intestinal lipoprotein overproduction in the fat-fed Syrian Golden hamster, an animal model of nutritionally-induced insulin resistance. Atherosclerosis 174, 235-241
16. Duez, H., Lamarche, B., Uffelman, K. D., Valero, R., Cohn, J. S., and Lewis, G. F. (2006) Hyperinsulinemia is associated with increased production rate of intestinal apolipoprotein B-48-containing lipoproteins in humans. Arterioscler. Thromb. Vasc. Biol. 26, 1357-1363
17. Nogueira, J.-P., Maraninchi, M., Béliard, S., Padilla, N., Duvillard, L., Mancini, J., Nicolay, A., Xiao, C., Vialettes, B., Lewis, G. F., and Valéro, R. (2012) Absence of acute inhibitory effect of insulin on chylomicron production in type 2 diabetes. Arterioscler. Thromb. Vasc. Biol. 32, 1039-1044
18. Larsen, P. J., and Tennagels, N. (2014) On ceramides, other sphingolipids and impaired glucose homeostasis. Mol. Metab. 3, 252-260
19. Holland, W. L., and Summers, S. A. (2008) Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr. Rev. 29, 381-402
20. Chavez, J. A., and Summers, S. A. (2012) A ceramide-centric view of insulin resistance. Cell Metab. 15, 585-594
21. Hage Hassan, R., Bourron, O., and Hajduch, E. (2014) Defect of insulin signal in peripheral tissues: important role of ceramide. World J. Diabetes 5, 244-257
22. Chateau, D., Pauquai, T., Delers, F., Rousset, M., Chambaz, J., and Demignot, S. (2005) Lipid micelles stimulate the secretion of triglyceride-enriched apolipoprotein B48-containing lipoproteins by Caco-2 cells. J. Cell. Physiol. 202, 767-776
23. Pauquai, T., Bouchoux, J., Chateau, D., Vidal, R., Rousset, M., Chambaz, J., and Demignot, S. (2006) Adaptation of enterocytic Caco-2 cells to glucose modulates triacylglycerol-rich lipoprotein secretion through triacylglycerol targeting into the endoplasmic reticulum lumen. Biochem. J. 395, 393-403
24. Frochot, V., Alqub, M., Cattin, A. L., Carrière, V., Houllier, A., Baraille, F., Barbot, L., Saint-Just, S., Ribeiro, A., Lacasa, M., Cardot, P., Chambaz, J., Rousset, M., and Lacorte, J. M. (2012) The transcription factor HNF-4α:a key factor of the intestinal uptake of fatty acids in mouse. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G1253-G1263
25. Hajduch, E., Alessi, D. R., Hemmings, B. A., and Hundal, H. S. (1998) Constitutive activation of protein kinase Bα by membrane targeting promotes glucose and system A amino acid transport, protein synthesis, and inactivation of glycogen synthase kinase 3 in L6 muscle cells. Diabetes 47, 1006-1013
26. Reis, A., Rudnitskaya, A., Blackburn, G. J., Mohd Fauzi, N., Pitt, A. R., and Spickett, C. M. (2013) A comparison of five lipid extraction solvent systems for lipidomic studies of human LDL. J. Lipid Res. 54, 1812-1824
27. Shimabukuro, M., Higa, M., Zhou, Y. T., Wang, M. Y., Newgard, C. B., and Unger, R. H. (1998) Lipoapoptosis in beta-cells of obese prediabetic fa/fa rats. Role of serine palmitoyltransferase overexpression. J. Biol. Chem. 273, 32487-32490
28. Hanada, K. (2003) Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta 1632, 16-30
29. Uchida, Y. (2014) Ceramide signaling in mammalian epidermis. Biochim. Biophys. Acta 1841, 453-462
30. Hajduch, E., Balendran, A., Batty, I. H., Litherland, G. J., Blair, A. S., Downes, C. P., and Hundal, H. S. (2001) Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells. Diabetologia 44, 173-183
31. Powell, D. J., Turban, S., Gray, A., Hajduch, E., and Hundal, H. S. (2004) Intracellular ceramide synthesis and protein kinase Cζ activation play an essential role in palmitate-induced insulin resistance in rat L6 skeletal muscle cells. Biochem. J. 382, 619-629
32. Blouin, C. M., Prado, C., Takane, K. K., Lasnier, F., Garcia-Ocana, A., Ferré, P., Dugail, I., and Hajduch, E. (2010) Plasma membrane subdomain compartmentalization contributes to distinct mechanisms of ceramide action on insulin signaling. Diabetes 59, 600-610
33. van Greevenbroek, M. M., van Meer, G., Erkelens, D. W., and de Bruin, T. W. (1996) Effects of saturated, mono-, and polyunsaturated fatty acids on the secretion of apo B containing lipoproteins by Caco-2 cells. Atherosclerosis 121, 139-150
34. Mathur, S. N., Born, E., Murthy, S., and Field, F. J. (1997) Microsomal triglyceride transfer protein in CaCo-2 cells: characterization and regulation. J. Lipid Res. 38, 61-67
