Saturated fatty acids activate ERK signaling to downregulate hepatic sortilin 1 in obese and diabetic mice

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2754-2762

  Bi, Lipeng ^a   Chiang, John Y L ^b   Ding, Wen Xing ^a   Dunn, Winston ^c   Roberts, Benjamin ^c   Li, Tiangang ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b Northeast Ohio Medical University   (United States)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Diabetes; Extracellular signal regulated kinase; Fatty liver; Lipid metabolism; Mitogen activated protein kinase; Obesity

Indexed keywords

MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; SATURATED FATTY ACID; SORTILIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DOWN REGULATION; DYSLIPIDEMIA; ENZYME ACTIVATION; FATTY LIVER; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SORT1 GENE; TRIACYLGLYCEROL BLOOD LEVEL; UBIQUITINATION;

DIABETES; EXTRACELLULAR SIGNAL-REGULATED KINASE; FATTY LIVER; LIPID METABOLISM; MITOGEN-ACTIVATED PROTEIN KINASE; OBESITY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DOWN-REGULATION; DYSLIPIDEMIAS; FATTY ACIDS, NONESTERIFIED; FATTY LIVER; GENE EXPRESSION REGULATION; HEP G2 CELLS; HUMANS; LIVER; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; PALMITIC ACID; PROTEOLYSIS; RNA, MESSENGER;

EID: 84884128246     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M039347     Document Type: Article

References (35)

