PPARα -independent actions of omega-3 PUFAs contribute to their beneficial effects on adiposity and glucose homeostasis

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Liu, Menghan ^a,b,c   Montgomery, Magdalene K ^a,b   Fiveash, Corrine E ^b   Osborne, Brenna ^a   Cooney, Gregory J ^a,b   Bell Anderson, Kim ^c   Turner, Nigel ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FISH OIL; OMEGA 3 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA;

ADIPOSE TISSUE; ANIMAL; C57BL MOUSE; DIET SUPPLEMENTATION; DIET THERAPY; DOSE RESPONSE; DRUG EFFECTS; GLUCOSE INTOLERANCE; HOMEOSTASIS; MALE; METABOLISM; MOUSE; OBESITY; ORAL DRUG ADMINISTRATION; PHYSIOLOGY; TREATMENT OUTCOME;

ADIPOSE TISSUE; ADIPOSITY; ADMINISTRATION, ORAL; ANIMALS; DIETARY SUPPLEMENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FATTY ACIDS, OMEGA-3; FISH OILS; GLUCOSE INTOLERANCE; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; OBESITY; PPAR ALPHA; TREATMENT OUTCOME;

EID: 84903769624     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05538     Document Type: Article

References (54)

1. Kelly, T., Yang, W., Chen, C. S., Reynolds, K. & He, J. Global burden of obesity in 2005 and projections to 2030. Int. J. Obes. 32, 1431-1437 (2008).
2. Chen, L., Magliano, D. J. & Zimmet, P. Z. The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat. Rev. Endocrinol. 8, 228-236 (2012).
3. Savage, D. B., Petersen, K. F. & Shulman, G. I. Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol. Rev. 87, 507-520 (2007). (Pubitemid 47084679)
4. Samuel, V. T., Petersen, K. F. & Shulman, G. I. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277 (2010).
5. Storlien, L. H. et al. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes 40, 280-289 (1991).
6. Hill, J. O. et al. Lipid-accumulation and body-fat distribution is influenced by type of dietary-fat fed to rats. Int. J. Obes. 17, 223-236 (1993). (Pubitemid 23133353)
7. Ikemoto, S. et al. High-fat diet-induced hyperglycemia and obesity in mice: Differential effects of dietary oils. Metabolism 45, 1539-1546 (1996). (Pubitemid 26424584)
8. Turner, N. et al. Enhancement of muscle mitochondrial oxidative capacity and alterations in insulin action are lipid species dependent: potent tissue-specific effects of medium-chain fatty acids. Diabetes 58, 2547-2554 (2009).
9. Poudyal, H., Panchal, S. K., Diwan, V. & Brown, L. Omega-3 fatty acids and metabolic syndrome: Effects and emergingmechanisms of action. Prog. Lipid Res. 50, 372-387 (2011).
10. Buettner, R. et al. Defining high-fat-diet rat models: metabolic and molecular effects of different fat types. J. Mol. Endocrinol. 36, 485-501 (2006). (Pubitemid 43904942)
11. Levy, J. R., Clore, J. N. & Stevens, W. Dietary n-3 polyunsaturated fatty acids decrease hepatic triglycerides in Fischer 344 rats. Hepatology 39, 608-616 (2004). (Pubitemid 38337640)
12. Samane, S. et al. Fish oil and argan oil intake differently modulate insulin resistance and glucose intolerance in a rat model of dietary-induced obesity. Metabolism 58, 909-919 (2009).
13. Kim, J.-Y. et al. High-fat diet-induced muscle insulin resistance: relationship to visceral fat mass. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R2057-R2065 (2000).
14. Jelenik, T. et al. AMP-activated protein kinase a2 subunit Is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids. Diabetes 59, 2737-2746 (2010).
15. Storlien, L. H. et al. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 237, 885-888 (1987). (Pubitemid 17128276)
