Modulation of adipose tissue inflammation by bioactive food compounds

Journal of Nutritional Biochemistry

Volumn 24, Issue 4, 2013, Pages 613-623

  Siriwardhana, Nalin ^a   Kalupahana, Nishan S ^b   Cekanova, Maria ^c   LeMieux, Monique ^a   Greer, Betty ^d   Moustaid Moussa, Naima ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b UNIVERSITY OF PERADENIYA   (Sri Lanka)

^c UNIVERSITY OF TENNESSEE   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Adipose tissue; Curcumin; Inflammation; Monounsaturated fatty acids; Obesity; Phytochemicals; Polyunsaturated fatty acids; Quercetin; Resveratrol; Tea polyphenols

Indexed keywords

ADENOSINE PHOSPHATE; ANTHOCYANIN; APIGENIN; CATECHIN; CONJUGATED LINOLEIC ACID; CURCUMIN; CYANIDIN 3 GLUCOSIDE; DOCOSAHEXAENOIC ACID; EPIGALLOCATECHIN GALLATE; FATTY ACID; FISETIN; FLAVANOL DERIVATIVE; FLAVANONE DERIVATIVE; HESPERETIN; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; ISOFLAVONE; ISORHAMNETIN; KAEMPFEROL; MITOGEN ACTIVATED PROTEIN KINASE; MONOUNSATURATED FATTY ACID; NARINGENIN; OLEIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; POLYPHENOL DERIVATIVE; QUERCETIN; RESVERATROL; THEAFLAVIN; TOLL LIKE RECEPTOR;

ADIPOSE TISSUE; ANTIINFLAMMATORY ACTIVITY; CALORIC INTAKE; DIETARY INTAKE; ENDOCRINE FUNCTION; FAT INTAKE; FRUIT; HUMAN; INSULIN RESISTANCE; METABOLIC DISORDER; OBESITY; REVIEW; VEGETABLE;

ADIPOSE TISSUE; CURCUMIN; ENDOCRINE GLANDS; FATTY ACIDS; FOOD; HUMANS; INFLAMMATION; INSULIN RESISTANCE; POLYPHENOLS; QUERCETIN; STILBENES;

EID: 84875078504     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.12.013     Document Type: Review

References (171)

1. Finkelstein E.A., Trogdon J.G., Cohen J.W., Dietz W. Annual medical spending attributable to obesity: payer- and service-specific estimates. Health Aff 2009, 28:W822-W831.
2. Tsai A.G., Williamson D.F., Glick H.A. Direct medical cost of overweight and obesity in the USA: a quantitative systematic review. Obes Rev 2011, 12:50-61.
3. Bray G.A. Medical consequences of obesity. J Clin Endocrinol Metab 2004, 89:2583-2589.
4. Kopelman P.G. Obesity as a medical problem. Nature 2000, 404:635-643.
5. Damcott C.M., Sack P., Shuldiner A.R. The genetics of obesity. Endocrinol Metab Clin North Am 2003, 32:761-786.
6. Arner E., Westermark P.O., Spalding K.L., Britton T., Rydén M., Frisén J., et al. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 2010, 59:105-109.
7. Kalupahana N.S., Moustaid-Moussa N., Claycombe K.J. Immunity as a link between obesity and insulin resistance. Mol Aspects Med 2012, 33:26-34.
8. Lolmède K., Duffaut C., Zakaroff-Girard A., Bouloumié A. Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab 2011, 37:283-290.
9. Tchoukalova Y.D., Votruba S.B., Tchkonia T., Giorgadze N., Kirkland J.L., Jensen M.D. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc Natl Acad Sci U S A 2010, 107:18226-18231.
10. Arner P. Regional differences in protein production by human adipose tissue. Biochem Soc Trans 2001, 29:72-75.
11. Kalupahana N.S., Claycombe K., Moustaid-Moussa N. (n-3) Fatty acids alleviate adipose tissue inflammation and insulin resistance: mechanistic insights 2011, Advances in, Nutrition.
12. Lumeng C.N., Bodzin J.L., Saltiel A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007, 117:175-184.
13. Odegaard J.I., Chawla A. Alternative macrophage activation and metabolism. Annu Rev Pathol 2011, 6:275-297.
14. Kershaw E.E., Flier J.S. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004, 89:2548-2556.
15. Ouchi N., Parker J.L., Lugus J.J., Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011, 11:85-97.
16. Vitseva O.I., Tanriverdi K., Tchkonia T.T., Kirkland J.L., McDonnell M.E., Apovian C.M., et al. Inducible Toll-like receptor and NF-kappaB regulatory pathway expression in human adipose tissue. Obesity (Silver Spring) 2008, 16:932-937.
17. Hsueh H.W., Zhou Z., Whelan J., Allen K.G., Moustaid-Moussa N., Kim H., et al. Stearidonic and eicosapentaenoic acids inhibit interleukin-6 expression in ob/ob mouse adipose stem cells via Toll-like receptor-2-mediated pathways. J Nutr 2011, 141:1260-1266.
18. Bost F., Aouadi M., Caron L., Binetruy B. The role of MAPKs in adipocyte differentiation and obesity. Biochimie 2005, 51-56.