35. Marandi, S., De Keyser, N., Saliez, A., Maernoudt, A. S., Sokal, E. M., Stilmant, C., Rider, M. H., and Buts, J. P. (2001) Insulin signal transduction in rat small intestine: role of MAP kinases in expression of mucosal hydrolases. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G229-G240
36. Loirdighi, N., Ménard, D., and Levy, E. (1992) Insulin decreases chylomicron production in human fetal small intestine. Biochim. Biophys. Acta 1175, 100-106
37. Levy, E., Sinnett, D., Thibault, L., Nguyen, T. D., Delvin, E., and Ménard, D. (1996) Insulin modulation of newly synthesized apolipoproteins B-100 and B-48 in human fetal intestine: gene expression and mRNA editing are not involved. FEBS Lett. 393, 253-258
38. Dash, S., Xiao, C., Morgantini, C., and Lewis, G. F. (2015) New insights into the regulation of chylomicron production. Annu. Rev. Nutr. 35, 265-294
39. Veilleux, A., Grenier, E., Marceau, P., Carpentier, A. C., Richard, D., and Levy, E. (2014) Intestinal lipid handling: evidence and implication of insulin signaling abnormalities in human obese subjects. Arterioscler. Thromb. Vasc. Biol. 34, 644-653
40. Padilla, N., Maraninchi, M., Béliard, S., Berthet, B., Nogueira, J.-P., Wolff, E., Nicolay, A., Bégu, A., Dubois, N., Grangeot, R., Mattei, C., Vialettes, B., Xiao, C., Lewis, G. F., and Valéro, R. (2014) Effects of bariatric surgery on hepatic and intestinal lipoprotein particle metabolism in obese, nondiabetic humans. Arterioscler. Thromb. Vasc. Biol. 34, 2330-2337
41. Hsieh, J., Hayashi, A. A., Webb, J., and Adeli, K. (2008) Postprandial dyslipidemia in insulin resistance: mechanisms and role of intestinal insulin sensitivity. Atherosclerosis 9, 7-13
42. Potten, C. S. (1998) Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 821-830
43. Castro, B. M., Prieto, M., and Silva, L. C. (2014) Ceramide: a simple sphingolipid with unique biophysical properties. Prog. Lipid Res. 54, 53-67
44. Guo, S. (2014) Insulin signaling, resistance, and the metabolic syndrome: insights from mouse models into disease mechanisms. J. Endocrinol. 220, T1-T23
45. Haus, J. M., Kashyap, S. R., Kasumov, T., Zhang, R., Kelly, K. R., Defronzo, R. A., and Kirwan, J. P. (2009) Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance. Diabetes 58, 337-343
46. de Mello, V. D., Lankinen, M., Schwab, U., Kolehmainen, M., Lehto, S., Seppänen-Laakso, T., Oresic, M., Pulkkinen, L., Uusitupa, M., and Erkkilä, A. T. (2009) Link between plasma ceramides, inflammation and insulin resistance: association with serum IL-6 concentration in patients with coronary heart disease. Diabetologia 52, 2612-2615
47. Boon, J., Hoy, A. J., Stark, R., Brown, R. D., Meex, R. C., Henstridge, D. C., Schenk, S., Meikle, P. J., Horowitz, J. F., Kingwell, B. A., Bruce, C. R., and Watt, M. J. (2013) Ceramides contained in LDL are elevated in type 2 diabetes and promote inflammation and skeletal muscle insulin resistance. Diabetes 62, 401-410
48. Huang, H., Kasumov, T., Gatmaitan, P., Heneghan, H. M., Kashyap, S. R., Schauer, P. R., Brethauer, S. A., and Kirwan, J. P. (2011) Gastric bypass surgery reduces plasma ceramide subspecies and improves insulin sensitivity in severely obese patients. Obesity 19:2235-2240
49. Ussher, J. R., Koves, T. R., Cadete, V. J., Zhang, L., Jaswal, J. S., Swyrd, S. J., Lopaschuk, D. G., Proctor, S. D., Keung, W., Muoio, D. M., and Lopaschuk, G. D. (2010) Inhibition of de novo ceramide synthesis reverses diet-induced insulin resistance and enhances whole-body oxygen consumption. Diabetes 59, 2453-2464
50. Holland, W. L., Brozinick, J. T., Wang, L.-P., Hawkins, E. D., Sargent, K. M., Liu, Y., Narra, K., Hoehn, K. L., Knotts, T. A., Siesky, A., Nelson, D. H., Karathanasis, S. K., Fontenot, G. K., Birnbaum, M. J., and Summers, S. A. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab. 5, 167-179
51. Hojjati, M. R., Li, Z., Zhou, H., Tang, S., Huan, C., Ooi, E., Lu, S., and Jiang, X.-C. (2005) Effect of myriocin on plasma sphingolipid metabolism and atherosclerosis in apoE-deficient mice. J. Biol. Chem. 280, 10284-10289
52. Ussher, J. R., Folmes, C. D., Keung, W., Fillmore, N., Jaswal, J. S., Cadete, V. J., Beker, D. L., Lam, V. H., Zhang, L., and Lopaschuk, G. D. (2012) Inhibition of serine palmitoyltransferase I reduces cardiac ceramide levels and increases glycolysis rates following diet-induced insulin resistance. PLoS One 7, e37703