16. Fiamoncini, J. et al. Enhanced peroxisomal b-oxidation is associated with prevention of obesity and glucose intolerance by fish oil-enriched diets. Obesity 21, 1200-1207 (2013).
17. Rossmeisl, M. et al. Omega-3 phospholipids from fish suppress hepatic steatosis by integrated inhibition of biosynthetic pathways in dietary obese mice. Biochim. Biophys. Acta - Mol. Cell Biol. Lipid 1841, 267-278 (2014).
18. Kim, H.-J., Takahashi, M. & Ezaki, O. Fish oil feeding decreases mature sterol regulatory element-binding protein 1 (SREBP-1) by down-regulation of SREBP- 1c mRNA in mouse liver. J. Biol. Chem. 274, 25892-25898 (1999).
19. Neschen, S. et al. Contrasting effects of fish oil and safflower oil on hepatic peroxisomal and tissue lipid content. Am. J. Physiol. Endocrinol. Metab. 282, E395-E401 (2002). (Pubitemid 34654810)
20. Neschen, S. et al. n-3 Fatty acids preserve insulin sensitivity in vivo in a peroxisome proliferator-activated receptor-a-dependent manner. Diabetes 56, 1034-1041 (2007). (Pubitemid 46525082)
21. Ruiz-Gutiérrez, V., Pérez-Espinosa, A., Vázquez, C. M. & Santa-María, C. Effects of dietary fats (fish, olive and high-oleic-acid sunflower oils) on lipid composition and antioxidant enzymes in rat liver. Br. J. Nutr. 82, 233-241 (1999). (Pubitemid 29438392)
22. Jucker, B. M., Cline, G. W., Barucci, N. & Schulman, G. I. Differential effects of safflower oil versus fish oil feeding on insulin-stimulated glycogen synthesis, glycolysis, and pyruvate dehydrogenase flux in skeletal muscle: A (13 C) nuclear magnetic resonance study. Diabetes 48, 134-140 (1999). (Pubitemid 29019364)
23. Fedor, D. & Kelley, D. S. Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr. Opin. Clin. Nutr. Metab. Care 12, 138-146 (2009).
24. Ferré, P. The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity. Diabetes 53, S43-S50 (2004). (Pubitemid 38168692)
25. Wanders, R. J. A. Peroxisomes, lipid metabolism, and peroxisomal disorders. Mol. Genet. Metab. 83, 16-27 (2004). (Pubitemid 39311277)
26. Wanders, R. J. A. & Waterham, H. R. Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75, 295-332 (2006). (Pubitemid 44118035)
27. Neschen, S. et al. Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-c-dependent mechanism in mice. Diabetes 55, 924-928 (2006). (Pubitemid 44100165)
28. Oh, D. Y. et al. GPR120 is an Omega-3 atty acid receptor mediating potent antiinflammatory and insulin-sensitizing effects. Cell 142, 687-698 (2010).
29. White, P. J., Arita, M., Taguchi, R., Kang, J. X. & Marette, A. Transgenic restoration of long-chain n-3 fatty acids in insulin target tissues improves resolution capacity and alleviates obesity-linked inflammation and insulin resistance in high-fat-fed mice. Diabetes 59, 3066-3073 (2010).
30. Guerre-Millo, M. et al. Peroxisome proliferator-activated receptor a activators improve insulin sensitivity and reduce adiposity. J. Biol. Chem. 275, 16638-16642 (2000). (Pubitemid 30398891)
31. Ye, J.-M. et al. Peroxisome proliferator-activated receptor (PPAR)-a activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats. Diabetes 50, 411-417 (2001). (Pubitemid 32127300)
32. Ye, J.-M. et al. PPARa/c ragaglitazar eliminates fatty liver and enhances insulin action in fat-fed rats in the absence of hepatomegaly. Am. J. Physiol. Endocrinol. Metab. 284, E531-E540 (2003). (Pubitemid 36237541)
33. Chan, S. M. et al. Activation of PPARalpha ameliorates hepatic insulin resistance and steatosis in high fructose-fed mice despite increased endoplasmic reticulum stress. Diabetes 62, 2095-2105 (2013).
34. Guerre-Millo, M. et al. PPAR-a-null mice are protected from high-fat diet-induced insulin resistance. Diabetes 50, 2809-2814 (2001). (Pubitemid 33733132)
