Activation of hepatic CREBH and Insig signaling in the anti-hypertriglyceridemic mechanism of R-α-lipoic acid

Journal of Nutritional Biochemistry

Volumn 26, Issue 9, 2015, Pages 921-928

  Tong, Xuedong ^a,b   Christian, Patricia ^b   Zhao, Miaoyun ^b   Wang, Hai ^b   Moreau, Regis ^b   Su, Qiaozhu ^b  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Apolipoproteins; Cell signaling; Dyslipidemias; Sterol regulatory element binding proteins; Triglyceride metabolism; Very low density lipoprotein

Indexed keywords

APOLIPOPROTEIN B100; APOLIPOPROTEIN E; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN H; GLUCOSE; INDAPAMIDE; INDAPAMIDE 1; INDAPAMIDE 2A; INDAPAMIDE 2B; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; THIOCTIC ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; ANTILIPEMIC AGENT; CREBH PROTEIN, RAT; INSIG-2 PROTEIN, RAT; INSIG1 PROTEIN, RAT; MEMBRANE PROTEIN; SIGNAL PEPTIDE; SREBF1 PROTEIN, RAT; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL METABOLISM; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG MECHANISM; FATTY ACID SYNTHESIS; GENETIC TRANSFECTION; HYPERLIPIDEMIA; HYPERTRIGLYCERIDEMIA; IMMUNOBLOTTING; IN VITRO STUDY; LIPOGENESIS; MALE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TRIACYLGLYCEROL BLOOD LEVEL; AGONISTS; ALTERNATIVE RNA SPLICING; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; BUFFALO RAT; DIET THERAPY; DIETARY SUPPLEMENT; ENZYMOLOGY; GENETICS; LIVER CELL; METABOLISM; PROTEIN PROCESSING; RANDOMIZATION; SECRETION (PROCESS); TUMOR CELL LINE; UPREGULATION; ZUCKER RAT;

RATTUS;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIETARY SUPPLEMENTS; HEPATOCYTES; HYPERTRIGLYCERIDEMIA; HYPOLIPIDEMIC AGENTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPROTEINS, VLDL; MALE; MEMBRANE PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RANDOM ALLOCATION; RATS, INBRED BUF; RATS, ZUCKER; SIGNAL TRANSDUCTION; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; THIOCTIC ACID; UP-REGULATION;

EID: 84983103295     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.03.011     Document Type: Article

References (35)