19. Gauthier M.S., O'Brien E.L., Bigornia S., Mott M., Cacicedo J.M., Xu X.J., et al. Decreased AMP-activated protein kinase activity is associated with increased inflammation in visceral adipose tissue and with whole-body insulin resistance in morbidly obese humans. Biochem Biophys Res Commun 2011, 404:382-387.
20. Moller D.E., Berger J.P. Role of PPARs in the regulation of obesity-related insulin sensitivity and inflammation. Int J Obes Relat Metab Disord 2003, 27(Suppl 3):S17-S21.
21. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
22. Dandona P., Aljada A., Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 2004, 25:4-7.
23. Franks P.W. Obesity, inflammatory markers and cardiovascular disease: distinguishing causality from confounding. J Hum Hypertens 2006, 20:837-840.
24. Roth C.L., Kratz M., Ralston M.M., Reinehr T. Changes in adipose-derived inflammatory cytokines and chemokines after successful lifestyle intervention in obese children. Metabolism 2011, 60:445-452.
25. Galland L. Diet and inflammation. Nutr Clin Pract 2010, 25:634-640.
26. Djuric Z. The Mediterranean diet: effects on proteins that mediate fatty acid metabolism in the colon. Nutr Rev 2011, 69:730-744.
27. Rosa F.T., Zulet M.A., Marchini J.S., Martínez J.A. Bioactive compounds with effects on inflammation markers in humans. Int J Food Sci Nutr 2012, 63:749-765.
28. Higami Y., Barger J.L., Page G.P., Allison D.B., Smith S.R., Prolla T.A., et al. Energy restriction lowers the expression of genes linked to inflammation, the cytoskeleton, the extracellular matrix, and angiogenesis in mouse adipose tissue. J Nutr 2006, 136:343-352.
29. Larson-Meyer D.E., Heilbronn L.K., Redman L.M., Newcomer B.R., Frisard M.I., Anton S., et al. Effect of calorie restriction with or without exercise on insulin sensitivity, beta-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care 2006, 29:1337-1344.
30. Esfahani A., Wong J.M., Truan J., Villa C.R., Mirrahimi A., Srichaikul K., et al. Health effects of mixed fruit and vegetable concentrates: a systematic review of the clinical interventions. J Am Coll Nutr 2011, 30:285-294.
31. U.S. Department of Agriculture and U.S. Department of Health and Human Services Dietary Guidelines for Americans 2010, U.S. Government Printing Office, Washington, DC, December 2010) Available from:. http://www.cnpp.usda.gov/Publications/DietaryGuidelines/2010/PolicyDoc/PolicyDoc.pdf, 7th ed.
32. Fantuzzi G. Adiponectin and inflammation: consensus and controversy. J Allergy Clin Immunol 2008, 121:326-330.
33. Décordé K., Teissèdre P.L., Sutra T., Ventura E., Cristol J.P., Rouanet J.M. Chardonnay grape seed procyanidin extract supplementation prevents high-fat diet-induced obesity in hamsters by improving adipokine imbalance and oxidative stress markers. Mol Nutr Food Res 2009, 53:659-666.
34. Link A., Balaguer F., Goel A. Cancer chemoprevention by dietary polyphenols: promising role for epigenetics. Biochem Pharmacol 2010, 80:1771-1792.
35. Bakker G.C., van Erk M.J., Pellis L., Wopereis S., Rubingh C.M., Cnubben N.H., et al. An antiinflammatory dietary mix modulates inflammation and oxidative and metabolic stress in overweight men: a nutrigenomics approach. Am J Clin Nutr 2010, 91:1044-1059.
36. Weisberg S.P., Leibel R., Tortoriello D.V. Dietary curcumin significantly improves obesity-associated inflammation and diabetes in mouse models of diabesity. Endocrinology 2008, 149:3549-3558.
37. Shishodia S., Sethi G., Aggarwal B.B. Curcumin: getting back to the roots. Ann N Y Acad Sci 2005, 1056:206-217.
38. Yekollu S.K., Thomas R., O'Sullivan B. Targeting curcusomes to inflammatory dendritic cells inhibits NF-kappaB and improves insulin resistance in obese mice. Diabetes 2011, 60:2928-2938.
39. Cheng A.L., Hsu C.H., Lin J.K., Hsu M.M., Ho Y.F., Shen T.S., et al. Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res 2001, 21:2895-2900.
40. Sharma R.A., Euden S.A., Platton S.L., Cooke D.N., Shafayat A., Hewitt H.R., et al. Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res 2004, 10:6847-6854.
41. Vermorken A.J., Zhu J., VAN DE Ven W.J., Cui Y., Fryns J.P. Curcumin for the prevention of progression in monoclonal gammopathy of undetermined significance: a word of caution. Exp Ther Med 2010, 2:265-269.
42. Shoba G., Joy D., Joseph T., Majeed M., Rajendran R., Srinivas P.S. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med 1998, 64:353-356.
43. Ahn J., Lee H., Kim S., Ha T. Curcumin-induced suppression of adipogenic differentiation is accompanied by activation of Wnt/beta-catenin signaling. Am J Physiol Cell Physiol 2010, C1510-C1516.
