Activation of Sphingosine Kinase 2 by Endoplasmic Reticulum Stress Ameliorates Hepatic Steatosis and Insulin Resistance in Mice

Hepatology

Volumn 62, Issue 1, 2015, Pages 135-146

  Lee, Su Yeon ^a   Hong, In Kyung ^a   Kim, Bo Rahm ^a   Shim, Soon Mi ^b   Sung Lee, Jae ^a   Lee, Hui Young ^a   Soo Choi, Cheol ^a   Kim, Bo Kyung ^c   Park, Tae Sik ^a  

^a Gachon University   (South Korea)

^b Sejong University   (South Korea)

^c Konkuk University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ACYL COENZYME A; ACYL COENZYME A OXIDASE; ALANINE AMINOTRANSFERASE; C/EBP HOMOLOGOUS PROTEIN; CARBOXYLASE; CARNITINE PALMITOYLTRANSFERASE I; CERAMIDE; CHOLESTEROL; DIACYLGLYCEROL ACYLTRANSFERASE; DIACYLGLYCEROL ACYLTRANSFERASE 2; ENDOTOXIN; FAT DROPLET; GLUCOSYLCERAMIDE; INSULIN; INSULIN RECEPTOR SUBSTRATE; LIPOPOLYSACCHARIDE; LOW DENSITY LIPOPROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN KINASE B; SMALL INTERFERING RNA; SPHINGOMYELIN; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 2; SPLICED X BOX BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; ATF4 PROTEIN, MOUSE; FATTY ACID; LIPID; LYSOPHOSPHOLIPID; PHOSPHOTRANSFERASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME REGULATION; FATTY ACID OXIDATION; FATTY LIVER; GENETIC TRANSFECTION; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; HISTOPATHOLOGY; IMMUNOBLOTTING; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN RESPONSE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; LIPID DIET; LIPID LIVER LEVEL; LIPID STORAGE; LIPOGENESIS; LIVER CELL; LUCIFERASE ASSAY; MALE; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; UNFOLDED PROTEIN RESPONSE; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; ENZYMOLOGY; LIVER; METABOLISM; OXIDATION REDUCTION REACTION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; CELLS, CULTURED; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS; FATTY LIVER; HEPATOCYTES; INSULIN RESISTANCE; LIPID DROPLETS; LIPIDS; LIVER; LYSOPHOSPHOLIPIDS; MALE; MICE, INBRED C57BL; OXIDATION-REDUCTION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTO-ONCOGENE PROTEINS C-AKT; SPHINGOSINE; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84933181968     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27804     Document Type: Article

References (40)

