Adipose tissue-related proteins locally associated with resolution of inflammation in obese mice

International Journal of Obesity

Volumn 38, Issue 2, 2014, Pages 216-223

  Jilkova, Z M ^a   Hensler, M ^a   Medrikova, D ^a   Janovska, P ^a   Horakova, O ^a   Rossmeisl, M ^a   Flachs, P ^a   Sell, H ^b   Eckel, J ^b   Kopecky, J ^a  

^a INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^b LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

Author keywords

docosahexaenoic acid; eicosapentaenoic acid; endoglin; interleukin 1 receptor antagonist; macrophage inflammatory protein 1g; vascular cell adhesion molecule 1

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; CHOLESTEROL; DOCOSAHEXAENOIC ACID; ENDOGLIN; GLUCOSE; ICOSAPENTAENOIC ACID; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; LEPTIN; MACROPHAGE INFLAMMATORY PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 1GAMMA; OMEGA 3 FATTY ACID; ROSIGLITAZONE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDIDYMIS FAT; FAT MASS; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HYPOLIPEMIA; INFLAMMATION; LIPID STORAGE; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING; WHITE ADIPOSE TISSUE;

MUS; ZEA MAYS;

ADIPOCYTES; ADIPOKINES; ADIPOSE TISSUE, WHITE; ANIMALS; DIET, HIGH-FAT; DIETARY FATS; DOCOSAHEXAENOIC ACIDS; ENERGY METABOLISM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY ACIDS, OMEGA-3; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; REAL-TIME POLYMERASE CHAIN REACTION; THIAZOLIDINEDIONES;

EID: 84896735055     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.108     Document Type: Article

References (49)