44. Ejaz A., Wu D., Kwan P., Meydani M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr 2009, 139:919-925.
45. Nishiyama T., Mae T., Kishida H., Tsukagawa M., Mimaki Y., Kuroda M., et al. Curcuminoids and sesquiterpenoids in turmeric (Curcuma longa L.) suppress an increase in blood glucose level in type 2 diabetic KK-A(y) mice. Journal of Agricultural and Food Chem 2005, 53:959-963.
46. Gonzales A.M., Orlando R.A. Curcumin and resveratrol inhibit nuclear factor-kappaB-mediated cytokine expression in adipocytes. Nutr Metab (Lond) 2008, 5:17.
47. Frémont L. Biological effects of resveratrol. Life Sci 2000, 66:663-673.
48. Moreno-Labanda J.F., Mallavia R., Pérez-Fons L., Lizama V., Saura D., Micol V. Determination of piceid and resveratrol in Spanish wines deriving from Monastrell (Vitis vinifera L.) grape variety. J Agric Food Chem 2004, 52:5396-5403.
49. Walle T., Hsieh F., DeLegge M.H., Oatis J.E., Walle U.K. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos 2004, 32:1377-1382.
50. Goldberg D.M., Yan J., Soleas G.J. Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin Biochem 2003, 36:79-87.
51. Vitaglione P., Sforza S., Galaverna G., Ghidini C., Caporaso N., Vescovi P.P., et al. Bioavailability of trans-resveratrol from red wine in humans. Mol Nutr Food Res 2005, 49:495-504.
52. Olholm J., Paulsen S.K., Cullberg K.B., Richelsen B., Pedersen S.B. Anti-inflammatory effect of resveratrol on adipokine expression and secretion in human adipose tissue explants. Int J Obes (Lond) 2010, 34:1546-1553.
53. Kim S., Jin Y., Choi Y., Park T. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 2011, 81:1343-1351.
54. Mercader J., Palou A., Bonet M.L. Resveratrol enhances fatty acid oxidation capacity and reduces resistin and Retinol-Binding Protein 4 expression in white adipocytes. J Nutr Biochem 2010, 22:828-834.
55. Wang A., Liu M., Liu X., Dong L.Q., Glickman R.D., Slaga T.J., et al. Up-regulation of adiponectin by resveratrol: the essential roles of the Akt/FOXO1 and AMP-activated protein kinase signaling pathways and DsbA-L. J Biol Chem 2011, 286:60-66.
56. Brasnyó P., Molnár G.A., Mohás M., Markó L., Laczy B., Cseh J., et al. Resveratrol improves insulin sensitivity, reduces oxidative stress and activates the Akt pathway in type 2 diabetic patients. Br J Nutr 2011, 106:383-389.
57. Lakenbrink C., Lapczynski S., Maiwald B., Engelhardt U.H. Flavonoids and other polyphenols in consumer brews of tea and other caffeinated beverages. J Agric Food Chem 2000, 48:2848-2852.
58. de Mejia E.G., Ramirez-Mares M.V., Puangpraphant S. Bioactive components of tea: cancer, inflammation and behavior. Brain Behav Immun 2009, 23:721-731.
59. Nomura M., Takahashi T., Nagata N., Tsutsumi K., Kobayashi S., Akiba T., et al. Inhibitory mechanisms of flavonoids on insulin-stimulated glucose uptake in MC3T3-G2/PA6 adipose cells. Biol Pharm Bull 2008, 1403-1409.
60. Hwang J., Park I., Shin J., Lee Y., Lee S., Baik H., et al. Genistein, EGCG, and capsaicin inhibit adipocyte differentiation process via activating AMP-activated protein kinase. Biochem Biophys Res Commun 2005, 694-699.
61. Kim H., Hiraishi A., Tsuchiya K., Sakamoto K. (-) Epigallocatechin gallate suppresses the differentiation of 3T3-L1 preadipocytes through transcription factors FoxO1 and SREBP1c. Cytotechnology 2010, 62:245-255.
62. Liu H.S., Chen Y.H., Hung P.F., Kao Y.H. Inhibitory effect of green tea (-)-epigallocatechin gallate on resistin gene expression in 3T3-L1 adipocytes depends on the ERK pathway. Am J Physiol Endocrinol Metab 2006, 290:E273-E281.
63. Cho S.Y., Park P.J., Shin H.J., Kim Y.K., Shin D.W., Shin E.S., et al. (-)-Catechin suppresses expression of Kruppel-like factor 7 and increases expression and secretion of adiponectin protein in 3T3-L1 cells. Am J Physiol Endocrinol Metab 2007, 292:E1166-E1172.
64. Bose M., Lambert J., Ju J., Reuhl K., Shapses S., Yang C. The major green tea polyphenol, (-)-epigallocatechin-3-gallate, inhibits obesity, metabolic syndrome, and fatty liver disease in high-fat-fed mice. J Nutr 2008, 1677-1683.
65. Lee M., Kim C., Kim Y. Green tea (-)-epigallocatechin-3-gallate reduces body weight with regulation of multiple genes expression in adipose tissue of diet-induced obese mice. Ann Nutr Metab 2009, 151-157.
66. Westerterp-Plantenga M. Green tea catechins, caffeine and body-weight regulation. Physiol Behav 2010, 42-46.
67. Wang H., Wen Y., Du Y., Yan X., Guo H., Rycroft J., et al. Effects of catechin enriched green tea on body composition. Obesity 2010, 773-779.