1. Reaven, G. M. 2002. Multiple CHD risk factors in type 2 diabetes: beyond hyperglycaemia. Diabetes Obes. Metab. 4 (Suppl. 1) : S13 - S18.
2. Adiels, M., J. Boren, M. J. Caslake, P. Stewart, A. Soro, J. Westerbacka, B. Wennberg, S. O. Olofsson, C. Packard, and M. R. Taskinen. 2005. Overproduction of VLDL1 driven by hyperglycemia is a dominant feature of diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol. 25: 1697-1703.
3. Boden, G., and G. I. Shulman. 2002. Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur. J. Clin. Invest. 32 (Suppl. 3) : 14-23.
4. Steinberg, H. O., and A. D. Baron. 2002. Vascular function, insulin resistance and fatty acids. Diabetologia. 45: 623-634.
5. Tripathy, D., A. Aljada, and P. Dandona. 2003. Free fatty acids (FFA) and endothelial dysfunction; role of increased oxidative stress and inflammation. [Comment on Steinberg, et al. 2002. Vascular function, insulin resistance and fatty acids. Diabetologia. 45: 623-634.]. Diabetologia. 46: 300-301.
6. Liu, L., Y. Li, C. Guan, K. Li, C. Wang, R. Feng, and C. Sun. 2010. Free fatty acid metabolic profile and biomarkers of isolated postchallenge diabetes and type 2 diabetes mellitus based on GC-MS and multivariate statistical analysis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 878: 2817-2825.
7. Cusi, K. 2012. Role of obesity and lipotoxicity in the development of nonalcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology. 142: 711-725.e716.
8. Griffin, M. E., M. J. Marcucci, G. W. Cline, K. Bell, N. Barucci, D. Lee, L. J. Goodyear, E. W. Kraegen, M. F. White, and G. I. Shulman. 1999. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 48: 1270-1274.
9. Lewis, G. F., and G. Steiner. 1996. Acute effects of insulin in the control of VLDL production in humans. Implications for the insulin- resistant state. Diabetes Care. 19: 390-393.
10. Taghibiglou, C., F. Rashid-Kolvear, S. C. Van Iderstine, H. Le-Tien, I. G. Fantus, G. F. Lewis, and K. Adeli. 2002. Hepatic very low density lipoprotein-ApoB overproduction is associated with attenuated hepatic insulin signaling and overexpression of protein-tyrosine phosphatase 1B in a fructose-fed hamster model of insulin resistance. J. Biol. Chem. 277: 793-803.
11. Hermey, G. 2009. The Vps10p-domain receptor family. Cell. Mol. Life Sci. 66: 2677-2689.
12. Musunuru, K., A. Strong, M. Frank-Kamenetsky, N. E. Lee, T. Ahfeldt, K. V. Sachs, X. Li, H. Li, N. Kuperwasser, V. M. Ruda, et al. 2010. From noncoding variant to phenotype via SORT1 at the 1p13 cholesterol locus. Nature. 466: 714-719.
13. Kjolby, M., O. M. Andersen, T. Breiderhoff, A. W. Fjorback, K. M. Pedersen, P. Madsen, P. Jansen, J. Heeren, T. E. Willnow, and A. Nykjaer. 2010. Sort1, encoded by the cardiovascular risk locus 1p13.3, is a regulator of hepatic lipoprotein export. Cell Metab. 12: 213-223.
14. Strong, A., Q. Ding, A. C. Edmondson, J. S. Millar, K. V. Sachs, X. Li, A. Kumaravel, M. Y. Wang, D. Ai, L. Guo, et al. 2012. Hepatic sortilin regulates both apolipoprotein B secretion and LDL catabolism. J. Clin. Invest. 122: 2807-2816.
15. Linsel-Nitschke, P., J. Heeren, Z. Aherrahrou, P. Bruse, C. Gieger, T. Illig, H. Prokisch, K. Heim, A. Doering, A. Peters, et al. 2010. Genetic variation at chromosome 1p13.3 affects sortilin mRNA expression, cellular LDL-uptake and serum LDL levels which translates to the risk of coronary artery disease. Atherosclerosis. 208: 183-189.
16. Lim, K. L., K. C. Chew, J. M. Tan, C. Wang, K. K. Chung, Y. Zhang, Y. Tanaka, W. Smith, S. Engelender, C. A. Ross, et al. 2005. Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J. Neurosci. 25: 2002-2009.
17. Twisk, J., D. L. Gillian-Daniel, A. Tebon, L. Wang, P. H. Barrett, and A. D. Attie. 2000. The role of the LDL receptor in apolipoprotein B secretion. J. Clin. Invest. 105: 521-532.
18. Li, T., E. Owsley, M. Matozel, P. Hsu, C. M. Novak, and J. Y. Chiang. 2010. Transgenic expression of cholesterol 7alpha-hydroxylase in the liver prevents high-fat diet-induced obesity and insulin resistance in mice. Hepatology. 52: 678-690.
19. Kamagate, A., S. Qu, G. Perdomo, D. Su, D. H. Kim, S. Slusher, M. Meseck, and H. H. Dong. 2008. FoxO1 mediates insulin-dependent regulation of hepatic VLDL production in mice. J. Clin. Invest. 118: 2347-2364.
20. Roden, M. 2006. Mechanisms of disease: hepatic steatosis in type 2 diabetes-pathogenesis and clinical relevance. Nat. Clin. Pract. Endocrinol. Metab. 2: 335-348.
21. Chavez, J. A., and S. A. Summers. 2012. A ceramide-centric view of insulin resistance. Cell Metab. 15: 585-594.
22. Fisher, E. A. 2012. The degradation of apolipoprotein B100: multiple opportunities to regulate VLDL triglyceride production by different proteolytic pathways. Biochim. Biophys. Acta. 1821: 778-781.
23. Cohen, J. C., J. D. Horton, and H. H. Hobbs. 2011. Human fatty liver disease: old questions and new insights. Science. 332: 1519-1523.
24. Fujishiro, M., Y. Gotoh, H. Katagiri, H. Sakoda, T. Ogihara, M. Anai, Y. Onishi, H. Ono, M. Abe, N. Shojima, et al. 2003. Three mitogen- activated protein kinases inhibit insulin signaling by different mechanisms in 3T3-L1 adipocytes. Mol. Endocrinol. 17: 487-497.
25. Tan, Y., T. Ichikawa, J. Li, Q. Si, H. Yang, X. Chen, C. S. Goldblatt, C. J. Meyer, X. Li, L. Cai, and T. Cui. 2011. Diabetic downregulation of Nrf2 activity via ERK contributes to oxidative stress-induced insulin resistance in cardiac cells in vitro and in vivo. Diabetes. 60: 625-633.
26. Izawa, Y., M. Yoshizumi, Y. Fujita, N. Ali, Y. Kanematsu, K. Ishizawa, K. Tsuchiya, T. Obata, Y. Ebina, S. Tomita, and T. Tamaki. 2005. ERK1/2 activation by angiotensin II in hibits insulin-induced glucose uptake in vascular smooth muscle cells. Exp. Cell Res. 308: 291-299.
27. Zheng, Y., W. Zhang, E. Pendleton, S. Leng, J. Wu, R. Chen, and X. J. Sun. 2009. Improved insulin sensitivity by calorie restriction is associated with reduction of ERK and p70S6K activities in the liver of obese Zucker rats. J. Endocrinol. 203: 337-347.
28. Lee, S. J., P. T. Pfluger, J. Y. Kim, R. Nogueiras, A. Duran, G. Pages, J. Pouyssegur, M. H. Tschop, M. T. Diaz-Meco, and J. Moscat. 2010. A functional role for the p62-ERK1 axis in the control of energy homeostasis and adipogenesis. EMBO Rep. 11: 226-232.
29. Jiang, X. C., I. J. Goldberg, and T. S. Park. 2011. Sphingolipids and cardiovascular diseases: lipoprotein metabolism, atherosclerosis and cardiomyopathy. Adv. Exp. Med. Biol. 721: 19-39.
30. Fox, T. E., M. C. Bewley, K. A. Unrath, M. M. Pedersen, R. E. Anderson, D. Y. Jung, L. S. Jefferson, J. K. Kim, S. K. Bronson, J. M. Flanagan, and M. Kester. 2011. Circulating sphingolipid biomarkers in models of type 1 diabetes. J. Lipid Res. 52: 509-517.
31. Boon, J., A. J. Hoy, R. Stark, R. D. Brown, R. C. Meex, D. C. Henstridge, S. Schenk, P. J. Meikle, J. F. Horowitz, B. A. Kingwell, et al. 2013. Ceramides contained in LDL are elevated in type 2 diabetes and promote inflammation and skeletal muscle insulin resistance. Diabetes. 62: 401-410.
32. Dumaresq-Doiron, K., F. Jules, and S. Lefrancois. 2013. Sortilin turnover is mediated by ubiquitination. Biochem. Biophys. Res. Commun. 433: 90-95.
33. Gentile, C. L., M. A. Frye, and M. J. Pagliassotti. 2011. Fatty acids and the endoplasmic reticulum in nonalcoholic fatty liver disease. Biofactors. 37: 8-16.
34. Wei, Y., D. Wang, F. Topczewski, and M. J. Pagliassotti. 2006. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am. J. Physiol. Endocrinol. Metab. 291: E275 - E281.
35. Ai, D., J. M. Baez, H. Jiang, D. M. Conlon, A. Hernandez-Ono, M. Frank-Kamenetsky, S. Milstein, K. Fitzgerald, A. J. Murphy, C. W. Woo, et al. 2012. Activation of ER stress and mTORC1 suppresses hepatic sortilin-1 levels in obese mice. J. Clin. Invest. 122: 1677-1687.