New insights into salvianolic acid A action: Regulation of the TXNIP/NLRP3 and TXNIP/ChREBP pathways ameliorates HFD-induced NAFLD in rats

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ding, Chunchun ^a   Zhao, Yan ^a   Shi, Xue ^a   Zhang, Ning ^a   Zu, Guo ^a   Li, Zhenlu ^a   Zhou, Junjun ^a   Gao, Dongyan ^a   Lv, Li ^a   Tian, Xiaofeng ^a   Yao, Jihong ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALKENE; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; CARRIER PROTEIN; CRYOPYRIN; NLRP3 PROTEIN, RAT; POLYPHENOL; SALVIANOLIC ACID; TXNIP PROTEIN, RAT; WBSCR14 PROTEIN, RAT;

ANIMAL; CHEMICALLY INDUCED; DRUG EFFECT; FAT INTAKE; HEP-G2 CELL LINE; HUMAN; LIPID METABOLISM; LIVER; MALE; METABOLISM; NONALCOHOLIC FATTY LIVER; PATHOLOGY; PHARMACOLOGY; RAT; SPRAGUE DAWLEY RAT;

ALKENES; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; DIETARY FATS; HEP G2 CELLS; HUMANS; LIPID METABOLISM; LIVER; MALE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; NON-ALCOHOLIC FATTY LIVER DISEASE; POLYPHENOLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84976574040     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28734     Document Type: Article

References (57)