68. Rivera L., Moron R., Sanchez M., Zarzuelo A., Galisteo M. Quercetin ameliorates metabolic syndrome and improves the inflammatory status in obese Zucker rats. Obesity (Silver Spring) 2008, 16:2081-2087.
69. Coskun O., Kanter M., Korkmaz A., Oter S. Quercetin, a flavonoid antioxidant, prevents and protects streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. Pharmacol Res 2005, 51:117-123.
70. Erlund I., Marniemi J., Hakala P., Alfthan G., Meririnne E., Aro A. Consumption of black currants, lingonberries and bilberries increases serum quercetin concentrations. Eur J Clin Nutr 2003, 57:37-42.
71. Overman A., Chuang C.C., McIntosh M. Quercetin attenuates inflammation in human macrophages and adipocytes exposed to macrophage-conditioned media. Int J Obes (Lond) 2011, 35:1165-1172.
72. Chuang C.C., Martinez K., Xie G., Kennedy A., Bumrungpert A., Overman A., et al. Quercetin is equally or more effective than resveratrol in attenuating tumor necrosis factor-{alpha}-mediated inflammation and insulin resistance in primary human adipocytes. Am J Clin Nutr 2010, 92:1511-1521.
73. Ahn J., Lee H., Kim S., Park J., Ha T. The anti-obesity effect of quercetin is mediated by the AMPK and MAPK signaling pathways. Biochem Biophys Res Commun 2008, 373:545-549.
74. Cassidy A., Albertazzi P., Lise Nielsen I., Hall W., Williamson G., Tetens I., et al. Critical review of health effects of soyabean phyto-oestrogens in post-menopausal women. Proc Nutr Soc 2006, 65:76-92.
75. Anderson J.W., Johnstone B.M., Cook-Newell M.E. Meta-analysis of the effects of soy protein intake on serum lipids. N Engl J Med 1995, 333:276-282.
76. United States Department of Agriculture (USDA) USDA-Iowa Sate University Database on Isoflavone Content of Foods http://www.nal.usda.gov/fnic/foodcomp/Data/isoflav/isoflav.html.
77. Ungar Y., Shimoni E. Phytoestrogens and prevention of cancer. Functional foods, ageing and degenerative disease 2004, 645-668. Woodhead Publishing Limited, Cambridge, UK. C. Remacle, B. Reusens (Eds.).
78. Goodman-Gruen D., Kritz-Silverstein D. Usual dietary isoflavone intake and body composition in postmenopausal women. Menopause 2003, 10:427-432.
79. Noriega-López L., Tovar A.R., Gonzalez-Granillo M., Hernández-Pando R., Escalante B., Santillán-Doherty P., et al. Pancreatic insulin secretion in rats fed a soy protein high fat diet depends on the interaction between the amino acid pattern and isoflavones. J Biol Chem 2007, 282:20657-20666.
80. Zhang H.M., Chen S.W., Zhang L.S., Feng X.F. Effects of soy isoflavone on low-grade inflammation in obese rats. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2006, 31:336-339.
81. Davis J., Higginbotham A., O'Connor T., Moustaid-Moussa N., Tebbe A., Kim Y.C., et al. Soy protein and isoflavones influence adiposity and development of metabolic syndrome in the obese male ZDF rat. Ann Nutr Metab 2007, 51:42-52.
82. Mezei O., Li Y., Mullen E., Ross-Viola J.S., Shay N.F. Dietary isoflavone supplementation modulates lipid metabolism via PPARalpha-dependent and -independent mechanisms. Physiol Genomics 2006, 26:8-14.
83. Kim M., Park J., Seo M., Jung J., Lee Y., Kang K. Genistein and daidzein repress adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells via Wnt/beta-catenin signalling or lipolysis. Cell Prolif 2010, 594-605.
84. Kim M., Kang K., Lee Y. The inhibitory effect of genistein on hepatic steatosis is linked to visceral adipocyte metabolism in mice with diet-induced non-alcoholic fatty liver disease. Br J Nutr 2010, 1333-1342.
85. Kalupahana N.S., Claycombe K., Newman S.J., Stewart T., Siriwardhana N., Matthan N., et al. Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. J Nutr 2010, 140:1915-1922.
86. Kalupahana N.S., Voy B.H., Saxton A.M., Moustaid-Moussa N. Energy-restricted high-fat diets only partially improve markers of systemic and adipose tissue inflammation. Obesity (Silver Spring) 2011, 19:245-254.
87. Kennedy A., Martinez K., Chuang C.C., LaPoint K., McIntosh M. Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. J Nutr 2009, 139:1-4.
88. 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 2004, 39:1177-1185.
89. Couet C., Delarue J., Ritz P., Antoine J.M., Lamisse F. Effect of dietary fish oil on body fat mass and basal fat oxidation in healthy adults. Int J Obes Relat Metab Disord 1997, 21:637-643.
90. Figueras M., Olivan M., Busquets S., Lopez-Soriano F.J., Argiles J.M. Effects of eicosapentaenoic Acid (EPA) treatment on insulin sensitivity in an animal model of diabetes: improvement of the inflammatory status. Obesity (Silver Spring) 2011, 19:362-369.