35. Tordjman, K. et al. PPARa deficiency reduces insulin resistance and atherosclerosis in apoE-null mice. J. Clin. Invest. 107, 1025-1034 (2001). (Pubitemid 32323412)
36. Finck, B. N. et al. A potential link between muscle peroxisome proliferatoractivated receptor-alpha signaling and obesity-related diabetes. Cell. Metab. 1, 133-144 (2005). (Pubitemid 43960595)
37. Finck, B. N. et al. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J. Clin. Invest. 109, 121-130 (2002). (Pubitemid 34052548)
38. Samuel, V. & Shulman, G. Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871 (2012).
39. Clarke, S. D. Polyunsaturated fatty acid regulation of gene transcription: a mechanism to improve energy balance and insulin resistance. Br. J. Nutr. 83, 59-66 (2000).
40. Mater, M. K., Thelen, A. P., Pan, D. A. & Jump, D. B. Sterol response elementbinding protein 1c (SREBP1c) is involved in the polyunsaturated fatty acid suppression of hepatic S14 gene transcription. J. Biol. Chem. 274, 32725-32732 (1999). (Pubitemid 129535302)
41. Ren, B., Thelen, A. P., Peters, J. M., Gonzalez, F. J. & Jump, D. B. Polyunsaturated fatty acid suppression of hepatic fatty acid synthase and S14 gene expression does not require peroxisome proliferator-activated receptor alpha. J. Biol. Chem. 272, 26827-26832 (1997). (Pubitemid 27452629)
42. Xu, J., Cho, H., O'Malley, S., Park, J. H. & Clarke, S. D. 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 (2002). (Pubitemid 35304240)
43. Oosterveer, M. H. et al. Fenofibrate simultaneously induces hepatic fatty acid oxidation, synthesis, and elongation in mice. J. Biol. Chem. 284, 34036-34044 (2009).
44. Knight, B. L. et al. A role for PPARalpha in the control of SREBP activity and lipid synthesis in the liver. Biochem. J. 389, 413-421 (2005). (Pubitemid 41021145)
45. Rakhshandehroo, M. et al. Comprehensive analysis of PPARalpha-dependent regulation of hepatic lipid metabolism by expression profiling. PPAR Res. 2007, 26839 (2007).
46. Lu, Y., Boekschoten, M. V., Wopereis, S., Müller, M. & Kersten, S. Comparative transcriptomic and metabolomic analysis of fenofibrate and fish oil treatments in mice. Physiol. Genomics 43, 1307-1318 (2011).
47. Baillie, R. A., Takada, R., Nakamura, M. & Clarke, S. D. Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostag. Leukotr. Ess. 60, 351-356 (1999). (Pubitemid 29401791)
48. de Lange, P. et al. Peroxisome proliferator-activated receptor delta: A conserved director of lipid homeostasis through regulation of the oxidative capacity of muscle. PPAR Res. 2008, 172676 (2008).
49. Wang, Y.-X. et al. Peroxisome-proliferator-activated receptor d activates fat metabolism to prevent obesity. Cell 113, 159-170 (2003). (Pubitemid 36514968)
50. Vasilakou, D. et al. Sodium-glucose cotransporter 2 inhibitors for type 2 diabetes: a systematic review and meta-analysis. Ann. Intern. Med. 159, 262-274 (2013).
51. Barnett, A. H. Impact of sodium glucose cotransporter 2 inhibitors on weight in patients with type 2 diabetes mellitus. Postgrad. Med. 125, 92-100 (2013).
52. Turner, N., Mitchell, T. W., Else, P. L. & Hulbert, A. J. The omega-3 and omega-6 fats in meals: a proposal for a simple new label. Nutrition 27, 719-726 (2011).
53. Montgomery, M. K. et al.Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia 56, 1129-1139 (2013).
54. Even, P. C. & Nadkarni, N. A. Indirect calorimetry in laboratory mice and rats: principles, practical considerations, interpretation and perspectives. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R459-476 (2012).