Interplay of adiponectin, TNFα and insulin on gene expression, glucose uptake and PPARγ, AKT and TOR pathways in rainbow trout cultured adipocytes

General and Comparative Endocrinology

Volumn 205, Issue , 2014, Pages 218-225

  Bou, Marta ^a   Todorčević, Marijana ^b   Rodríguez, Júlia ^a   Capilla, Encarnación ^a   Gutiérrez, Joaquim ^a   Navarro, Isabel ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b NOFIMA   (Norway)

Author keywords

Adipokines; Adiponectin receptors; Glucose transport; IGF I; Insulin signaling

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; CYTOCHALASIN B; DEOXYGLUCOSE; ELONGATION FACTOR 1ALPHA; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE B; SOMATOMEDIN C; TARGET OF RAPAMYCIN KINASE; TUMOR NECROSIS FACTOR ALPHA; ADIPONECTIN RECEPTOR; GLUCOSE;

ADIPOCYTE; ADIPONECTIN GENE; ADIPOR1 GENE; ADIPOR2 GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EF1 ALPHA GENE; GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PPAR GAMMA GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAINBOW TROUT; SIGNAL TRANSDUCTION; TNF ALPHA GENE; UPREGULATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; SWINE;

ADIPOCYTES; ADIPONECTIN; ANIMALS; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION; GLUCOSE; INSULIN; INSULIN-LIKE GROWTH FACTOR I; ONCORHYNCHUS MYKISS; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ADIPONECTIN; SIGNAL TRANSDUCTION; SUS SCROFA; TOR SERINE-THREONINE KINASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84908641907     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2014.05.005     Document Type: Article

References (68)