91. Flachs P., Horakova O., Brauner P., Rossmeisl M., Pecina P., Franssen-van Hal N., et al. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 2005, 48:2365-2375.
92. van Schothorst E.M., Flachs P., Franssen-van Hal N.L., Kuda O., Bunschoten A., Molthoff J., et al. Induction of lipid oxidation by polyunsaturated fatty acids of marine origin in small intestine of mice fed a high-fat diet. BMC Genomics 2009, 10:110.
93. Hein G.J., Bernasconi A.M., Montanaro M.A., Pellon-Maison M., Finarelli G., Chicco A., et al. Nuclear receptors and hepatic lipidogenic enzyme response to a dyslipidemic sucrose-rich diet and its reversal by fish oil n-3 polyunsaturated fatty acids. Am J Physiol Endocrinol Metab 2010, 298:E429-E439.
94. Neschen S., Morino K., Rossbacher J.C., Pongratz R.L., Cline G.W., Sono S., et al. Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-gamma-dependent mechanism in mice. Diabetes 2006, 55:924-928.
95. Oh D.Y., Talukdar S., Bae E.J., Imamura T., Morinaga H., Fan W., et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010, 142:687-698.
96. Hsueh H.W., Zhou Z., Whelan J., Allen K.G., Moustaid-Moussa N., Kim H., et al. Stearidonic and eicosapentaenoic acids inhibit interleukin-6 expression in ob/ob mouse adipose stem cells via toll-like receptor-2-mediated pathways. J Nutr 2011, 141:1260-1266.
97. Wortman P., Miyazaki Y., Kalupahana N.S., Kim S., Hansen-Petrik M., Saxton A.M., et al. n3 and n6 polyunsaturated fatty acids differentially modulate prostaglandin E secretion but not markers of lipogenesis in adipocytes. Nutr Metab (Lond) 2009, 6:5.
98. Schwab J.M., Chiang N., Arita M., Serhan C.N. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007, 447:869-874.
99. Hellmann J., Tang Y., Kosuri M., Bhatnagar A., Spite M. Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J 2011, 25:2399-2407.
100. 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 2010, 59:3066-3073.
101. Due A., Larsen T.M., Mu H., Hermansen K., Stender S., Astrup A. Comparison of 3 ad libitum diets for weight-loss maintenance, risk of cardiovascular disease, and diabetes: a 6-mo randomized, controlled trial. Am J Clin Nutr 2008, 88:1232-1241.
102. Paniagua J.A., Gallego de la Sacristana A., Romero I., Vidal-Puig A., Latre J.M., Sanchez E., et al. Monounsaturated fat-rich diet prevents central body fat distribution and decreases postprandial adiponectin expression induced by a carbohydrate-rich diet in insulin-resistant subjects. Diabetes Care 2007, 30:1717-1723.
103. Shirakawa J., Fujii H., Ohnuma K., Sato K., Ito Y., Kaji M., et al. Diet-induced adipose tissue inflammation and liver steatosis are prevented by DPP-4 inhibition in diabetic mice. Diabetes 2011, 60:1246-1257.
104. Garcia-Escobar E., Rodriguez-Pacheco F., Garcia-Serrano S., Gomez-Zumaquero J.M., Haro-Mora J.J., Soriguer F., et al. Nutritional regulation of interleukin-6 release from adipocytes. Int J Obes (Lond) 2010, 34:1328-1332.
105. Granados N., Amengual J., Ribot J., Palou A., Luisa Bonet M. Distinct effects of oleic acid and its trans-isomer elaidic acid on the expression of myokines and adipokines in cell models. Br J Nutr 2011, 105:1226-1234.
106. Liao F.H., Liou T.H., Chiu W.C., Shieh M.J., Chien Y.W. Differential effects of high MUFA with high or low P/S ratio (polyunsaturated to saturated fatty acids) on improving hepatic lipolytic enzymes and mediating PPARgamma related with lipoprotein lipase and hormone-sensitive lipase of white adipose tissue in diet-induced obese hamster. Int J Obes (Lond) 2010, 34:1608-1617.
107. van Dijk S.J., Feskens E.J., Bos M.B., Hoelen D.W., Heijligenberg R., Bromhaar M.G., et al. A saturated fatty acid-rich diet induces an obesity-linked proinflammatory gene expression profile in adipose tissue of subjects at risk of metabolic syndrome. Am J Clin Nutr 2009, 90:1656-1664.
108. Norris L.E., Collene A.L., Asp M.L., Hsu J.C., Liu L.F., Richardson J.R., et al. Comparison of dietary conjugated linoleic acid with safflower oil on body composition in obese postmenopausal women with type 2 diabetes mellitus. Am J Clin Nutr 2009, 90:468-476.
109. Garcia-Escobar E., Soriguer F., Garcia-Serrano S., Gomez-Zumaquero J.M., Morcillo S., Haro J., et al. Dietary oleic acid and adipocyte lipolytic activity in culture. J Nutr Biochem 2008, 19:727-731.
110. Soriguer F., Moreno F., Rojo-Martinez G., Garcia-Fuentes E., Tinahones F., Gomez-Zumaquero J.M., et al. Monounsaturated n-9 fatty acids and adipocyte lipolysis in rats. Br J Nutr 2003, 90:1015-1022.
