Hepatic n-3 polyunsaturated fatty acid depletion promotes steatosis and insulin resistance in mice: Genomic analysis of cellular targets

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Pachikian, Barbara D ^a   Essaghir, Ahmed ^b   Demoulin, Jean Baptiste ^b   Neyrinck, Audrey M ^a   Catry, Emilie ^a   de Backer, Fabienne C ^a   Dejeans, Nicolas ^a   Dewulf, Evelyne M ^a   Sohet, Florence M ^a   Portois, Laurence ^c   Deldicque, Louise ^d   Molendi Coste, Olivier ^a   Leclercq, Isabelle A ^a   Francaux, Marc ^a   Carpentier, Yvon A ^c   Foufelle, Fabienne ^e   Muccioli, Giulio G ^a   Cani, Patrice D ^a   Delzenne, Nathalie M ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b DE DUVE INSTITUTE   (Belgium)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LIVER X RECEPTOR; OMEGA 3 FATTY ACID; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; CHOLESTEROL; ENDOCANNABINOID; MESSENGER RNA; ORPHAN NUCLEAR RECEPTOR; PHOSPHOLIPID; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL GENETICS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPLETION; DIETARY INTAKE; DISEASE ASSOCIATION; DISEASE COURSE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; FATTY ACID ANALYSIS; FATTY ACID DEPLETION; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FATTY LIVER; GENETIC ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; LIPID COMPOSITION; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIVER; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRESS; TARGET CELL; ANIMAL; BIOSYNTHESIS; DIET; DNA MICROARRAY; ENDOPLASMIC RETICULUM STRESS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; REPRODUCIBILITY;

MUS;

ANIMALS; CHOLESTEROL; DIET; ENDOCANNABINOIDS; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS, OMEGA-3; FATTY LIVER; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENOME; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORPHAN NUCLEAR RECEPTORS; OXIDATION-REDUCTION; PHOSPHOLIPIDS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIGLYCERIDES;

EID: 80051501874     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023365     Document Type: Article

References (63)

