AMPK activator-mediated inhibition of endoplasmic reticulum stress ameliorates carrageenan-induced insulin resistance through the suppression of selenoprotein P in HepG2 hepatocytes

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 66-73

  Jung, Tae Woo ^a   Lee, So Young ^a   Hong, Ho Cheol ^a   Choi, Hae Yoon ^a   Yoo, Hye Jin ^a   Baik, Sei Hyun ^a   Choi, Kyung Mook ^a  

^a Korea University College of Medicine   (South Korea)

Author keywords

AMPK; ER stress; Hepatokine; Insulin resistance; Salsalate; Selenoprotein P

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 PHENYLBUTYRIC ACID; ACETYLSALICYLIC ACID; ADENOSINE PHOSPHATE; CARRAGEENAN; CCAAT ENHANCER BINDING PROTEIN; GLUCOSE; GLYCOPROTEIN; INSULIN; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; SALICYLIC ACID; SALSALATE; SELENOPROTEIN P; TOLL LIKE RECEPTOR 4;

ARTICLE; CAUCASIAN; ENDOPLASMIC RETICULUM STRESS; GLUCOSE TOLERANCE; HEPATOMA CELL; HUMAN; HUMAN CELL; INSULIN RESISTANCE; LIVER CELL; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

AMPK; ER STRESS; HEPATOKINE; INSULIN RESISTANCE; SALSALATE; SELENOPROTEIN P;

ADOLESCENT; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; CARRAGEENAN; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVATORS; HEP G2 CELLS; HEPATOCYTES; HUMANS; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MAP KINASE SIGNALING SYSTEM; METFORMIN; RIBONUCLEOTIDES; SALICYLATES; SELENOPROTEIN P;

EID: 84884939573     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.09.013     Document Type: Article

References (30)