1. Sattar, N., Forrest, E. & Preiss, D. Non-Alcoholic fatty liver disease. BMJ 349, g4596 (2014).
2. Farrell, G. C. & Larter, C. Z. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43, S99-S112 (2006).
3. Day, C. P. & James, O. F. W. Steatohepatitis: A tale of two "hits"? Gastroenterology 114, 842-845 (1998).
4. Musso, G., Gambino, R. & Cassader, M. Recent insights into hepatic lipid metabolism in non-Alcoholic fatty liver disease (NAFLD). Prog. Lipid Res. 48, 1-26 (2009).
5. Cheung, O. & Sanyal, A. J. Recent advances in nonalcoholic fatty liver disease. Curr. Opin. Gastroenterol. 26, 202-208 (2010).
6. Zhang, X. et al. CXCL10 plays a key role as an inflammatory mediator and a non-invasive biomarker of non-Alcoholic steatohepatitis. J. Hepatol. 61, 1365-1375 (2014).
7. Han, Y. H. et al. RORα decreases oxidative stress through the induction of SOD2 and GPx1 expression and thereby protects against nonalcoholic steatohepatitis in mice. Antioxid. Redox Signal. 21, 2083-2094 (2014).
8. Zhang, X. et al. Reactive oxygen species-induced TXNIP drives fructose-mediated hepatic inflammation and lipid accumulation through NLRP3 inflammasome activation. Antioxid. Redox Signal. 22, 848-870 (2015).
9. Chan, H. L. et al. How should we manage patients with non-Alcoholic fatty liver disease in 2007? J. Gastroenterol. Hepatol. 22, 801-808 (2007).
10. Ahmed, A., Wong, R. J. & Harrison, S. A. Nonalcoholic Fatty Liver Disease review: diagnosis, treatment, and outcomes. Clin. Gastroenterol. Hepatol. 13, 2062-2070 (2015).
11. Lin, T. J., Zhang, K. J. & Liu, G. T. Effects of Salvianolic Acid A on oxygen radicals released by Rat neutrophils and on neutrophil function. Biochem. Pharmacol. 51, 1237-1241 (1996).
12. Zhang, H. et al. Salvianolic acid A protects RPE cells against oxidative stress through activation of Nrf2/HO-1 signaling. Free Radic. Biol. Med. 69, 219-228 (2014).
13. Wang, X. et al. Salvianolic acid A shows selective cytotoxicity against multidrug-resistant MCF-7 breast cancer cells. Anticancer Drugs 26, 210-223 (2015).
14. Dai, J. P. et al. Inhibition of Tanshinone IIA, salvianolic acid A and salvianolic acid B on Areca nut extract-induced oral submucous fibrosis in vitro. Molecules 20, 6794-6807 (2015).
15. Qiang, G. et al. Salvianolic acid A prevents the pathological progression of hepatic fibrosis in high-fat diet-fed and streptozotocininduced diabetic rats. Am. J. Chin. Med. 42, 1183-1198 (2014).
16. Xu, X. et al. Salvianolic acid A preconditioning confers protection against concanavalin A-induced liver injury through SIRT1-mediated repression of p66shc in mice. Toxicol. Appl. Pharmacol. 273, 68-76 (2013).
17. Zeng, W. et al. Inhibition of HMGB1 release via salvianolic acid B-mediated SIRT1 up-regulation protects rats against non-Alcoholic fatty liver disease. Sci. Rep. 5, 16013 (2015).
18. Zhang, Y. et al. Resveratrol improves hepatic steatosis by inducing autophagy through the cAMP signaling pathway. Mol. Nutr. Food Res. 59, 1443-57 (2015).
19. Wang, W. et al. Quercetin and allopurinol reduce liver thioredoxin-interacting protein to alleviate inflammation and lipid accumulation in diabetic rats. Br. J. Pharmacol. 169, 1352-1371 (2013).
20. Shan, W. et al. Activation of the SIRT1/p66shc antiapoptosis pathway via carnosic acid-induced inhibition of miR-34a protects rats against nonalcoholic fatty liver disease. Cell Death Dis. 6, e1833 (2015).
21. Lu, J. & Holmgren, A. The thioredoxin antioxidant system. Free Radic. Biol. Med. 66, 75-87 (2014).
22. Hwang, J. et al. The structural basis for the negative regulation of thioredoxin by thioredoxin-interacting protein. Nat. Commun. 5, 2958 (2014).
23. Zhou, J. & Chng, W. J. Roles of thioredoxin binding protein (TXNIP) in oxidative stress, apoptosis and cancer. Mitochondrion 13, 163-169 (2013).
24. Park, M. J. et al. Thioredoxin-interacting protein mediates hepatic lipogenesis and inflammation via PRMT1 and PGC-1α regulation in vitro and in vivo. J. Hepatol. 61, 1151-1157 (2014).
25. Ahsan, M. K. et al. Thioredoxin-binding protein-2 deficiency enhances methionine-choline-deficient diet-induced hepatic steatosis but inhibits steatohepatitis in mice. Antioxid. Redox Signal. 11, 2573-2584(2009).
26. Zhou, R., Tardivel, A., Thorens, B., Choi, I. & Tschopp, J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136-140 (2010).
27. Henao-Mejia, J. et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482, 179-185 (2012).
28. Schroder, K. & Tschopp, J. The inflammasomes. Cell 140, 821-832 (2010).