1. Ginsberg H.N., Zhang Y.L., Hernandez-Ono A. Metabolic syndrome: focus on dyslipidemia. Obesity 2006, 14:41s-49s.
2. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
3. Asada R., Kanemoto S., Kondo S., Saito A., Imaizumi K. The signalling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J Biochem 2011, 149:507-518.
4. Yamamoto K., Sato T., Matsui T., Sato M., Okada T., Yoshida H., et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007, 13:365-376.
5. Bailey D., O'Hare P. Transmembrane bZIP transcription factors in ER stress signaling and the unfolded protein response. Antioxid Redox Signal 2007, 9:2305-2321.
6. Zhang C., Wang G., Zheng Z., Maddipati K.R., Zhang X., Dyson G., et al. Endoplasmic reticulum-tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology 2012, 55:1070-1082.
7. Kondo S., Murakami T., Tatsumi K., Ogata M., Kanemoto S., Otori K., et al. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol 2005, 7:186-194.
8. Liang G., Audas T.E., Li Y., Cockram G.P., Dean J.D., Martyn A.C., et al. Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein Herp through an ER stress response element. Mol Cell Biol 2006, 26:7999-8010.
9. Lee J.H., Giannikopoulos P., Duncan S.A., Wang J., Johansen C.T., Brown J.D., et al. The transcription factor cyclic AMP-responsive element-binding protein H regulates triglyceride metabolism. Nat Med 2011, 17:812-815.
10. Llarena M., Bailey D., Curtis H., O'Hare P. Different mechanisms of recognition and ER retention by transmembrane transcription factors CREB-H and ATF6. Traffic 2010, 11:48-69.
11. Yabe D., Brown M.S., Goldstein J.L. Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins. Proc Natl Acad Sci U S A 2002, 99:12753-12758.
12. Yang T., Espenshade P.J., Wright M.E., Yabe D., Gong Y., Aebersold R., et al. Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell 2002, 110:489-500.
13. Shay K.P., Moreau R.F., Smith E.J., Smith A.R., Hagen T.M. Alpha-lipoic acid as a dietary supplement: molecular mechanisms and therapeutic potential. Biochim Biophys Acta 1790, 2009:1149-1160.
14. Packer L., Kraemer K., Rimbach G. Molecular aspects of lipoic acid in the prevention of diabetes complications. Nutrition 2001, 17:888-895.
15. Pashaj A., Yi X.H., Xia M.N., Canny S., Riethoven J.J.M., Moreau R. Characterization of genome-wide transcriptional changes in liver and adipose tissues of ZDF (fa/fa) rats fed R-alpha-lipoic acid by next-generation sequencing. Physiol Genomics 2013, 45:1136-1143.
16. Butler J.A., Hagen T.M., Moreau R. Lipoic acid improves hypertriglyceridemia by stimulating triacylglycerol clearance and downregulating liver triacylglycerol secretion. Arch Biochem Biophys 2009, 485:63-71.
17. Yi X., Pashaj A., Xia M., Moreau R. Reversal of obesity-induced hypertriglyceridemia by (R)-alpha-lipoic acid in ZDF (fa/fa) rats. Biochem Biophys Res Commun 2013, 439:390-395.
18. Finlay L.A., Michels A.J., Butler J.A., Smith E.J., Monette J.S., Moreau R.F., et al. R-alpha-Lipoic acid does not reverse hepatic inflammation of aging, but lowers lipid anabolism, while accentuating circadian rhythm transcript profiles. Am J Physiol Regul Integr Comp Physiol 2012, 302:R587-R597.
19. Huong D.T., Ide T. Dietary lipoic acid-dependent changes in the activity and mRNA levels of hepatic lipogenic enzymes in rats. Br J Nutr 2008, 100:79-87.
20. Takaishi K., Duplomb L., Wang M.Y., Li J., Unger R.H. Hepatic insig-1 or -2 overexpression reduces lipogenesis in obese Zucker diabetic fatty rats and in fasted/refed normal rats. Proc Natl Acad Sci U S A 2004, 101:7106-7111.
21. Carlson D.A., Smith A.R., Fischer S.J., Young K.L., Packer L. The plasma pharmacokinetics of R-(+)-lipoic acid administered as sodium R-(+)-lipoate to healthy human subjects. Altern Med Rev 2007, 12:343-351.
22. Nakamura T., Furuhashi M., Li P., Cao H., Tuncman G., Sonenberg N., et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 2010, 140:338-348.
23. Su Q.Z., Tsai J., Xu E., Qiu W., Bereczki E., Santha M., et al. Apolipoprotein B100 acts as a molecular link between lipid-induced endoplasmic reticulum stress and hepatic insulin resistance. Hepatology 2009, 50:77-84.
24. Danno H., Ishii K.A., Nakagawa Y., Mikami M., Yamamoto T., Yabe S., et al. The liver-enriched transcription factor CREBH is nutritionally regulated and activated by fatty acids and PPARalpha. Biochem Biophys Res Commun 2010, 391:1222-1227.
25. Gentile C.L., Wang D., Pfaffenbach K.T., Cox R., Wei Y., Pagliassotti M.J. Fatty acids regulate CREBh via transcriptional mechanisms that are dependent on proteasome activity and insulin. Mol Cell Biochem 2010, 344:99-107.
26. Aas V., Kase E.T., Solberg R., Jensen J., Rustan A.C. Chronic hyperglycaemia promotes lipogenesis and triacylglycerol accumulation in human skeletal muscle cells. Diabetologia 2004, 47:1452-1461.
27. Rutledge A.C., Su Q., Adeli K. Apolipoprotein B100 biogenesis: a complex array of intracellular mechanisms regulating folding, stability, and lipoprotein assembly. Biochem Cell Biol 2010, 88:251-267.
28. Mensenkamp A.R., Jong M.C., van G.H., van Luyn M.J., Bloks V., Havinga R., et al. Apolipoprotein E participates in the regulation of very low density lipoprotein-triglyceride secretion by the liver. J Biol Chem 1999, 274:35711-35718.
29. Gong Y., Lee J.N., Lee P.C., Goldstein J.L., Brown M.S., Ye J. Sterol-regulated ubiquitination and degradation of Insig-1 creates a convergent mechanism for feedback control of cholesterol synthesis and uptake. Cell Metab 2006, 3:15-24.
30. Yabe D., Komuro R., Liang G., Goldstein J.L., Brown M.S. Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc Natl Acad Sci U S A 2003, 100:3155-3160.
31. Park K.G., Min A.K., Koh E.H., Kim H.S., Kim M.O., Park H.S., et al. alpha-Lipoic acid decreases hepatic lipogenesis through adenosine mono phosphate-activated protein kinase (AMPK)-dependent and AMPK-independent pathways. Hepatology 2008, 48:1477-1486.
32. Timmers S., Bosch dV-vd, Towler M.C., Schaart G., Moonen-Kornips E., Mensink R.P., et al. Prevention of high-fat diet-induced muscular lipid accumulation in rats by alpha lipoic acid is not mediated by AMPK activation. J Lipid Res 2010, 51:352-359.
33. Dashti N., Gandhi M., Liu X., Lin X., Segrest J.P. The N-terminal 1000 residues of apolipoprotein B associate with microsomal triglyceride transfer protein to create a lipid transfer pocket required for lipoprotein assembly. Biochemistry 2002, 41:6978-6987.
34. Kulinski A., Rustaeus S., Vance J.E. Microsomal triacylglycerol transfer protein is required for lumenal accretion of triacylglycerol not associated with ApoB, as well as for ApoB lipidation. J Biol Chem 2002, 277:31516-31525.
35. Hussain M.M., Rava P., Walsh M., Rana M., Iqbal J. Multiple functions of microsomal triglyceride transfer protein. Nutr Metab (Lond) 2012, 9:14.