3T3-L1 preadipocytes exhibit heightened monocyte-chemoattractant protein-1 response to acute fatty acid exposure

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Dordevic, Aimee L ^a,b   Konstantopoulos, Nicky ^a   Cameron Smith, David ^a,c  

^a DEAKIN UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; FATTY ACID; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LEPTIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MYRISTIC ACID; OLEIC ACID; PALMITIC ACID; PHOSPHOTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOTAGMIN I; MESSENGER RNA;

ADIPOCYTE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; GENE EXPRESSION; INFLAMMATION; PROADIPOCYTE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; 3T3 CELL LINE; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; CHEMOKINE CCL2; FATTY ACIDS; GENE EXPRESSION REGULATION; INTERLEUKIN-6; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RNA, MESSENGER;

EID: 84902602774     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099382     Document Type: Article

References (57)

1. Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW (2004) Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145: 2273-2282. (Pubitemid 38535056)
2. Song MJ, Kim KH, Yoon JM, Kim JB (2006) Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem Biophys Res Commun 346: 739-745.
3. Stehno-Bittel L (2008) Intricacies of fat. Phys Ther 88: 1265-1278.
4. Hauner H (2005) Secretory factors from human adipose tissue and their functional role. Proc Nutr Soc 64: 163-169.
5. Guo W, Wong S, Xie W, Lei T, Luo Z (2007) Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 293: E576-586. (Pubitemid 47205102)
6. Isakson P, Hammarstedt A, Gustafson B, Smith U (2009) Impaired preadipocyte differentiation in human abdominal obesity: role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes 58: 1550-1557.
7. Charriere G, Cousin B, Arnaud E, Andre M, Bacou F, et al. (2003) Preadipocyte conversion to macrophage. Evidence of plasticity. J Biol Chem 278: 9850-9855. (Pubitemid 36800488)
8. Fain JN (2010) Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediators Inflamm 2010: 513948.
9. Chung S, Lapoint K, Martinez K, Kennedy A, Boysen Sandberg M, et al. (2006) Preadipocytes mediate lipopolysaccharide-induced inflammation and insulin resistance in primary cultures of newly differentiated human adipocytes. Endocrinology 147: 5340-5351. (Pubitemid 44790589)
10. van Dijk SJ, Feskens EJ, Bos MB, Hoelen DW, Heijligenberg R, et al. (2009) 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 90: 1656-1664.
11. Nappo F, Esposito K, Cioffi M, Giugliano G, Molinari AM, et al. (2002) Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. J Am Coll Cardiol 39: 1145-1150. (Pubitemid 34267417)
12. Peairs AD, Rankin JW, Lee YW (2011) Effects of acute ingestion of different fats on oxidative stress and inflammation in overweight and obese adults. Nutr J 10: 122.
13. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, et al. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015-3025. (Pubitemid 44684486)
14. Yeop Han C, Kargi AY, Omer M, Chan CK, Wabitsch M, et al. (2010) Differential effect of saturated and unsaturated free fatty acids on the generation of monocyte adhesion and chemotactic factors by adipocytes: dissociation of adipocyte hypertrophy from inflammation. Diabetes 59: 386-396.
15. Chai W, Liu Z (2007) p38 mitogen-activated protein kinase mediates palmitate-induced apoptosis but not inhibitor of nuclear factor-kappaB degradation in human coronary artery endothelial cells. Endocrinology 148: 1622-1628. (Pubitemid 46457113)
16. Crunkhorn S, Dearie F, Mantzoros C, Gami H, da Silva WS, et al. (2007) Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J Biol Chem 282: 15439-15450. (Pubitemid 47093279)
17. Ajuwon KM, Spurlock ME (2005) Palmitate activates the NF-kappaB transcription factor and induces IL-6 and TNFalpha expression in 3T3-L1 adipocytes. J Nutr 135: 1841-1846. (Pubitemid 41099739)
18. Schaeffler A, Gross P, Buettner R, Bollheimer C, Buechler C, et al. (2009) Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology 126: 233-245.