29. Tack, C. J., Stienstra, R., Joosten, L. A. & Netea, M. G. Inflammation links excess fat to insulin resistance: The role of the interleukin-1 family. Immunol. Rev. 249, 239-252 (2012).
30. Mehal, W. Z. Constitutive NLRP3 activation: Too much of a bad thing. Hepatology 59, 761-763 (2014).
31. Hari, A. et al. Activation of NLRP3 inflammasome by crystalline structures via cell surface contact. Sci. Rep. 4, 7281 (2014).
32. Wen, H., Ting, J. P. & ONeill, L. A. A role for the NLRP3 inflammasome in metabolic diseases-did Warburg miss inflammation? Nat. Immunol. 13, 352-357 (2012).
33. Strable, M. S. & Ntambi, J. M. Genetic control of de novo lipogenesis: role in diet-induced obesity. Crit. Rev. Biochem. Mol. Biol. 45, 199-214 (2010).
34. Charlton, M. R. ChREBP in Nash-A liver transcription factor comes in from the cold. J. Hepatol. 59, 178-179 (2013).
35. Filhoulaud, G., Guilmeau, S., Dentin, R., Girard, J. & Postic, C. Novel insights into ChREBP regulation and function. Trends Endocrinol. Metab. 24, 257-268 (2013).
36. Chen, J., Jing, G., Xu, G. & Shalev, A. Thioredoxin-interacting protein stimulates its own expression via a positive feedback loop. Mol. Endocrinol. 28, 674-680 (2014).
37. Rolo, A. P., Teodoro, J. S. & Palmeira, C. M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic. Biol. Med. 52, 59-69 (2012).
38. Leamy, A. K., Egnatchik, R. A. & Young, J. D. Molecular mechanisms and the role of saturated fatty acids in the progression of nonalcoholic fatty liver disease. Prog. Lipid Res. 52, 165-174 (2013).
39. Hall, L. J. et al. Induction and activation of adaptive immune populations during acute and chronic phases of a murine model of experimental colitis. Dig. Dis. Sci. 56, 79-89 (2011).
40. Ishrat, T. et al. Thioredoxin-interacting protein: A novel target for neuroprotection in experimental thromboembolic stroke in mice. Mol. Neurobiol. 51, 766-778 (2015).
41. Yang, S. J. & Lim, Y. Resveratrol ameliorates hepatic metaflammation and inhibits NLRP3 inflammasome activation. Metabolism 63, 693-701 (2014).
42. Liu, Y. et al. TXNIP mediates NLRP3 inflammasome activation in cardiac microvascular endothelial cells as a novel mechanism in myocardial ischemia/reperfusion injury. Basic Res Cardiol. 109(5), 415 (2014).
43. Dentin, R. et al. Liver-specific inhibition of ChREBP improves hepatic steatosis and insulin resistance in ob/ob mice. Diabetes 55, 2159-2170 (2006).
44. Dentin, R. et al. Polyunsaturated fatty acids suppress glycolytic and lipogenic genes through the inhibition of ChREBP nuclear protein translocation. J. Clin. Invest. 115, 2843-2854 (2005).
45. Guo, T. et al. Berberine ameliorates hepatic steatosis and suppresses liver and adipose tissue inflammation in mice with diet-induced obesity. Sci. Rep. 6, 22612 (2016).
46. Fan, H. Y. et al. Salvianolic acid A as a multifunctional agent ameliorates doxorubicin-induced nephropathy in rats. Sci. Rep. 5, 12273 (2015).
47. Strowig, T., Henao-Mejia, J., Elinav, E. & Flavell, R. Inflammasomes in health and disease. Nature 481, 278-286 (2012).
48. Benhamed, F. et al. The lipogenic transcription factor ChREBP dissociates hepatic steatosis from insulin resistance in mice and humans. J. Clin. Invest. 122, 2176-2194 (2012).
49. Bricambert, J. et al. Salt-inducible kinase 2 links transcriptional coactivator p300 phosphorylation to the prevention of ChREBPdependent hepatic steatosis in mice. J. Clin. Invest. 120, 4316-4331 (2010).
50. Guinez, C. et al. O-GlcNAcylation increases ChREBP protein content and transcriptional activity in the liver. Diabetes 60, 1399-1413 (2011).
51. Dentin, R. et al. Glucose 6-phosphate, rather than xylulose 5-phosphate, is required for the activation of ChREBP in response to glucose in the liver. J. Hepatol. 56, 199-209 (2012).
52. Postic, C., Dentin, R., Denechaud, P. D. & Girard, J. ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu. Rev. Nutr. 27, 179-192 (2007).
53. Wang, P. et al. Salvianolic acid B inhibited PPARγ expression and attenuated weight gain in mice with high-fat diet-induced obesity. Cell. Physiol. Biochem. 34, 288-98 (2014).
54. Li, L. et al. Obesity is an independent risk factor for non-Alcoholic fatty liver disease: evidence from a meta-Analysis of 21 cohort studies. Obes. Rev. 17, 510-519, doi: 10.1111/obr.12407 (2016).
55. Woo Baidal, J. A. & Lavine, J. E. The intersection of nonalcoholic fatty liver disease and obesity. Sci. Transl. Med. 8, 323rv1 (2016).
56. Kleiner, D. E. et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321 (2005).
57. Yao, Z. et al. P311 promotes renal fibrosis via TGFβ1/Smad signaling. Sci. Rep. 5, 17032 (2015).