1. Clarke SD, (2001) Nonalcoholic steatosis and steatohepatitis. I. Molecular mechanism for polyunsaturated fatty acid regulation of gene transcription. Am J Physiol Gastrointest Liver Physiol 281: G865-G869.
2. Jump DB, (2008) N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Curr Opin Lipidol 19: 242-247.
3. Pawar A, Jump DB, (2003) Unsaturated fatty acid regulation of peroxisome proliferator-activated receptor alpha activity in rat primary hepatocytes. J Biol Chem 278: 35931-35939.
4. Schmitz G, Ecker J, (2008) The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res 47: 147-155.
5. Sekiya M, Yahagi N, Matsuzaka T, Najima Y, Nakakuki M, et al. (2003) Polyunsaturated fatty acids ameliorate hepatic steatosis in obese mice by SREBP-1 suppression. Hepatology 38: 1529-1539.
6. Xu J, Cho H, O'Malley S, Park JH, Clarke SD, (2002) Dietary polyunsaturated fats regulate rat liver sterol regulatory element binding proteins-1 and-2 in three distinct stages and by different mechanisms. J Nutr 132: 3333-3339.
7. Davidson MH, (2006) Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol 98: 27i-33i.
8. Appel LJ, Miller ER III, Seidler AJ, Whelton PK, (1993) Does supplementation of diet with 'fish oil' reduce blood pressure? A meta-analysis of controlled clinical trials. Arch Intern Med 153: 1429-1438.
9. Calder PC, (2006) Polyunsaturated fatty acids and inflammation. Prostaglandins Leukot Essent Fatty Acids 75: 197-202.
10. Delarue J, Li CH, Cohen R, Corporeau C, Simon B, (2006) Interaction of fish oil and a glucocorticoid on metabolic responses to an oral glucose load in healthy human subjects. Br J Nutr 95: 267-272.
11. Simopoulos AP, (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56: 365-379.
12. Simopoulos AP, (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med (Maywood) 233: 674-688.
13. Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, Webb M, Blendis L, et al. (2007) Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): a population based study. J Hepatol 47: 711-717.
14. Shapiro H, Tehilla M, ttal-Singer J, Bruck R, Luzzatti R, et al. (2011) The therapeutic potential of long-chain omega-3 fatty acids in nonalcoholic fatty liver disease. Clin Nutr 30: 6-19.
15. Araya J, Rodrigo R, Videla LA, Thielemann L, Orellana M, et al. (2004) Increase in long-chain polyunsaturated fatty acid n- 6/n- 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin Sci (Lond) 106: 635-643.
16. Elizondo A, Araya J, Rodrigo R, Poniachik J, Csendes A, et al. (2007) Polyunsaturated fatty acid pattern in liver and erythrocyte phospholipids from obese patients. Obesity (Silver Spring) 15: 24-31.
17. Louchami K, Zhang Y, Oguzhan B, Delporte C, Portois L, et al. (2006) Rapid changes in liver lipid composition and pancreatic islet K+ handling and secretory behaviour provoked by the intravenous administration of a medium-chain triglyceride: fish oil emulsion to long-chain polyunsaturated omega3 fatty acid-depleted rats. Int J Mol Med 18: 1047-1055.
18. Pachikian BD, Neyrinck AM, Cani PD, Portois L, Deldicque L, et al. (2008) Hepatic steatosis in n-3 fatty acid depleted mice: focus on metabolic alterations related to tissue fatty acid composition. BMC Physiol 8: 21.
19. Essaghir A, Toffalini F, Knoops L, Kallin A, van HJ, et al. (2010) Transcription factor regulation can be accurately predicted from the presence of target gene signatures in microarray gene expression data. Nucleic Acids Res 38: e120.
20. Ferre P, Foufelle F, (2007) SREBP-1c Transcription Factor and Lipid Homeostasis: Clinical Perspective. Horm Res 68: 72-82.
21. Raghow R, Yellaturu C, Deng X, Park EA, Elam MB, (2008) SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol Metab 19: 65-73.
22. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, et al. (2009) GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 119: 1201-1215.
23. Malaisse WJ, Bulur N, Zhang Y, Hacquebard M, Portois L, et al. (2009) The metabolic syndrome of omega3-depleted rats. I. Liver data. Int J Mol Med 24: 111-123.
24. Paton CM, Ntambi JM, (2009) Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab 297: E28-E37.
25. Deckelbaum RJ, Worgall TS, Seo T, (2006) n-3 fatty acids and gene expression. Am J Clin Nutr 83: 1520S-1525S.
26. Yellaturu CR, Deng X, Park EA, Raghow R, Elam MB, (2009) Insulin enhances the biogenesis of nuclear sterol regulatory element-binding protein (SREBP)-1c by posttranscriptional down-regulation of Insig-2A and its dissociation from SREBP cleavage-activating protein (SCAP).SREBP-1c complex. J Biol Chem 284: 31726-31734.
27. Schroder M, Kaufman RJ, (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789.
28. Malhi H, Kaufman RJ, (2010) Endoplasmic reticulum stress in liver disease. J Hepatol.
29. Werstuck GH, Lentz SR, Dayal S, Hossain GS, Sood SK, et al. (2001) Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest 107: 1263-1273.
30. Esfandiari F, Villanueva JA, Wong DH, French SW, Halsted CH, (2005) Chronic ethanol feeding and folate deficiency activate hepatic endoplasmic reticulum stress pathway in micropigs. Am J Physiol Gastrointest Liver Physiol 289: G54-G63.
31. Kammoun HL, Hainault I, Ferre P, Foufelle F, (2009) Nutritional related liver disease: targeting the endoplasmic reticulum stress. Curr Opin Clin Nutr Metab Care 12: 575-582.
32. Baranowski M, (2008) Biological role of liver X receptors. J Physiol Pharmacol 59 (Suppl 7): 31-55.
33. Chen G, Liang G, Ou J, Goldstein JL, Brown MS, (2004) Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc Natl Acad Sci U S A 101: 11245-11250.