1. Albalat A., Liarte C., MacKenzie S., Tort L., Planas J.V., Navarro I. Control of adipose tissue lipid metabolism by tumor necrosis factor-α in rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 2005, 184:527-534.
2. Ali A.T., Hochfeld W.E., Myburgh R., Pepper M.S. Adipocyte and adipogenesis. Eur. J. Cell Biol. 2013, 92:229-236.
3. Arita Y. Reprint of "Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity". Biochem. Biophys. Res. Commun. 2012, 425:560-564.
4. Berg A.H., Combs T.P., Du X., Brownlee M., Scherer P.E. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 2001, 7:947-953.
5. Bouraoui L., Gutiérrez J., Navarro I. Regulation of proliferation and differentiation of adipocyte precursor cells in rainbow trout (Oncorhynchus mykiss). J. Endocrinol. 2008, 198:459-469.
6. Bouraoui L., Capilla E., Gutiérrez J., Navarro I. Insulin and insulin-like growth factor I signaling pathways in rainbow trout (Oncorhynchus mykiss) during adipogenesis and their implication in glucose uptake. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:33-41.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Bruun J.M., Lihn A.S., Verdich C., Pedersen S.B., Toubro S., Astrup A., Richelsen B. Regulation of adiponectin by adipose tissue-derived cytokines: in vivo and in vitro investigations in humans. Am. J. Physiol. Endocrinol. Metab. 2003, 285:527-533.
9. Capilla E., Díaz M., Albalat A., Navarro I., Pessin J.E., Keller K., Planas J.V. Functional characterization of an insulin-responsive glucose transporter (GLUT4) from fish adipose tissue. Am. J. Physiol. Endocrinol. Metab. 2004, 287:348-357.
10. Cornelius P., Marlowe M., Lee M.D., Pekala P.H. The growth factor-like effects of tumor necrosis factor-alpha. Stimulation of glucose transport activity and induction of glucose transporter and immediate early gene expression in 3T3-L1 preadipocytes. J. Biol. Chem. 1990, 265:20506-20516.
11. Cruz-Garcia L., Saera-Vila A., Navarro I., Calduch-Giner J., Pérez-Sánchez J. Targets for TNFalpha-induced lipolysis in gilthead sea bream (Sparus aurata L.) adipocytes isolated from lean and fat juvenile fish. J. Exp. Biol. 2009, 212:2254-2260.
12. 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.
13. Fang X., Palanivel R., Zhou X., Liu Y., Xu A., Wang Y., Sweeney G. Hyperglycemia- and hyperinsulinemia-induced alteration of adiponectin receptor expression and adiponectin effects in L6 myoblasts. J. Mol. Endocrinol. 2005, 35:465-476.
14. Fasshauer M., Klein J., Neumann S., Eszlinger M., Paschke R. Hormonal regulation of adiponectin gene expression in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 2002, 290:1084-1089.
15. Fernández-Veledo S., Vila-Bedmar R., Nieto-Vazquez I., Lorenzo M. C-Jun N-terminal kinase 1/2 activation by tumor necrosis factor-alpha induces insulin resistance in human visceral but not subcutaneous adipocytes: reversal by liver X receptor agonists. J. Clin. Endocrinol. Metab. 2009, 94:3583-3593.
16. Fruebis J., Tsao T.S., Javorschi S., Ebbets-Reed D., Erickson M.R., Yen F.T., Bihain B.E., Lodish H.F. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:2005-2010.
17. Fu Y., Luo N., Klein R.L., Garvey W.T. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J. Lipid Res. 2005, 46:1369-1379.
18. Gao Z., He Q., Peng B., Chiao P.J., Ye J. Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferator-activated receptor gamma function. J. Biol. Chem. 2006, 281:4540-4547.
19. Guerre-Millo M. Adiponectin: an update. Diabetes Metab. 2008, 34:12-18.
20. Hajri T., Tao H., Wattacheril J., Marks-Shulman P., Abumrad N.N. Regulation of adiponectin production by insulin: interactions with tumor necrosis factor-alpha and interleukin-6. Am. J. Physiol. Endocrinol. Metab. 2011, 300:350-360.
21. Halleux C.M., Takahashi M., Delporte M.L., Detry R., Funahashi T., Matsuzawa Y., Brichard S.M. Secretion of adiponectin and regulation of apM1 gene expression in human visceral adipose tissue. Biochem. Biophys. Res. Commun. 2001, 288:1102-1107.
22. Harwood H.J. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012, 63:57-75.
23. Hotamisligil G.S. Mechanisms of TNF-alpha-induced insulin resistance. Exp. Clin. Endocrinol. Diabetes 1999, 107:119-125.
24. Hotamisligil G.S., Shargill N.S., Spiegelman B.M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