1. Bhattacharyya S., Dudeja P.K., Tobacman J.K. Carrageenan-induced NFkappaB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10. Biochim. Biophys. Acta 2008, 1780:973-982.
2. Bhattacharyya S., Gill R., Chen M.L., Zhang F., Linhardt R.J., Dudeja P.K., Tobacman J.K. Toll-like receptor 4 mediates induction of the Bcl10-NFkappaB-interleukin-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J. Biol. Chem. 2008, 283:10550-10558.
3. Borthakur A., Bhattacharyya S., Dudeja P.K., Tobacman J.K. Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292. G829-38.
4. Tsukumo D.M., Carvalho-Filho M.A., Carvalheira J.B., Prada P.O., Hirabara S.M., Schenka A.A., Araujo E.P., Vassallo J., Curi R., Velloso L.A., Saad M.J. Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 2007, 56:1986-1998.
5. Misu H., Takamura T., Takayama H., Hayashi H., Matsuzawa-Nagata N., Kurita S., Ishikura K., Ando H., Takeshita Y., Ota T., Sakurai M., Yamashita T., Mizukoshi E., Honda M., Miyamoto K., Kubota T., Kubota N., Kadowaki T., Kim H.J., Lee I.K., Minokoshi Y., Saito Y., Takahashi K., Yamada Y., Takakura N., Kaneko S. A liver-derived secretory protein, selenoprotein P, causes insulin resistance. Cell Metab. 2010, 12:483-495.
6. Misu H., Ishikura K., Kurita S., Takeshita Y., Ota T., Saito Y., Takahashi K., Kaneko S., Takamura T. Inverse correlation between serum levels of selenoprotein P and adiponectin in patients with type 2 diabetes. PLoS One 2012, 7:e34952.
7. Yang S.J., Hwang S.Y., Choi H.Y., Yoo H.J., Seo J.A., Kim S.G., Kim N.H., Baik S.H., Choi D.S., Choi K.M. Serum selenoprotein P levels in patients with type 2 diabetes and prediabetes: implications for insulin resistance, inflammation, and atherosclerosis. J. Clin. Endocrinol. Metab. 2011, 96. E1325-9.
8. Choi H.Y., Hwang S.Y., Lee C.H., Hong H.C., Yang S.J., Yoo H.J., Seo J.A., Kim S.G., Kim N.H., Baik S.H., Choi D.S., Choi K.M. Increased selenoprotein p levels in subjects with visceral obesity and nonalcoholic Fatty liver disease. Diab. Metab. J. 2013, 37:63-71.
9. Hardie D.G., Hawley S.A., Scott J.W. AMP-activated protein kinase-development of the energy sensor concept. J. Physiol. 2006, 574:7-15.
10. Salminen A., Hyttinen J.M., Kaarniranta K. AMP-activated protein kinase inhibits NF-kappaB signaling and inflammation: impact on healthspan and lifespan. J. Mol. Med. (Berl) 2011, 89:667-676.
11. Hawley S.A., Fullerton M.D., Ross F.A., Schertzer J.D., Chevtzoff C., Walker K.J., Peggie M.W., Zibrova D., Green K.A., Mustard K.J., Kemp B.E., Sakamoto K., Steinberg G.R., Hardie D.G. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012, 336:918-922.
12. Hundal R.S., Petersen K.F., Mayerson A.B., Randhawa P.S., Inzucchi S., Shoelson S.E., Shulman G.I. Mechanism by which high-dose aspirin improves glucose metabolism in type 2 diabetes. J. Clin. Invest. 2002, 109:1321-1326.
13. Goldfine A.B., Fonseca V., Shoelson S.E. Therapeutic approaches to target inflammation in type 2 diabetes. Clin. Chem. 2011, 57:162-167.
14. Goldfine A.B., Fonseca V., Jablonski K.A., Pyle L., Staten M.A., Shoelson S.E. The effects of salsalate on glycemic control in patients with type 2 diabetes: a randomized trial. Annu. Int. Med. 2010, 152:346-357.
15. Cong X.D., Wu Y., Dai D.Z., Ding M.J., Zhang Y., Dai Y. Activation of AQP4, p66Shc and endoplasmic reticulum stress is involved in inflammation by carrageenan and is suppressed by argirein, a derivative of rhein. J. Pharm. Pharmacol. 2012, 64:1138-1145.
16. Sung J.Y., Choi H.C. Aspirin-induced AMP-activated protein kinase activation regulates the proliferation of vascular smooth muscle cells from spontaneously hypertensive rats. Biochem. Biophys. Res. Commun. 2011, 408:312-317.
17. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
18. Shi Y., Vattem K.M., Sood R., An J., Liang J., Stramm L., Wek R.C. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 1998, 18:7499-7509.
19. Coope A., Milanski M., Arruda A.P., Ignacio-Souza L.M., Saad M.J., Anhe G.F., Velloso L.A. Chaperone insufficiency links TLR4 protein signaling to endoplasmic reticulum stress. J. Biol. Chem. 2012, 287:15580-15589.
20. Zhang X., Zhang G., Zhang H., Karin M., Bai H., Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 2008, 135:61-73.
21. Nakamura T., Furuhashi M., Li P., Cao H., Tuncman G., Sonenberg N., Gorgun C.Z., Hotamisligil G.S. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 2010, 140:338-348.
22. Tobacman J.K., Wallace R.B., Zimmerman M.B. Consumption of carrageenan and other water-soluble polymers used as food additives and incidence of mammary carcinoma. Med. Hypotheses 2001, 56:589-598.
23. Bhattacharyya S.I.O.S., Katyal S., Unterman T, Tobacman J.K. Exposure to the common food additive carrageenan leads to glucose intolerance, insulin resistance and inhibition of insulin signalling in HepG2 cells and C57BL/6J mice. Diabetologia 2012, 55:194-203.
24. Milanski M., Degasperi G., Coope A., Morari J., Denis R., Cintra D.E., Tsukumo D.M., Anhe G., Amaral M.E., Takahashi H.K., Curi R., Oliveira H.C., Carvalheira J.B., Bordin S., Saad M.J., Velloso L.A. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity. J. Neurosci. 2009, 29:359-370.
25. Yuan M., Konstantopoulos N., Lee J., Hansen L., Li Z.W., Karin M., Shoelson S.E. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001, 293:1673-1677.
26. Hardie D.G. Sensing of energy and nutrients by AMP-activated protein kinase. Am. J. Clin. Nutr. 2011, 93. 891S-6.
27. Lu J., Wang Q., Huang L., Dong H., Lin L., Lin N., Zheng F., Tan J. Palmitate causes endoplasmic reticulum stress and apoptosis in human mesenchymal stem cells: prevention by AMPK activator. Endocrinology 2012, 153:5275-5284.
28. Cacicedo J.M., Benjachareonwong S., Chou E., Yagihashi N., Ruderman N.B., Ido Y. Activation of AMP-activated protein kinase prevents lipotoxicity in retinal pericytes. Invest. Ophthalmol. Vis. Sci. 2011, 52:3630-3639.
29. Terai K., Hiramoto Y., Masaki M., Sugiyama S., Kuroda T., Hori M., Kawase I., Hirota H. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell Biol. 2005, 25:9554-9575.
30. Dong Y., Zhang M., Liang B., Xie Z., Zhao Z., Asfa S., Choi H.C., Zou M.H. Reduction of AMP-activated protein kinase alpha2 increases endoplasmic reticulum stress and atherosclerosis in vivo. Circulation 2010, 121:792-803.