111. Hsu S.C., Huang C.J. Reduced fat mass in rats fed a high oleic acid-rich safflower oil diet is associated with changes in expression of hepatic PPARalpha and adipose SREBP-1c-regulated genes. J Nutr 2006, 136:1779-1785.
112. Roche H.M., Noone E., Sewter C., Mc Bennett S., Savage D., Gibney M.J., et al. Isomer-dependent metabolic effects of conjugated linoleic acid: insights from molecular markers sterol regulatory element-binding protein-1c and LXRalpha. Diabetes 2002, 51:2037-2044.
113. Parra P., Serra F., Palou A. Moderate doses of conjugated linoleic acid isomers mix contribute to lowering body fat content maintaining insulin sensitivity and a noninflammatory pattern in adipose tissue in mice. J Nutr Biochem 2010, 21:107-115.
114. Hernandez-Diaz G., Alexander-Aguilera A., Arzaba-Villalba A., Soto-Rodriguez I., Garcia H.S. Effect of conjugated linoleic acid on body fat, tumor necrosis factor alpha and resistin secretion in spontaneously hypertensive rats. Prostaglandins Leukot Essent Fatty Acids 2010, 82:105-109.
115. Corl B.A., Mathews Oliver S.A., Lin X., Oliver W.T., Ma Y., Harrell R.J., et al. Conjugated linoleic acid reduces body fat accretion and lipogenic gene expression in neonatal pigs fed low- or high-fat formulas. J Nutr 2008, 138:449-454.
116. Whigham L.D., Watras A.C., Schoeller D.A. Efficacy of conjugated linoleic acid for reducing fat mass: a meta-analysis in humans. Am J Clin Nutr 2007, 85:1203-1211.
117. Racine N.M., Watras A.C., Carrel A.L., Allen D.B., McVean J.J., Clark R.R., et al. Effect of conjugated linoleic acid on body fat accretion in overweight or obese children. Am J Clin Nutr 2010, 91:1157-1164.
118. Park Y. Conjugated nonadecadienoic acid is more potent than conjugated linoleic acid on body fat reduction. J Nutr Biochem 2010, 21:764-773.
119. Moon H.S., Lee H.G., Seo J.H., Chung C.S., Kim T.G., Choi Y.J., et al. Antiobesity effect of PEGylated conjugated linoleic acid on high-fat diet-induced obese C57BL/6J (ob/ob) mice: attenuation of insulin resistance and enhancement of antioxidant defenses. J Nutr Biochem 2009, 20:187-194.
120. Close R.N., Schoeller D.A., Watras A.C., Nora E.H. Conjugated linoleic acid supplementation alters the 6-mo change in fat oxidation during sleep. Am J Clin Nutr 2007, 86:797-804.
121. Terpstra A.H., Beynen A.C., Everts H., Kocsis S., Katan M.B., Zock P.L. The decrease in body fat in mice fed conjugated linoleic acid is due to increases in energy expenditure and energy loss in the excreta. J Nutr 2002, 132:940-945.
122. Wendel A.A., Purushotham A., Liu L.F., Belury M.A. Conjugated linoleic acid induces uncoupling protein 1 in white adipose tissue of ob/ob mice. Lipids 2009, 44:975-982.
123. Tarling E.J., Ryan K.J., Bennett A.J., Salter A.M. Effect of dietary conjugated linoleic acid isomers on lipid metabolism in hamsters fed high-carbohydrate and high-fat diets. Br J Nutr 2009, 101:1630-1638.
124. Di Giancamillo A., Rossi R., Vitari F., Pastorelli G., Corino C., Domeneghini C. Dietary conjugated linoleic acids decrease leptin in porcine adipose tissue. J Nutr 2009, 139:1867-1872.
125. House R.L., Cassady J.P., Eisen E.J., McIntosh M.K., Odle J. Conjugated linoleic acid evokes de-lipidation through the regulation of genes controlling lipid metabolism in adipose and liver tissue. Obes Rev 2005, 6:247-258.
126. Tsuboyama-Kasaoka N., Takahashi M., Tanemura K., Kim H.J., Tange T., Okuyama H., et al. Conjugated linoleic acid supplementation reduces adipose tissue by apoptosis and develops lipodystrophy in mice. Diabetes 2000, 49:1534-1542.
127. DeClercq V., Zahradka P., Taylor C.G. Dietary t10, c12-CLA but not c9, t11 CLA reduces adipocyte size in the absence of changes in the adipose renin-angiotensin system in fa/fa Zucker rats. Lipids 2010, 45:1025-1033.
128. Moloney F., Toomey S., Noone E., Nugent A., Allan B., Loscher C.E., et al. Antidiabetic effects of cis-9, trans-11-conjugated linoleic acid may be mediated via anti-inflammatory effects in white adipose tissue. Diabetes 2007, 56:574-582.
129. Simon E., Macarulla M.T., Churruca I., Fernandez-Quintela A., Portillo M.P. trans-10,cis-12 conjugated linoleic acid prevents adiposity but not insulin resistance induced by an atherogenic diet in hamsters. J Nutr Biochem 2006, 17:126-131.