1. Barr EL, Cameron AJ, Balkau B, Zimmet PZ, Welborn TA, Tonkin AM, Shaw JE. HOMA insulin sensitivity index and the risk of all-cause mortality and cardiovascular disease events in the general population: the Australian Diabetes, Obesity and Lifestyle Study (AusDiab) study. Diabetologia 2010;53:79-88.
2. Hastie CE, Padmanabhan S, Slack R, Pell AC, Oldroyd KG, Flapan AD, et al. Obesity paradox in a cohort of 4880 consecutive patients undergoing percutaneous coronary intervention. Eur Heart J 2010;31:222-226.
3. Roberts AW, Clark AL, Witte KK. Review article: left ventricular dysfunction and heart failure in metabolic syndrome and diabetes without overt coronary artery disease-do we need to screen our patients? Diab Vasc Dis Res 2009;6:153-163.
4. Bradbury MW. Lipid metabolism and liver inflammation. I. Hepatic fatty acid uptake: possible role in steatosis. Am J Physiol Gastrointest Liver Physiol 2006;290:G194-G198.
5. Zhou YT, Grayburn P, Karim A, Shimabukuro M, Higa M, Baetens D, et al. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci U S A 2000;97:1784-1789.
6. Unger RH. Lipid overload and overflow: metabolic trauma and the metabolic syndrome. Trends Endocrinol Metab 2003;14:398-403.
7. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Jr., Ory DS, Schaffer JE. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 2003;100:3077-3082.
8. Chavez JA, Summers SA. 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 2003;419:101-109.
9. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, Liu Y, et al. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 2007;5:167-179.
10. Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, et al. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 2002;277:50230-50236.
11. Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest 2002;110:1389-1398.
12. Hampton RY. ER stress response: getting the UPR hand on misfolded proteins. Curr Biol 2000;10:R518-R521.
13. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005;74:739-789.
14. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol 2011;54:795-809.
15. Winnay JN, Boucher J, Mori MA, Ueki K, Kahn CR. A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat Med 2010;16:438-445.
16. Wang Y, Vera L, Fischer WH, Montminy M. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 2009;460:534-537.
17. Park SW, Zhou Y, Lee J, Lu A, Sun C, Chung J, et al. The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation. Nat Med 2010;16:429-437.
18. Maceyka M, Payne SG, Milstien S, Spiegel S. Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 2002;1585:193-201.
19. Taha TA, Hannun YA, Obeid LM. Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 2006;39:113-131.
20. Billich A, Bornancin F, Devay P, Mechtcheriakova D, Urtz N, Baumruker T. Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J Biol Chem 2003;278:47408-47415.
21. Kihara A, Anada Y, Igarashi Y. Mouse sphingosine kinase isoforms SPHK1a and SPHK1b differ in enzymatic traits including stability, localization, modification, and oligomerization. J Biol Chem 2006;281:4532-4539.
22. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003;4:397-407.
23. Maceyka M, Sankala H, Hait NC, Le Stunff H, Liu H, Toman R, et al. SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J Biol Chem 2005;280:37118-37129.
24. Renton KW, Deloria LB, Mannering GJ. Effects of polyribonoinosinic acid polyribocytidylic acid and a mouse interferon preparation on cytochrome P-450-dependent monooxygenase systems in cultures of primary mouse hepatocytes. Mol Pharmacol 1978;14:672-681.
25. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, et al. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2007;2:1236-1247.
26. Lee SY, Kim JR, Hu Y, Khan R, Kim SJ, Bharadwaj KG, et al. Cardiomyocyte specific deficiency of serine palmitoyltransferase subunit 2 reduces ceramide but leads to cardiac dysfunction. J Biol Chem 2012;287:18429-18439.
27. Ryu D, Seo WY, Yoon YS, Kim YN, Kim SS, Kim HJ, et al. Endoplasmic reticulum stress promotes LIPIN2-dependent hepatic insulin resistance. Diabetes 2011;60:1072-1081.
28. Summers SA. Sphingolipids and insulin resistance: the five Ws. Curr Opin Lipidol 2010;21:128-135.
29. Ma MM, Chen JL, Wang GG, Wang H, Lu Y, Li JF, et al. Sphingosine kinase 1 participates in insulin signalling and regulates glucose metabolism and homeostasis in KK/Ay diabetic mice. Diabetologia 2007;50:891-900.
30. Nakagawa Y, Shimano H, Yoshikawa T, Ide T, Tamura M, Furusawa M, et al. TFE3 transcriptionally activates hepatic IRS-2, participates in insulin signaling and ameliorates diabetes. Nat Med 2006;12:107-113.
31. Liu K, Guo TL, Hait NC, Allegood J, Parikh HI, Xu W, et al. Biological characterization of 3-(2-amino-ethyl)-5-[3-(4-butoxyl-phenyl)-propylidene]-thiazolidine-2, 4-dione (K145) as a selective sphingosine kinase-2 inhibitor and anticancer agent. PLoS One 2013;8:e56471.
32. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010;140:900-917.
33. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 2008;320:1492-1496.
34. Seo J, Fortuno ES, 3rd, Suh JM, Stenesen D, Tang W, Parks EJ, et al. Atf4 regulates obesity, glucose homeostasis, and energy expenditure. Diabetes 2009;58:2565-2573.
35. Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, et al. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 2004;24:10161-10168.
36. Hannun YA, Luberto C, Argraves KM. Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 2001;40:4893-4903.
37. Park TS, Panek RL, Mueller SB, Hanselman JC, Rosebury WS, Robertson AW, et al. Inhibition of sphingomyelin synthesis reduces atherogenesis in apolipoprotein E-knockout mice. Circulation 2004;110:3465-3471.
38. Ussher JR, Koves TR, Cadete VJ, Zhang L, Jaswal JS, Swyrd SJ, et al. Inhibition of de novo ceramide synthesis reverses diet-induced insulin resistance and enhances whole-body oxygen consumption. Diabetes 2010;59:2453-2464.
39. Li Z, Zhang H, Liu J, Liang CP, Li Y, Teitelman G, et al. Reducing plasma membrane sphingomyelin increases insulin sensitivity. Mol Cell Biol 2011;31:4205-4218.
40. Guan H, Song L, Cai J, Huang Y, Wu J, Yuan J, et al. Sphingosine kinase 1 regulates the Akt/FOXO3a/Bim pathway and contributes to apoptosis resistance in glioma cells. PLoS One 2011;6:e19946.