19. Voon PT, Ng TK, Lee VK, Nesaretnam K (2011) Diets high in palmitic acid (16:0), lauric and myristic acids (12:0+14:0), or oleic acid (18:1) do not alter postprandial or fasting plasma homocysteine and inflammatory markers in healthy Malaysian adults. Am J Clin Nutr 94: 1451-1457.
20. Manning PJ, Sutherland WH, McGrath MM, de Jong SA, Walker RJ, et al. (2008) Postprandial cytokine concentrations and meal composition in obese and lean women. Obesity 16: 2046-2052.
21. Konstantopoulos N, Marcuccio S, Kyi S, Stoichevska V, Castelli LA, et al. (2007) A purine analog kinase inhibitor, calcium/calmodulin-dependent protein kinase II inhibitor 59, reveals a role for calcium/calmodulin-dependent protein kinase II in insulin-stimulated glucose transport. Endocrinology 148: 374-385. (Pubitemid 46021470)
22. Hudak CS, Sul HS (2013) Pref-1, a gatekeeper of adipogenesis. Front Endocrinol (Lausanne) 4: 79.
23. Chavez JA, Summers SA (2003) Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys 419: 101-109. (Pubitemid 37329976)
24. Thompson GM, Trainor D, Biswas C, LaCerte C, Berger JP, et al. (2004) A high-capacity assay for PPARgamma ligand regulation of endogenous aP2 expression in 3T3-L1 cells. Anal Biochem 330: 21-28. (Pubitemid 38746970)
25. O'Hara A, Lim FL, Mazzatti DJ, Trayhurn P (2012) Stimulation of inflammatory gene expression in human preadipocytes by macrophage-conditioned medium: upregulation of IL-6 production by macrophage-derived IL-1beta. Mol Cell Endocrinol 349: 239-247.
26. Poulain-Godefroy O, Froguel P (2007) Preadipocyte response and impairment of differentiation in an inflammatory environment. Biochem Biophys Res Commun 356: 662-667. (Pubitemid 46499015)
27. Keophiphath M, Achard V, Henegar C, Rouault C, Clement K, et al. (2009) Macrophage-secreted factors promote a profibrotic phenotype in human preadipocytes. Mol Endocrinol 23: 11-24.
28. Lacasa D, Taleb S, Keophiphath M, Miranville A, Clement K (2007) Macrophage-secreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology 148: 868-877. (Pubitemid 46143186)
29. Jove M, Planavila A, Sanchez RM, Merlos M, Laguna JC, et al. (2006) Palmitate induces tumor necrosis factor-alpha expression in C2C12 skeletal muscle cells by a mechanism involving protein kinase C and nuclear factor-kappaB activation. Endocrinology 147: 552-561. (Pubitemid 43004310)
30. Jove M, Planavila A, Laguna JC, Vazquez-Carrera M (2005) Palmitate-induced interleukin 6 production is mediated by protein kinase C and nuclear-factor kappaB activation and leads to glucose transporter 4 down-regulation in skeletal muscle cells. Endocrinology 146: 3087-3095. (Pubitemid 41002818)
31. Weigert C, Brodbeck K, Staiger H, Kausch C, Machicao F, et al. (2004) Palmitate, but not unsaturated fatty acids, induces the expression of interleukin-6 in human myotubes through proteasome-dependent activation of nuclear factorkappaB. J Biol Chem 279: 23942-23952. (Pubitemid 38725252)
32. Joshi-Barve S, Barve SS, Amancherla K, Gobejishvili L, Hill D, et al. (2007) Palmitic acid induces production of proinflammatory cytokine interleukin-8 from hepatocytes. Hepatology 46: 823-830. (Pubitemid 47436129)
33. Bradley RL, Fisher FF, Maratos-Flier E (2008) Dietary fatty acids differentially regulate production of TNF-alpha and IL-10 by murine 3T3-L1 adipocytes. Obesity 16: 938-944. (Pubitemid 351620481)
34. Meneses ME, Camargo A, Perez-Martinez P, Delgado-Lista J, Cruz-Teno C, et al. (2011) Postprandial inflammatory response in adipose tissue of patients with metabolic syndrome after the intake of different dietary models. Mol Nutr Food Res 55: 1759-1770.
35. Masson CJ, Mensink RP (2011) Exchanging saturated fatty acids for (n-6) polyunsaturated fatty acids in a mixed meal may decrease postprandial lipemia and markers of inflammation and endothelial activity in overweight men. J Nutr 141: 816-821.
36. Annuzzi G, Bozzetto L, Patti L, Santangelo C, Giacco R, et al. (2010) Type 2 diabetes mellitus is characterized by reduced postprandial adiponectin response: a possible link with diabetic postprandial dyslipidemia. Metabolism 59: 567-574.
