Astaxanthin prevents and reverses diet-induced insulin resistance and steatohepatitis in mice: A comparison with Vitamin E

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Ni, Yinhua ^a   Nagashimada, Mayumi ^a   Zhuge, Fen ^a   Zhan, Lili ^a   Nagata, Naoto ^a   Tsutsui, Akemi ^a   Nakanuma, Yasuni ^a   Kaneko, Shuichi ^a   Ota, Tsuguhito ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASTAXANTHIN; SREBF1 PROTEIN, MOUSE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; XANTHOPHYLL;

ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENETICS; GLUCOSE METABOLISM DISORDERS; HUMAN; IMMUNOLOGY; INSULIN RESISTANCE; KUPFFER CELL; LIPID DIET; LIPID PEROXIDATION; LIVER; MACROPHAGE; MALE; METABOLISM; MOUSE; MOUSE MUTANT; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY;

ANIMALS; ANTIOXIDANTS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; GLUCOSE METABOLISM DISORDERS; HUMANS; INSULIN RESISTANCE; KUPFFER CELLS; LIPID PEROXIDATION; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; NON-ALCOHOLIC FATTY LIVER DISEASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; VITAMIN E; XANTHOPHYLLS;

EID: 84948456496     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17192     Document Type: Article

References (44)