1. Dalmas E, Clement K, Guerre-Millo M. Defining macrophage phenotype and function in adipose tissue. Trends Immunol 2011; 32: 307-314
2. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011; 121: 2111-2117
3. Sell H, Habich Ch, Eckel J. Adaptive immunity in obesity and insulin resistance. Nat Rev Endocrinol 2012; 8: 709-716
4. Recchiuti A, Serhan CN. Pro-resolving lipid mediators (SPMs) and their actions in regulating miRNA in novel resolution circuits in inflammation. Front Immunol 2012; 3: 298
5. Huber J, Loffler M, Bilban M, Reimers M, Kadl A, Todoric J et al. Prevention of highfat diet-induced adipose tissue remodeling in obese diabetic mice by n-3 polyunsaturated fatty acids. Int J Obes (Lond) 2007; 31: 1004-1013
6. Flachs P, Ruhl R, Hensler M, Janovská P, Zouhar P, Kus V et al. Synergistic induction of lipid catabolism and anti-inflammatory lipids in white fat of dietary obese mice in response to calorie restriction and n-3 fatty acids. Diabetologia 2011; 10: 2626-2638
7. Itariu BK, Zeyda M, Hochbrugger EE, Neuhofer A, Prager G, Schindler K et al. Long-chain n-3 PUFAs reduce adipose tissue and systemic inflammation in severely obese nondiabetic patients: A randomized controlled trial. Am J Clin Nutr 2012; 96/5: 1137-1149
8. Ruxton CH, Reed SC, Simpson MJ, Millington KJ. The health benefits of omega-3 polyunsaturated fatty acids: A review of the evidence. J Hum Nutr Diet 2007; 17/5: 449-459
9. Flachs P, Rossmeisl M, Bryhn M, Kopecky J. Cellular and molecular effects of n-3 polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci 2009; 116: 1-16
10. Flachs P, Horakova O, Brauner P, Rossmeisl M, Pecina P, Franssen-van Hal NL et al. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 2005; 48: 2365-2375
11. Kuda O, Jelenik T, Jilkova Z, Flachs P, Rossmeisl M, Hensler M et al. n-3 Fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet. Diabetologia 2009; 52: 941-951
12. Sato A, Kawano H, Notsu T, Ohta M, Nakakuki M, Mizuguchi K et al. Antiobesity effect of eicosapentaenoic acid in high-fat/high-sucrose diet-induced obesity: Importance of hepatic lipogenesis. Diabetes 2010; 59: 2495-2504
13. Belzung F, Raclot T, Groscolas R. Fish oil n-3 fatty acids selectively limit the hypertrophy of abdominal fat depots in growing rats fed high-fat diets. Am J Physiol 1993; 264: R1111-R1118
14. Raclot T, Groscolas R, Langin D, Ferre P. Site-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. J Lipid Res 1997; 38/10: 1963-1972
15. Storlien LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, Pascoe WS. Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 1987; 237: 885-888
16. Neschen S, Morino K, Dong J, Wang-Fischer Y, Cline GW, Romanelli AJ et al. N-3 fatty acids preserve insulin sensitivity in vivo in a PPAR{alpha}-dependent manner. Diabetes 2007; 56: 1034-1041
17. Jucker BM, Cline GW, Barucci N, Shulman GI. Differential effects of safflower oil versus fish oil feeding on insulin-stimulated glycogen synthesis, glycolysis, and pyruvate dehydrogenase flux in skeletal muscle: A 13C nuclear magnetic resonance study. Diabetes 1999; 48: 134-140
18. Kus V, Flachs P, Kuda O, Bardova K, Janovska P, Svobodova M et al. Unmasking differential effects of rosiglitazone and pioglitazone in the combination treatment with n-3 fatty acids in mice fed a high-fat diet. PLoS One 2011; 6: E27126-e27127
19. Groeger AL, Cipollina C, Cole MP, Woodcock SR, Bonacci G, Rudolph TK et al. Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat Chem Biol 2010; 6: 433-411
20. Tsuchida A, Yamauchi T, Takekawa S, Hada Y, Ito Y, Maki T et al. Peroxisome proliferator-Activated receptor (PPAR)alpha activation increases adiponectin receptors and reduces obesity-related inflammation in adipose tissue: Comparison of activation of PPARalpha, PPARgamma, and their combination. Diabetes 2005; 54/12: 3358-3370
21. Sugii S, Olson P, Sears DD, Saberi M, Atkins AR, Barish GD et al. PPARgamma activation in adipocytes is sufficient for systemic insulin sensitization. Proc Natl Acad Sci USA 2009; 106: 22504-22509
22. Flachs P, Mohamed-Ali V, Horakova O, Rossmeisl M, Hosseinzadeh-Attar MJ, Hensler M et al. Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed high-fat diet. Diabetologia 2006; 49/2: 394-397
23. Neschen S, Morino K, Rossbacher JC, Pongratz RL, Cline GW, Sono S et al. Fish oil regulates adiponectin secretion by a peroxisome proliferator-Activated receptorgamma-dependent mechanism in mice. Diabetes 2006; 55: 924-928
24. Kim H, Haluzik M, Gavrilova O, Yakar S, Portas J, Sun H et al. Thiazolidinediones improve insulin sensitivity in adipose tissue and reduce the hyperlipidaemia without affecting the hyperglycaemia in a transgenic model of type 2 diabetes. Diabetologia 2004; 47: 2215-2225