37. Wang B, Jenkins JR, Trayhurn P (2005) Expression and secretion of inflammation-related adipokines by human adipocytes differentiated in culture: integrated response to TNF-alpha. American journal of physiology Endocrinology and metabolism 288: E731-740. (Pubitemid 40397208)
38. Verrijn Stuart AA, Schipper HS, Tasdelen I, Egan DA, Prakken BJ, et al. (2012) Altered plasma adipokine levels and in vitro adipocyte differentiation in pediatric type 1 diabetes. J Clin Endocrinol Metab 97: 463-472.
39. Granados N, Amengual J, Ribot J, Palou A, Bonet ML (2011) Distinct effects of oleic acid and its trans-isomer elaidic acid on the expression of myokines and adipokines in cell models. Br J Nutr 105: 1226-1234.
40. Gao D, Trayhurn P, Bing C (2012) 1,25-Dihydroxyvitamin D(3) inhibits the cytokine-induced secretion of MCP-1 and reduces monocyte recruitment by human preadipocytes. Int J Obes (Lond).
41. Melloni E, Zauli G, Celeghini C, Volpi I, Secchiero P (2013) Release of a specific set of proinflammatory adipokines by differentiating 3T3-L1 cells. Nutrition 29: 332-337.
42. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, et al. (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116: 1494-1505.
43. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, et al. (2006) Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281: 26602-26614. (Pubitemid 44401869)
44. Lumeng CN, Deyoung SM, Bodzin JL, Saltiel AR (2007) Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity. Diabetes 56: 16-23.
45. Tardif N, Salles J, Landrier JF, Mothe-Satney I, Guillet C, et al. (2011) Oleate-enriched diet improves insulin sensitivity and restores muscle protein synthesis in old rats. Clin Nutr 30: 799-806.
46. Shang Z, Guo L, Wang N, Shi H, Wang Y, et al. (2014) Oleate promotes differentiation of chicken primary preadipocytes in vitro. Biosci Rep.
47. Lamers D, Schlich R, Horrighs A, Cramer A, Sell H, et al. (2012) Differential impact of oleate, palmitate, and adipokines on expression of NF-kappaB target genes in human vascular smooth muscle cells. Mol Cell Endocrinol 362: 194-201.
48. Liu HY, Collins QF, Xiong Y, Moukdar F, Lupo EG Jr, et al. (2007) Prolonged treatment of primary hepatocytes with oleate induces insulin resistance through p38 mitogen-activated protein kinase. J Biol Chem 282: 14205-14212. (Pubitemid 47100474)
49. Oeckinghaus A, Hayden MS, Ghosh S (2011) Crosstalk in NF-kappaB signaling pathways. Nat Immunol 12: 695-708.
50. Hunter JE, Zhang J, Kris-Etherton PM (2010) Cardiovascular disease risk of dietary stearic acid compared with trans, other saturated, and unsaturated fatty acids: a systematic review. Am J Clin Nutr 91: 46-63.
51. Berg AH, Lin Y, Lisanti MP, Scherer PE (2004) Adipocyte differentiation induces dynamic changes in NF-kappaB expression and activity. Am J Physiol Endocrinol Metab 287: E1178-1188. (Pubitemid 39491960)
52. Bradley RL, Fisher FF, Maratos-Flier E (2008) Dietary fatty acids differentially regulate production of TNF-alpha and IL-10 by murine 3T3-L1 adipocytes. Obesity (Silver Spring) 16: 938-944. (Pubitemid 351620481)
53. Nguyen MT, Satoh H, Favelyukis S, Babendure JL, Imamura T, et al. (2005) JNK and tumor necrosis factor-alpha mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J Biol Chem 280: 35361-35371. (Pubitemid 41532725)
54. Kubota Y, Unoki H, Bujo H, Rikihisa N, Udagawa A, et al. (2008) Low-dose GH supplementation reduces the TLR2 and TNF-alpha expressions in visceral fat. Biochem Biophys Res Commun 368: 81-87.
55. Neacsu O, Cleveland K, Xu H, Tchkonia TT, Kirkland JL, et al. (2013) IGF-I attenuates FFA-induced activation of JNK1 phosphorylation and TNFalpha expression in human subcutaneous preadipocytes. Obesity (Silver Spring) 21: 1843-1849.
56. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808. (Pubitemid 38063703)
57. Xu H, Barnes GT, Yang Q, Tan G, Yang D, et al. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830. (Pubitemid 38063705)