Menhaden oil decreases high-fat diet-induced markers of hepatic damage, steatosis, inflammation, and fibrosis in obese Ldlr-/- mice

Journal of Nutrition

Volumn 142, Issue 8, 2012, Pages 1495-1503

  Depner, Christopher M ^a   Torres Gonzalez, Moises ^a,b   Tripathy, Sasmita ^a   Milne, Ginger ^c   Jump, Donald B ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CHOLESTEROL; FAT; FATTY ACID; HEME OXYGENASE 1; LARD; MENHADEN OIL; MONOCYTE CHEMOTACTIC PROTEIN 1; OLIVE OIL; OMEGA 3 FATTY ACID; PROCOLLAGEN; PROCOLLAGEN 1ALPHA1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BODY WEIGHT; CALORIC INTAKE; CHOLESTEROL DIET; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; GENE EXPRESSION; HEPATITIS; INSULIN RESISTANCE; LIPID DIET; LIPID LIVER LEVEL; LIVER FIBROSIS; LIVER INJURY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; OXIDATIVE STRESS; PROTEIN EXPRESSION; STEATOSIS; TRANSCRIPTION REGULATION;

ANIMAL FEED; ANIMALS; BIOLOGICAL MARKERS; CYTOKINES; DIETARY FATS; FATTY LIVER; FISH OILS; GENE EXPRESSION REGULATION; INFLAMMATION; LIPID METABOLISM; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; MICE, OBESE; OXIDATIVE STRESS; RECEPTORS, LDL; TRANSCRIPTION FACTORS;

MUS;

EID: 84866296564     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.112.158865     Document Type: Article

References (64)

1. Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43:S99-112.
2. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science. 2011;332:1519-23.
3. Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of nonalcoholic fatty liver disease. Dig Dis. 2010;28:155-61.
4. Kim CH, Younossi ZM. Nonalcoholic fatty liver disease: a manifestation of the metabolic syndrome. Cleve Clin J Med. 2008;75:721-8.
5. Alberti KG, Zimmet P, Shaw J. The metabolic syndrome-a new world wide definition. Lancet. 2005;366:1059-62.
6. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002;346:1221-31.
7. Hashimoto E, Tokushige K, Farrell GC. Histological features of nonalcoholic fatty liver disease: what is important? J Gastroenterol Hepatol. 2012;27:5-7.
8. McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol. 2006;40 Suppl 1:S17-29.
9. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology. 1998;114:842-5.
10. Larter CZ, Chitturi S, Heydet D, Farrell GC. A fresh look at NASH pathogenesis. Part 1: the metabolic movers. J Gastroenterol Hepatol. 2010;25:672-90.
11. Chan HL, de Silva HJ, Leung NW, Lim SG, Farrell GC. How should we manage patients with non-alcoholic fatty liver disease in 2007? J Gastroenterol Hepatol. 2007;22:801-8.
12. Jump DB. Fatty acid regulation of hepatic gene expression. Curr Opin Clin Nutr Metab Care. 2011;14:115-20.
13. Shearer GC, Savinova OV, Harris WS. Fish oil-how does it reduceplasma triglycerides? Biochim Biophys Acta. 2012; in press.
14. Jump DB. The biochemistry of (n-3) polyunsaturated fatty acids. J Biol Chem. 2002;277:8755-8.
15. Nobili V, Bedogni G, Alisi A, Pietrobattista A, Risé P, Galli C, Agostoni C. Docosahexaenoic acid supplementation decreases liver fat content in children with non-alcoholic fatty liver disease: double-blind randomised controlled clinical trial. Arch Dis Child. 2011;96:350-3.
16. Sofi F, Giangrandi I, Cesari F, Corsani I, Abbate R, Gensini GF, Casini A. Effects of a 1-year dietary intervention with (n-3) polyunsaturated fatty acid-enriched olive oil on non-alcoholic fatty liver disease patients: a preliminary study. Int J Food Sci Nutr. 2010;61:792-802.
17. Bulchandani DG, Nachnani JS, Nookala A, Naumovitch C, Herndon B, Molteni A, Quinn T, Alba LM. Treatment with omega-3 fatty acids but not exendin-4 improves hepatic steatosis. Eur J Gastroenterol Hepatol. 2010;22:1245-52.
18. Oya J, Nakagami T, Sasaki S, Jimba S, Murakami K, Kasahara T, Wasada T, Sekiguchi H, Hasegawa M, Endo Y, et al. Intake of (n-3) polyunsaturated fatty acids and non-alcoholic fatty liver disease: a crosssectional study in Japanese men and women. Eur J Clin Nutr. 2010;64:1179-85.
19. Kishino T, Ohnishi H, Ohtsuka K, Matsushima S, Urata T, Watanebe K, Honda Y, Mine Y, Matsumoto M, Nishikawa K, et al. Low concentrations of serum (n-3) polyunsaturated fatty acids in non-alcoholic fatty liver disease patients with liver injury. Clin Chem Lab Med. 2011;49:159-62.
20. Tripathy S, Torres-Gonzalez M, Jump DB. Elevated hepatic fatty acid elongase-5 (Elovl5) activity corrects dietary fat induced hyperglycemia in obese C57BL/6J mice. J Lipid Res. 2010;51:2642-54.
21. Miller RS, Becker KG, Prabhu V, Cooke DW. Adipocyte gene expression is altered in formerly obese mice as a function of diet composition. J Nutr. 2008;138:1033-8.
22. Saraswathi V, Gao L, Morrow JD, Chait A, Niswender KD, Hasty AH. Fish oil increases cholesterol storage in white adipose tissue with concomitant decreases in inflammation, hepatic steatosis, and atherosclerosis in mice. J Nutr. 2007;137:1776-82.
23. Davidson MH, Stein EA, Bays HE, Maki KC, Doyle RT, Shalwitz RA, Ballantyne CM, Ginsberg HN; COMBination of prescription Omega-3 with Simvastatin (COMBOS) Investigators. Efficacy and tolerability of adding prescription omega-3 fatty acids 4 g/d to simvastatin 40 mg/d in hypertriglyceridemic patients: an 8-week, randomized, double-blind, placebo-controlled study. Clin Ther. 2007;29:1354-67.
24. Milne GL, Yin H, Morrow JD. Human biochemistry of the isoprostane pathway. J Biol Chem. 2008;283:15533-7.
25. Jump DB, Torres-Gonzalez M, Olson LK. Soraphen A, a inhibitor of acetyl CoA carboxylase activity, interferes with fatty acid elongation. Biochem Pharmacol. 2011;81:649-60.
26. Subramanian S, Goodspeed L, Wang S, Kim J, Zeng L, Ioannou GN, Haigh WG, Yeh MM, Kowdley KV, O'Brien KD, et al. Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice. J Lipid Res. 2011;52:1626-35.
27. Wouters K, van Gorp PJ, Bieghs V, Gijbelsm MJ, Duimel H, Lütjohann D, Kerksiekm A, van Kruchtenm R, Maedam N, Staels B, et al. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology. 2008;48:474-86.
28. Van Rooyen DM, Larter CZ, Haigh WG, Yeh MM, Ioannou G, Kuver R, Lee SP, Teoh NC, Farrell GC, Hepatic free cholesterol accumulates in obese, diabetic mice and causes nonalcoholic steatohepatitis. Gastroenterology 2011;141:1393-403.
29. Morrow JD. The isoprostanes-unique products of arachidonate peroxidation: their role as mediators of oxidant stress. Curr Pharm Des. 2006;12:895-902.