130. Poirier H., Shapiro J.S., Kim R.J., Lazar M.A. Nutritional supplementation with trans-10, cis-12-conjugated linoleic acid induces inflammation of white adipose tissue. Diabetes 2006, 55:1634-1641.
131. Poirier H., Rouault C., Clement L., Niot I., Monnot M.C., Guerre-Millo M., et al. Hyperinsulinaemia triggered by dietary conjugated linoleic acid is associated with a decrease in leptin and adiponectin plasma levels and pancreatic beta cell hyperplasia in the mouse. Diabetologia 2005, 48:1059-1065.
132. Chung S., Brown J.M., Provo J.N., Hopkins R., McIntosh M.K. Conjugated linoleic acid promotes human adipocyte insulin resistance through NFkappaB-dependent cytokine production. J Biol Chem 2005, 280:38445-38456.
133. Riserus U., Vessby B., Arner P., Zethelius B. Supplementation with trans10cis12-conjugated linoleic acid induces hyperproinsulinaemia in obese men: close association with impaired insulin sensitivity. Diabetologia 2004, 47:1016-1019.
134. Raff M., Tholstrup T., Toubro S., Bruun J.M., Lund P., Straarup E.M., et al. Conjugated linoleic acids reduce body fat in healthy postmenopausal women. J Nutr 2009, 139:1347-1352.
135. Silveira M.B., Carraro R., Monereo S., Tebar J. Conjugated linoleic acid (CLA) and obesity. Public Health Nutr 2007, 10:1181-1186.
136. Tricon S., Burdge G.C., Kew S., Banerjee T., Russell J.J., Jones E.L., et al. Opposing effects of cis-9, trans-11 and trans-10, cis-12 conjugated linoleic acid on blood lipids in healthy humans. Am J Clin Nutr 2004, 80:614-620.
137. McQuaid S.E., Hodson L., Neville M.J., Dennis A.L., Cheeseman J., Humphreys S.M., et al. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition?. Diabetes 2011, 60:47-55.
138. Kang K., Liu W., Albright K.J., Park Y., Pariza M.W. trans-10,cis-12 CLA inhibits differentiation of 3T3-L1 adipocytes and decreases PPAR gamma expression. Biochem Biophys Res Commun 2003, 303:795-799.
139. Zhou X., Li D., Yin J., Ni J., Dong B., Zhang J., et al. CLA differently regulates adipogenesis in stromal vascular cells from porcine subcutaneous adipose and skeletal muscle. J Lipid Res 2007, 48:1701-1709.
140. Ide T. Interaction of fish oil and conjugated linoleic acid in affecting hepatic activity of lipogenic enzymes and gene expression in liver and adipose tissue. Diabetes 2005, 54:412-423.
141. Chuang C.C., McIntosh M.K. Potential mechanisms by which polyphenol-rich grapes prevent obesity-mediated inflammation and metabolic diseases. Annu Rev Nutr 2010, 31:155-176.
142. Sakurai T., Nishioka H., Fujii H., Nakano N., Kizaki T., Radak Z., et al. Antioxidative effects of a new lychee fruit-derived polyphenol mixture, oligonol, converted into a low-molecular form in adipocytes. Biosci Biotechnol Biochem 2008, 72:463-476.
143. Nakazato K., Song H., Waga T. Effects of dietary apple polyphenol on adipose tissues weights in Wistar rats. Exp Anim 2006, 55:383-389.
144. Park H.J., Yang J.Y., Ambati S., Della-Fera M.A., Hausman D.B., Rayalam S., et al. Combined effects of genistein, quercetin, and resveratrol in human and 3T3-L1 adipocytes. J Med Food 2008, 11:773-783.
145. Medina I., Lois S., Lizárraga D., Pazos M., Touriño S., Cascante M., et al. Functional fatty fish supplemented with grape procyanidins. Antioxidant and proapoptotic properties on colon cell lines. J Agric Food Chem 2006, 54:3598-3603.
146. Massaro M., Scoditti E., Carluccio M., De Caterina R. Nutraceuticals and prevention of atherosclerosis: focus on omega-3 polyunsaturated fatty acids and Mediterranean diet polyphenols. Cardiovasc Ther 2010, e13-e19.
147. Corona G., Spencer J.P., Dessì M.A. Extra virgin olive oil phenolics: absorption, metabolism, and biological activities in the GI tract. Toxicol Ind Health 2009, 25:285-293.
148. Jacomelli M., Pitozzi V., Zaid M., Larrosa M., Tonini G., Martini A., et al. Dietary extra-virgin olive oil rich in phenolic antioxidants and the aging process: long-term effects in the rat. J Nutr Biochem 2010, 21:290-296.
149. Wiseman S.A., Mathot J.N., de Fouw N.J., Tijburg L.B. Dietary non-tocopherol antioxidants present in extra virgin olive oil increase the resistance of low density lipoproteins to oxidation in rabbits. Atherosclerosis 1996, 120:15-23.
150. Covas M., Nyyssonen K., Poulsen H., Kaikkonen J., Zunft H., Kiesewetter H., et al. The effect of polyphenols in olive oil on heart disease risk factors - a randomized trial. Ann Intern Med 2006, 333-341.