25. Hu E., Liang P., Spiegelman B.M. AdipoQ is a novel adipose-specific gene dysregulated in obesity. J. Biol. Chem. 1996, 271:10697-10703.
26. Im J.-A., Kim S.-H., Lee J.-W., Shim J.-Y., Lee H.-R., Lee D.-C. Association between hypoadiponectinemia and cardiovascular risk factors in nonobese healthy adults. Metab. Clin. Exp. 2006, 55:1546-1550.
27. Iwaki M., Matsuda M., Maeda N., Funahashi T., Matsuzawa Y., Makishima M., Shimomura I. Induction of adiponectin, a fat-derived antidiabetic and antiatherogenic factor, by nuclear receptors. Diabetes 2003, 52:1655-1663.
28. Kappes A., Löffler G. Influences of ionomycin, dibutyryl-cycloAMP and tumour necrosis factor-alpha on intracellular amount and secretion of apM1 in differentiating primary human preadipocytes. Horm. Metab. Res. 2000, 32:548-554.
29. Kim H.B., Kim W.H., Han K.L., Park J.H., Lee J., Yeo J., Jung M.H. CAMP-response element binding protein (CREB) positively regulates mouse adiponectin gene expression in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 2010, 391:634-639.
30. Kondo H., Suda S., Kawana Y., Hirono I., Nagasaka R., Kaneko G., Ushio H., Watabe S. Effects of feed restriction on the expression profiles of the glucose and fatty acid metabolism-related genes in rainbow trout Oncorhynchus mykiss muscle. Fish Sci. 2012, 78:1205-1211.
31. Kondo H., Suga R., Suda S., Nozaki R., Hirono I., Nagasaka R., Kaneko G., Ushio H., Watabe S. EST analysis on adipose tissue of rainbow trout Oncorhynchus mykiss and tissue distribution of adiponectin. Gene 2011, 485:40-45.
32. Kwon H., Pessin J.E. Adipokines mediate inflammation and insulin resistance. Front. Endocrinol. 2013, 4:71.
33. Lee B., Shao J. Adiponectin and lipid metabolism in skeletal muscle. Acta Pharm. Sin. B 2012, 2:335-340.
34. Lee B., Shao J. Adiponectin and energy homeostasis. Rev. Endocr. Metab. Disord. 2013, 10.1007/s11154-013-9283-3.
35. Liu B.H., Wang Y.C., Wu S.C., Mersmann H.J., Cheng W.T.K., Ding S.T. Insulin regulates the expression of adiponectin and adiponectin receptors in porcine adipocytes. Domest. Anim. Endocrinol. 2008, 34:352-359.
36. Liu Y., Sweeney G. Adiponectin action in skeletal muscle. Best Pract. Res. Clin. Endocrinol. Metab. 2014, 28(1):33-41.
37. -δδCT method. Methods 2001, 25:402-408.
38. Maeda N., Takahashi M., Funahashi T., Kihara S., Nishizawa H., Kishida K., Nagaretani H., Matsuda M., Komuro R., Ouchi N., et al. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 2001, 50:2094-2099.
39. Maeda N., Shimomura I., Kishida K., Nishizawa H., Matsuda M., Nagaretani H., Furuyama N., Kondo H., Takahashi M., Arita Y., et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 2002, 8:731-737.
40. Matsushita K., Yatsuya H., Tamakoshi K., Wada K., Otsuka R., Takefuji S., Sugiura K., Kondo T., Murohara T., Toyoshima H. Comparison of circulating adiponectin and proinflammatory markers regarding their association with metabolic syndrome in japanese men. Arterioscler. Thromb. Vasc. Biol. 2006, 26:871-876.
41. Medina E.A., Stanhope K.L., Mizuno T.M., Mobbs C.V., Gregoire F., Hubbard N.E., Erickson K.L., Havel P.J. Effects of tumor necrosis factor alpha on leptin secretion and gene expression: relationship to changes of glucose metabolism in isolated rat adipocytes. Int. J. Obes. Relat. Metab. Disord. 1999, 23:896-903.
42. Montserrat N., Capilla E., Navarro I., Gutiérrez J. Metabolic effects of insulin and IGFs on gilthead sea bream (Sparus aurata) muscle cells. Front. Endocrinol. 2012, 3:55.
43. Nieto-Vazquez I., Fernández-Veledo S., de Alvaro C., Lorenzo M. Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle. Diabetes 2008, 57:3211-3221.
44. Nishio S.-I., Gibert Y., Bernard L., Brunet F., Triqueneaux G., Laudet V. Adiponectin and adiponectin receptor genes are coexpressed during zebrafish embryogenesis and regulated by food deprivation. Dev. Dyn. 2008, 237:1682-1690.
45. Phillips S.A., Ciaraldi T.P., Kong A.P., Bandukwala R., Aroda V., Carter L., Baxi S., Mudaliar S.R., Henry R.R. Modulation of circulating and adipose tissue adiponectin levels by antidiabetic therapy. Diabetes 2003, 52:667-674.
46. Porter M.H., Cutchins A., Fine J.B., Bai Y., Digirolamo M. Effects of TNF-α on glucose metabolism and lipolysis in adipose tissue and isolated fat-cell preparations. J. Lab. Clin. Med. 2002, 139:140-146.