25. Wang P, Renes J, Bouwman F, Bunschoten A, Mariman E, Keijer J. Absence of an adipogenic effect of rosiglitazone on mature 3T3-L1 adipocytes: Increase of lipid catabolism and reduction of adipokine expression. Diabetologia 2007; 50: 654-665
26. Tilg H, Moschen AR. Adipocytokines: Mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 2006; 6: 772-783
27. Iwaki M, Matsuda M, Maeda N, Funahashi T, Matsuzawa Y, Makishima M et al. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 2003; 52: 1655-1663
28. Maury E, Brichard SM. Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 2010; 314: 1-16
29. Hung J, McQuillan BM, Thompson PL, Beilby JP. Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity. Int J Obes (Lond) 2008; 32: 772-779
30. Horakova O, Medrikova D, van Schothorst EM, Bunschoten A, Flachs P, Kus V et al. Preservation of metabolic flexibility in skeletal muscle by a combined use of n-3 PUFA and rosiglitazone in dietary obese mice. PLoS One 2012; 7: E43764
31. Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, Veck M et al. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 2005; 12: 1177-1185
32. Rossmeisl M, Macek JZ, Kuda O, Jelenik T, Medrikova D, Stankova B et al. Metabolic Effects of n-3 PUFA as phospholipids are superior to triglycerides in mice fed a high-fat diet: Possible role of endocannabinoids. PLoS One 2012; 7: E38834
33. Medrikova D, Macek JZ, Bardova K, Janovská P, Rossmeisl M, Kopecky J. Sex differences during the course of diet-induced obesity in mice: Adipose tissue expandability and glycemic control. Int J Obes (Lond) 2011; 2: 262-272
34. Dietze-Schroeder D, Sell H, Uhlig M, Koenen M, Eckel J. Autocrine action of adiponectin on human fat cells prevents the release of insulin resistance-inducing factors. Diabetes 2005; 54: 2003-2011
35. Baumruk F, Flachs P, Horakova M, Floryk D, Kopecky J. Transgenic UCP1 in white adipocytes modulates mitochondrial membrane potential. FEBS Lett 1999; 444: 206-210
36. Fujisaka S, Usui I, Bukhari A, Ikutani M, Oya T, Kanatani Y et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes 2009; 58: 2574-2582
37. Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the antiinflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004; 323: 630-635
38. Lawrence T, Gilroy DW, Colville-Nash PR, Willoughby DA. Possible new role for NF-kappaB in the resolution of inflammation. Nat Med 2001; 7: 1291-1297
39. Kim CS, Kawada T, Yoo H, Kwon BS, Yu R. Macrophage inflammatory proteinrelated protein-2, a novel CC chemokine, can regulate preadipocyte migration and adipocyte differentiation. FEBS Lett 2003; 548: 125-130
40. Nunez V, Alameda D, Rico D, Mota R, Gonzalo P, Cedenilla M et al. Retinoid X receptor alpha controls innate inflammatory responses through the up-regulation of chemokine expression. Proc Natl Acad Sci USA 2010; 107: 10626-10631
41. Surmi BK, Webb CD, Ristau AC, Hasty AH. Absence of macrophage inflammatory protein-1{alpha} does not impact macrophage accumulation in adipose tissue of diet-induced obese mice. Am J Physiol Endocrinol Metab 2010; 299/3: E437-E445
42. Hung SC, Chang CF, Ma HL, Chen TH, Low-Tone HL. Gene expression profiles of early adipogenesis in human mesenchymal stem cells. Gene 2004; 340: 141-150
43. Shockley KR, Rosen CJ, Churchill GA, Lecka-Czernik B. PPARgamma2 regulates a molecular signature of marrow mesenchymal stem cells. PPAR Res 2007; 2007: 81219
44. Xu F, Burk D, Gao Z, Yin J, Zhang X, Weng J et al. Angiogenic deficiency and adipose tissue dysfunction are associated with macrophage malfunction in SIRT1-/-mice. Endocrinology 2012; 153: 1706-1716
45. Goldberg RB. Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J Clin Endocrinol Metab 2009; 94: 3171-3182
46. Bosanska L, Michalsky D, Lacinova Z, Dostalova I, Bartlova M, Haluzikova D et al. The influence of obesity and different fat depots on adipose tissue gene expression and protein levels of cell adhesion molecules. Physiol Res 2010; 59: 79-88
47. Meier CA, Bobbioni E, Gabay C, Assimacopoulos-Jeannet F, Golay A, Dayer JM. IL-1 receptor antagonist serum levels are increased in human obesity: A possible link to the resistance to leptin? J Clin Endocrinol Metab 2002; 87/3: 1184-1188
48. Cartier A, Bergeron J, Poirier P, Almeras N, Tremblay A, Lemieux I et al. Increased plasma interleukin-1 receptor antagonist levels in men with visceral obesity. Ann Med 2009; 41: 471-478
49. Juge-Aubry CE, Somm E, Giusti V, Pernin A, Chicheportiche R, Verdumo C et al. Adipose tissue is a major source of interleukin-1 receptor antagonist: Upregulation in obesity and inflammation. Diabetes 2003; 52: 1104-1110