34. Cagen LM, Deng X, Wilcox HG, Park EA, Raghow R, et al. (2005) Insulin activates the rat sterol-regulatory-element-binding protein 1c (SREBP-1c) promoter through the combinatorial actions of SREBP, LXR, Sp-1 and NF-Y cis-acting elements. Biochem J 385: 207-216.
35. Privalsky ML, (2004) The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol 66: 315-360.
36. Nakatani T, Katsumata A, Miura S, Kamei Y, Ezaki O, (2005) Effects of fish oil feeding and fasting on LXRalpha/RXRalpha binding to LXRE in the SREBP-1c promoter in mouse liver. Biochim Biophys Acta 1736: 77-86.
37. Pawar A, Botolin D, Mangelsdorf DJ, Jump DB, (2003) The role of liver X receptor-alpha in the fatty acid regulation of hepatic gene expression. J Biol Chem 278: 40736-40743.
38. Yoshikawa T, Shimano H, Yahagi N, Ide T, Memiya-Kudo M, et al. (2002) Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J Biol Chem 277: 1705-1711.
39. Howell G, III, Deng X, Yellaturu C, Park EA, Wilcox HG, et al. (2009) N-3 polyunsaturated fatty acids suppress insulin-induced SREBP-1c transcription via reduced trans-activating capacity of LXRalpha. Biochim Biophys Acta.
40. Ou J, Tu H, Shan B, Luk A, Bose-Boyd RA, et al. (2001) Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc Natl Acad Sci U S A 98: 6027-6032.
41. Fu X, Menke JG, Chen Y, Zhou G, MacNaul KL, et al. (2001) 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J Biol Chem 276: 38378-38387.
42. Wong J, Quinn CM, Brown AJ, (2007) Synthesis of the oxysterol, 24(S), 25-epoxycholesterol, parallels cholesterol production and may protect against cellular accumulation of newly-synthesized cholesterol. Lipids Health Dis 6: 10.
43. Li-Hawkins J, Lund EG, Turley SD, Russell DW, (2000) Disruption of the oxysterol 7alpha-hydroxylase gene in mice. J Biol Chem 275: 16536-16542.
44. Wada T, Kang HS, Angers M, Gong H, Bhatia S, et al. (2008) Identification of oxysterol 7alpha-hydroxylase (Cyp7b1) as a novel retinoid-related orphan receptor alpha (RORalpha) (NR1F1) target gene and a functional cross-talk between RORalpha and liver X receptor (NR1H3). Mol Pharmacol 73: 891-899.
45. Okazaki H, Goldstein JL, Brown MS, Liang G, (2010) LXR-SREBP-1c-phospholipid transfer protein axis controls very low density lipoprotein (VLDL) particle size. J Biol Chem 285: 6801-6810.
46. Watanabe S, Doshi M, Hamazaki T, (2003) n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice. Prostaglandins Leukot Essent Fatty Acids 69: 51-59.
47. Wang J, Ueda N, (2009) Biology of endocannabinoid synthesis system. Prostaglandins Other Lipid Mediat 89: 112-119.
48. Osei-Hyiaman D, DePetrillo M, Pacher P, Liu J, Radaeva S, et al. (2005) Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 115: 1298-1305.
49. Muccioli GG, Naslain D, Backhed F, Reigstad CS, Lambert DM, et al. (2010) The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol 6: 392.
50. Jeong WI, Osei-Hyiaman D, Park O, Liu J, Batkai S, et al. (2008) Paracrine activation of hepatic CB1 receptors by stellate cell-derived endocannabinoids mediates alcoholic fatty liver. Cell Metab 7: 227-235.
51. Postic C, Dentin R, Denechaud PD, Girard J, (2007) ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr 27: 179-192.
52. Dentin R, Benhamed F, Pegorier JP, Foufelle F, Viollet B, et al. (2005) Polyunsaturated fatty acids suppress glycolytic and lipogenic genes through the inhibition of ChREBP nuclear protein translocation. J Clin Invest 115: 2843-2854.
53. Dentin R, Denechaud PD, Benhamed F, Girard J, Postic C, (2006) Hepatic gene regulation by glucose and polyunsaturated fatty acids: a role for ChREBP. J Nutr 136: 1145-1149.
54. Pettinelli P, Del PT, Araya J, Rodrigo R, Araya AV, et al. (2009) Enhancement in liver SREBP-1c/PPAR-alpha ratio and steatosis in obese patients: correlations with insulin resistance and n-3 long-chain polyunsaturated fatty acid depletion. Biochim Biophys Acta 1792: 1080-1086.
55. Richelle M, Carpentier YA, Deckelbaum RJ, (1994) Long- and medium-chain triacylglycerols in neutral lipid-exchange processes with human plasma low-density lipoproteins. Biochemistry 33: 4872-4878.
56. Folch J, Lees M, Sloane Stanley GH, (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
57. Muccioli GG, Stella N, (2008) An optimized GC-MS method detects nanomolar amounts of anandamide in mouse brain. Anal Biochem 373: 220-228.
58. Muccioli GG, Xu C, Odah E, Cudaback E, Cisneros JA, et al. (2007) Identification of a novel endocannabinoid-hydrolyzing enzyme expressed by microglial cells. J Neurosci 27: 2883-2889.
59. Essaghir A, Dif N, Marbehant CY, Coffer PJ, Demoulin JB, (2009) The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J Biol Chem 284: 10334-10342.
60. Leja J, Essaghir A, Essand M, Wester K, Oberg K, et al. (2009) Novel markers for enterochromaffin cells and gastrointestinal neuroendocrine carcinomas. Mod Pathol 22: 261-272.
61. Neyrinck A, Eeckhoudt SL, Meunier CJ, Pampfer S, Taper HS, et al. (1999) Modulation of paracetamol metabolism by Kupffer cells: a study on rat liver slices. Life Sci 65: 2851-2859.
62. Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, et al. (2006) Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like Peptide 1 receptor. Diabetes 55: 1484-1490.
63. Lanthier N, Molendi-Coste O, Horsmans Y, van RN, Cani PD, et al. (2010) Kupffer cell activation is a causal factor for hepatic insulin resistance. Am J Physiol Gastrointest Liver Physiol 298: G107-G116.