47. Saera-Vila A., Calduch-Giner J.A., Navarro I., Perez-Sanchez J. Tumour necrosis factor (TNF)alpha as a regulator of fat tissue mass in the Mediterranean gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 2007, 146:338-345.
48. Sánchez-Gurmaches J., Cruz-Garcia L., Gutiérrez J., Navarro I. Adiponectin effects and gene expression in rainbow trout: an in vivo and in vitro approach. J. Exp. Biol. 2012, 215:1373-1383.
49. Scherer P.E., Williams S., Fogliano M., Baldini G., Lodish H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 1995, 270:26746-26749.
50. Seiliez I., Gutiérrez J., Salmerón C., Skiba-Cassy S., Chauvin C., Dias K., Kaushik S., Tesseraud S., Panserat S. An in vivo and in vitro assessment of autophagy-related gene expression in muscle of rainbow trout (Oncorhynchus mykiss). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 157:258-266.
51. Stephens J.M., Lee J., Pilch P.F. Tumor necrosis factor-alpha-induced insulin resistance in 3T3-L1 adipocytes is accompanied by a loss of insulin receptor substrate-1 and GLUT4 expression without a loss of insulin receptor-mediated signal transduction. J. Biol. Chem. 1997, 272:971-976.
52. Sun Y., Zan L., Wang H., Guo H., Yang D., Zhao X., Gui L. Insulin inhibits the expression of adiponectin and adipoR2 mRNA in cultured bovine adipocytes. Asian-Aust. J. Anim. Sci. 2009, 22:1429-1436.
53. Tang T., Zhang J., Yin J., Staszkiewicz J., Gawronska-Kozak B., Jung D.Y., Ko H.J., Ong H., Kim J.K., Mynatt R., et al. Uncoupling of inflammation and insulin resistance by NF-kappaB in transgenic mice through elevated energy expenditure. J. Biol. Chem. 2010, 285:4637-4644.
54. Tilg H., Moschen A.R. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 2006, 6:772-783.
55. Todorčević M., Skugor S., Krasnov A., Ruyter B. Gene expression profiles in Atlantic salmon adipose-derived stromo-vascular fraction during differentiation into adipocytes. BMC Genomics 2010, 11:39.
56. Tsuchida A., Yamauchi T., Takekawa S., Hada Y., Ito Y., Maki T., Kadowaki T. 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, 54:3358-3370.
57. Vraskou Y., Roher N., Díaz M., Antonescu C.N., MacKenzie S.A., Planas J.V. Direct involvement of tumor necrosis factor-α in the regulation of glucose uptake in rainbow trout muscle cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:716-723.
58. Wang Y., Wang H., Hegde V., Dubuisson O., Gao Z., Dhurandhar N.V., Ye J. Interplay of pro- and anti-inflammatory cytokines to determine lipid accretion in adipocytes. Int. J. Obes. (Lond) 2013, 37(11):1490-1498. 10.1038/ijo.2013.9.
59. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
60. Wu X., Motoshima H., Mahadev K., Stalker T.J., Scalia R., Goldstein B.J. Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 2003, 52:1355-1363.
61. Xing H., Northrop J.P., Grove J.R., Kilpatrick K.E., Su J.L., Ringold G.M. TNF alpha-mediated inhibition and reversal of adipocyte differentiation is accompanied by suppressed expression of PPARgamma without effects on Pref-1 expression. Endocrinology 1997, 138:2776-2783.
62. Yamamoto Y., Hirose H., Saito I., Nishikai K., Saruta T. Adiponectin, an adipocyte-derived protein, predicts future insulin resistance: two-year follow-up study in japanese population. J. Clin. Endocrinol. Metab. 2004, 89:87-90.
63. Yamauchi T., Kamon J., Waki H., Terauchi Y., Kubota N., Hara K., Mori Y., Ide T., Murakami K., Tsuboyama-Kasaoka N., et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med. 2001, 7:941-946.
64. Yamauchi T., Nio Y., Maki T., Kobayashi M., Takazawa T., Iwabu M., Okada-Iwabu M., Kawamoto S., Kubota N., Kubota T., et al. Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 2007, 13:332-339.
65. Yan J., Gan L., Chen D., Sun C. Adiponectin impairs chicken preadipocytes differentiation through p38 MAPK/ATF-2 and TOR/p70 S6 kinase pathways. PLoS One 2013, 8:e77716. 10.1371/journal.pone.0077716.
66. Yatagai T., Nagasaka S., Taniguchi A., Fukushima M., Nakamura T., Kuroe A., Nakai Y., Ishibashi S. Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metab. Clin. Exp. 2003, 52:1274-1278.
67. Ye J. Regulation of PPARgamma function by TNF-alpha. Biochem. Biophys. Res. Commun. 2008, 374:405-408.
68. Ye J. Obesity, inflammation and the metabolic syndrome. Obesity 2011, 169-188. Elsevier, Barcelona. M. Serrano-Ríos, J.M. Ordovás, J.A. Gutiérrez-Fuentes (Eds.).