151. Watkins B., Hannon K., Ferruzzi M., Li Y. Dietary PUFA and flavonoids as deterrents for environmental pollutants. J Nutr Biochem 2007, 196-205.
152. Nakagawa H., Yamamoto D., Kiyozuka Y., Tsuta K., Uemura Y., Hioki K., et al. Effects of genistein and synergistic action in combination with eicosapentaenoic acid on the growth of breast cancer cell lines. J Cancer Res Clin Oncol 2000, 126:448-454.
153. Akahoshi A., Koba K., Ichinose F., Kaneko M., Shimoda A., Nonaka K., et al. Dietary protein modulates the effect of CLA on lipid metabolism in rats. Lipids 2004, 39:25-30.
154. Akahoshi A., Koba K., Enmoto R., Nishimura K., Honda Y., Minami M., et al. Combined effects of dietary protein type and fat level on the body fat-reducing activity of conjugated linoleic acid (CLA) in rats. Biosci Biotechnol Biochem 2005, 69:2409-2415.
155. Baile C.A., Yang J.Y., Rayalam S., Hartzell D.L., Lai C.Y., Andersen C., et al. Effect of resveratrol on fat mobilization. Ann N Y Acad Sci 2011, 1215:40-47.
156. Rie S., Nishimura N., Hoshino H., Yasuka I., Kadowaki M., Ichi T., et al. Cyanidin 3-glucoside ameliorates hyperglycemia and, insulin sensitivity due to downregulation of retinol binding protein 4 expression in diabetic mice. Biochem Pharmacol 2007, 1619-1627.
157. Wei X., Wang D., Yang Y., Xia M., Li D., Li G., et al. Cyanidin-3-O-beta-glucoside improves obesity and triglyceride metabolism in KK-Ay mice by regulating lipoprotein lipase activity. J Sci Food Agric 2011, 1006-1013.
158. Hsieh C.F., Tsuei Y.W., Liu C.W., Kao C.C., Shih L.J., Ho L.T., et al. Green tea epigallocatechin gallate inhibits insulin stimulation of adipocyte glucose uptake via the 67-kilodalton laminin receptor and AMP-activated protein kinase pathways. Planta Med 2010, 76:1694-1698.
159. Sakurai N., Mochizuki K., Kameji H., Shimada M., Goda T. (-)-Epigallocatechin gallate enhances the expression of genes related to insulin sensitivity and adipocyte differentiation in 3T3-L1 adipocytes at an early stage of differentiation. Nutrition 2009, 25:1047-1056.
160. Anderson R., Polansky M. Tea enhances insulin activity. J Agric Food Chem 2002, 7182-7186.
161. Liu L., Shan S., Zhang K., Ning Z.Q., Lu X.P., Cheng Y.Y. Naringenin and hesperetin, two flavonoids derived from Citrus aurantium up-regulate transcription of adiponectin. Phytother Res 2008, 22:1400-1403.
162. Yoshida H., Takamura N., Shuto T., Ogata K., Tokunaga J., Kawai K., et al. The citrus flavonoids hesperetin and naringenin block the lipolytic actions of TNF-alpha in mouse adipocytes. Biochem Biophys Res Commun 2010, 394:728-732.
163. Morikawa K., Nonaka M., Mochizuki H., Handa K., Hanada H., Hirota K. Naringenin and hesperetin induce growth arrest, apoptosis, and cytoplasmic fat deposit in human preadipocytes. J Agric Food Chem 2008, 56:11030-11037.
164. Yu S., Shun C., Chen T., Chen Y. 3-O-beta-d-glucosyl-(1 -> 6)-beta-d-glucosyl-kaempferol isolated from Sauropus androgenus reduces body weight gain in Wistar rats. Biol Pharm Bull 2006, 2510-2513.
165. Lee J., Lee J., Jung E., Hwang W., Kim Y., Park D. Isorhamnetin-induced anti-adipogenesis is mediated by stabilization of beta-catenin protein. Life Sci 2010, 416-423.
166. Strobel P., Allard C., Perez-Acle T., Calderon R., Aldunate R., Leighton F. Myricetin, quercetin and catechin-gallate inhibit glucose uptake in isolated rat adipocytes. Biochem J 2005, 471-478.
167. Ding L., Jin D., Chen X. Luteolin enhances insulin sensitivity via activation of PPAR gamma transcriptional activity in adipocytes. J Nutr Biochem 2010, 941-947.
168. Guo Y., Wu G., Su X., Yang H., Zhang J. Antiobesity action of a daidzein derivative on male obese mice induced by a high-fat diet. Nutr Res 2009, 656-663.
169. Bhathena S., Velasquez M. Beneficial role of dietary phytoestrogens in obesity and diabetes. Am J Clin Nutr 2002, 1191-1201.
170. Hirota K., Morikawa K., Hanada H., Nonaka M., Nakajima Y., Kobayashi M., et al. Effect of genistein and daidzein on the proliferation and differentiation of human preadipocyte cell line. J Agric Food Chem 2010, 5821-5827.
171. Cho K.W., Lee O.H., Banz W.J., Moustaid-Moussa N., Shay N.F., Kim Y.C. Daidzein and the daidzein metabolite, equol, enhance adipocyte differentiation and PPARgamma transcriptional activity. J Nutr Biochem 2010, 21:841-847.