1. Marchesini, G. et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37, 917-923 (2003).
2. Farrell, G. C. & Larter, C. Z. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43, S99-S112 (2006).
3. Chalasani, N. et al. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55, 2005-2023 (2012).
4. Cusi, K. Role of obesity and lipotoxicity in the development of nonalcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology 142, 711-725 e716 (2012).
5. Matsuzawa, N. et al. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46, 1392-1403 (2007).
6. Ratziu, V. Pharmacological agents for NASH. Nature reviews Gastroenterology & hepatology 10, 676-685 (2013).
7. Sanyal, A. J. et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med 362, 1675-1685 (2010).
8. Leo, M. A., Rosman, A. S. & Lieber, C. S. Differential depletion of carotenoids and tocopherol in liver disease. Hepatology 17, 977-986 (1993).
9. Yadav, D., Hertan, H. I., Schweitzer, P., Norkus, E. P. & Pitchumoni, C. S. Serum and liver micronutrient antioxidants and serum oxidative stress in patients with chronic hepatitis C. The American Journal of Gastroenterology 97, 2634-2639 (2002).
10. Ruhl, C. E. & Everhart, J. E. Relation of elevated serum alanine aminotransferase activity with iron and antioxidant levels in the United States. Gastroenterology 124, 1821-1829 (2003).
11. Erhardt, A., Stahl, W., Sies, H., Lirussi, F., Donner, A. & Haussinger, D. Plasma levels of vitamin E and carotenoids are decreased in patients with Nonalcoholic Steatohepatitis (NASH). European Journal of Medical Research 16, 76-78 (2011).
12. Upritchard, J. E. et al. Spread supplemented with moderate doses of vitamin E and carotenoids reduces lipid peroxidation in healthy, nonsmoking adults. Am J Clin Nutr 78, 985-992 (2003).
13. Rock, C. L., Jacob, R. A. & Bowen, P. E. Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E, and the carotenoids. Journal of the American Dietetic Association 96, 693-702, quiz 703-694 (1996).
14. Kobori, M et al.-Cryptoxanthin Alleviates Diet-Induced Nonalcoholic Steatohepatitis by Suppressing Inflammatory Gene Expression in Mice. PLoS One 9, e98294 (2014).
15. Ni, Y. et al. Prevention and reversal of lipotoxicity-induced hepatic insulin resistance and steatohepatitis in mice by an antioxidant carotenoid,-cryptoxanthin. Endocrinology 156, 987-999 (2015).
16. Ambati, R. R., Phang, S. M., Ravi, S. & Aswathanarayana, R. G. Astaxanthin: sources, extraction, stability, biological activities and its commercial applications-a review. Mar Drugs 12, 128-152 (2014).
17. Kurashige, M., Okimasu, E., Inoue, M. & Utsumi, K. Inhibition of oxidative injury of biological membranes by astaxanthin. Physiological chemistry and physics and medical NMR 22, 27-38 (1990).
18. Guerin, M., Huntley, M. E. & Olaizola, M. Haematococcus astaxanthin: applications for human health and nutrition. Trends in Biotechnology 21, 210-216 (2003).
19. Kang, J. O., Kim, S. J. & Kim, H. Effect of astaxanthin on the hepatotoxicity, lipid peroxidation and antioxidative enzymes in the liver of CCl4-treated rats. Methods and Findings in Experimental and Clinical Pharmacology 23, 79-84 (2001).
20. Yang, Y., Kim, B., Park, Y. K., Koo, S. I. & Lee, J. Y. Astaxanthin prevents TGF? 1-induced pro-fibrogenic gene expression by inhibiting Smad3 activation in hepatic stellate cells. Biochimica et biophysica acta 1850, 178-185 (2015).
21. Ikeuchi, M., Koyama, T., Takahashi, J. & Yazawa, K. Effects of astaxanthin in obese mice fed a high-fat diet. Biosci Biotechnol Biochem 71, 893-899 (2007).
22. Ishiki, M. et al. Impact of divergent effects of astaxanthin on insulin signaling in L6 cells. Endocrinology 154, 2600-2612 (2013).
23. Odegaard, J. I. et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 7, 496-507 (2008).
24. Lumeng, C. N., Bodzin, J. L. & Saltiel, A. R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117, 175-184 (2007).
25. Sica, A., Invernizzi, P. & Mantovani, A. Macrophage plasticity and polarization in liver homeostasis and pathology. Hepatology 59, 2034-2042 (2014).
26. Kitade, H. et al. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61, 1680-1690 (2012).
27. Wan, J et al. M2 Kupffer cells promote M1 Kupffer cell apoptosis: a protective mechanism against alcoholic and nonalcoholic fatty liver disease. Hepatology 59, 130-142 (2014).
28. Han, M. S. et al. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science 339, 218-222 (2013).
29. Sell, H., Habich, C. & Eckel, J. Adaptive immunity in obesity and insulin resistance. Nature reviews Endocrinology 8, 709-716 (2012).
30. Sutti, S. et al. Adaptive immune responses triggered by oxidative stress contribute to hepatic inflammation in NASH. Hepatology 59, 886-897 (2014).
31. Showalter, L. A., Weinman, S. A., Osterlie, M. & Lockwood, S. F. Plasma appearance and tissue accumulation of non-esterified, free astaxanthin in C57BL/6 mice after oral dosing of a disodium disuccinate diester of astaxanthin (Heptax). Comparative Biochemistry and Physiology Toxicology & Pharmacology: CBP 137, 227-236 (2004).
32. Ota, T., Gayet, C. & Ginsberg, H. N. Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents. The Journal of Clinical Investigation 118, 316-332 (2008).
33. Nakamura, S. et al. Palmitate induces insulin resistance in H4IIEC3 hepatocytes through reactive oxygen species produced by mitochondria. The Journal of Biological Chemistry 284, 14809-14818 (2009).
34. Guy, C. D., Suzuki, A., Abdelmalek, M. F., Burchette, J. L. & Diehl, A. M., for the NC. Treatment response in the PIVENS trial is associated with decreased hedgehog pathway activity. Hepatology 61, 98-107 (2015).
35. von Lintig, J. Provitamin A metabolism and functions in mammalian biology. The American Journal of Clinical Nutrition 96, 1234S-1244S (2012).
36. Vine, A. L. & Bertram, J. S. Upregulation of connexin 43 by retinoids but not by non-provitamin A carotenoids requires RARs. Nutr Cancer 52, 105-113 (2005).
37. Sayo, T., Sugiyama, Y. & Inoue, S. Lutein, a nonprovitamin A, activates the retinoic acid receptor to induce HAS3-dependent hyaluronan synthesis in keratinocytes. Biosci Biotechnol Biochem 77, 1282-1286 (2013).
38. Chung, M. Y., Yeung, S. F., Park, H. J., Volek, J. S. & Bruno, R. S. Dietary alpha-and gamma-tocopherol supplementation attenuates lipopolysaccharide-induced oxidative stress and inflammatory-related responses in an obese mouse model of nonalcoholic steatohepatitis. J Nutr Biochem 21, 1200-1206 (2010).
39. McNulty, H. P., Byun, J., Lockwood, S. F., Jacob, R. F. & Mason, R. P. Differential effects of carotenoids on lipid peroxidation due to membrane interactions: X-ray diffraction analysis. Biochimica et biophysica acta 1768, 167-174 (2007).
40. Neuschwander-Tetri, B. A. et al. Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): a multicentre, randomised, placebo-controlled trial. Lancet 385, 956-965 (2015).
41. Ota, T. et al. Insulin resistance accelerates a dietary rat model of nonalcoholic steatohepatitis. Gastroenterology 132, 282-293 (2007).
42. Uchinami, H., Seki, E., Brenner, D. A. & D'Armiento, J. Loss of MMP 13 attenuates murine hepatic injury and fibrosis during cholestasis Hepatology 44 420-429 (2006).
43. Kimura, K. et al. Endoplasmic reticulum stress inhibits STAT3-dependent suppression of hepatic gluconeogenesis via dephosphorylation and deacetylation. Diabetes 61, 61-73 (2012).
44. Kleiner, D. E. et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321 (2005).