30. Hasty AH, Gruen JL, Terry ES, Surmi BK, Atkinson RD, Gao L, Morrow JD. Effect of vitamin E on oxidative stress and atherosclerosis in an obese hyperlipidemic mouse model. J Nutr Biochem. 2007;18:127-33.
31. Ndisang JF, Jadhav A. Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulinresistant diabetes in Goto-Kakizaki rats. Endocrinology. 2009;150:2627-36.
32. Yu J, Chu ES, Wang R, Wang S, Wu CW, Wong VW, Chan HL, Farrell GC, Sung JJ. Heme oxygenase-1 protects against steatohepatitis in both cultured hepatocytes and mice. Gastroenterology. 2010;138:694-704.
33. Nicolai A, LiM, Kim DH, Peterson SJ, Vanella L, Positano V, Gastaldelli A, Rezzani R, Rodella LF, Drummond G, et al. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension. 2009;53:508-15.
34. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev. 2008;60:79-127.
35. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol. 2010;80:1895-903.
36. Inoue M, Tazuma S, Kanno K, Hyogo H, Igarashi K, Chayama K. Bach1 gene ablation reduces steatohepatitis in mouse MCD diet model. J Clin Biochem Nutr. 2011;48:161-6.
37. Hur W, Gray NS. Small molecule modulators of antioxidant response pathway. Curr Opin Chem Biol. 2011;15:162-73.
38. Botolin D, Wang Y, Christian B, Jump DB. Docosahexaneoic acid (22:6, n-3) regulates rat hepatocyte SREBP-1 nuclear abundance by Erk- and 26S proteasome-dependent pathways. J Lipid Res. 2006;47:181-92.
39. Wang Y, Botolin D, Xu J, Christian B, Mitchell E, Jayaprakasam B, Nair MG, Peters JM, Busik JV, Olson LK, et al. Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J Lipid Res. 2006;47:2028-41.
40. Qin Y, Dalen KT, Gustafsson JA, Nebb HI. Regulation of hepatic fatty acid elongase 5 by LXRa-SREBP-1c. Biochim Biophys Acta. 2009;1791:140-7.
41. Matsuzaka T, Shimano H, Yahagi N, Amemiya-Kudo M, Yoshikawa T, Hasty AH, Tamura Y, Osuga J, Okazaki H, Lizuka Y, et al. Dual regulation of mouse Delta(5)- and Delta(6)-desaturase gene expression by SREBP-1 and PPARa. J Lipid Res. 2002;43:107-14.
42. Parini P, Davis M, Lada AT, Erickson SK, Wright TL, Gustafsson U, Sahlin S, Einarsson C, Eriksson M, Angelin B, et al. ACAT2 is localized to hepatocytes and is the major cholesterol-esterifying enzyme in human liver. Circulation. 2004;110:2017-23.
43. Lee RG, Willingham MC, Davis MA, Skinner KA, Rudel LL. Differential expression of ACAT1 and ACAT2 among cells within liver, intestine, kidney, and adrenal of nonhuman primates. J Lipid Res. 2000;41:1991-2001.
44. Hotamisligil GS, Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol. 2008;8:923-34.
45. Ben-Neriah Y, Karin M. Inflammation meets cancer, with NFkB as the matchmaker. Nat Immunol. 2011;12:715-23.
46. Zhou X, Jamil A, Nash A, Chan J, Trim N, Iredale JP, Benyon RC. Impaired proteolysis of collagen I inhibits proliferation of hepatic stellate cells: implications for regulation of liver fibrosis. J Biol Chem. 2006;281:39757-65.
47. Byrne CD. Fatty liver: role of inflammation and fatty acid nutrition. Prostaglandins Leukot Essent Fatty Acids. 2010;82:265-71.
48. De Bleser PJ, Kiki T, Rogiers V, Geerts A. Transforming growth factor-b gene expression in normal and fibrotic rat liver. J Hepatol. 1997;26:886-93.
49. Garcia-Trevijano ER, Iraburu JJ, Fontana L, Dominguez-Rosales JA, Auster A, Cavarrubias-Pinedo A, Rojkind M. Transforming growth factor b1 induces expression of a1(1)procollagen mRNA by a hydrogen peroxide-c/EBP-b dependent mechanism in rat hepatic stellate cells. Hepatology. 1999;29:960-70.
50. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, Neuschwander-Tetri BA, Lavine JE, Tonascia J, Unalp A, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010;362:1675-85.
51. Lavine JE, Schwimmer JB, Van Natta ML, Lavine JE, Schwimmer JB, Van Natta ML, Molleston JP, Murray KF, Rosenthal P, Abrams SH, et al. Effect of vitamin E or metformin for treatment of nonalcoholic fatty liver disease in children and adolescents: the TONIC randomized controlled trial. JAMA. 2011;305:1659-68.
52. Song WL, Paschos G, Fries S, Reilly MP, Yu Y, Rokach J, Chang CT, Patel P, Lawson JA, Fitzgerald GA. Novel eicosapentaenoic acid-derived F3-isoprostanes as biomarkers of lipid peroxidation. J Biol Chem. 2009;284:23636-43.
53. Milne GL, Yin H, Hardy KD, Davies SS, Roberts LJ II. Isoprostane generation and function. Chem Rev. 2011;111:5973-96.
54. Calder PC. (n-3) polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr. 2006;83:1505S-19S.
55. Pachikian BD, Essaghir A, Demoulin JB, Neyrinck AM, Catry E, De Backer FC, Dejeans N, Dewulf EM, Sohet FM, Portois L, et al. Hepatic (n-3) polyunsaturated fatty acid depletion promotes steatosis and insulin resistance in mice: genomic analysis of cellular targets. PLoS ONE. 2011;6:e23365.
56. Postic C, Girard J. The role of the lipogenic pathway in the development of hepatic steatosis. Diabetes Metab. 2008;34:643-8.
57. Postic C, Dentin R, Denechaud PD, Girard J. ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr. 2007;27:179-92.
58. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest. 2004;114:147-52.
59. Denechaud PD, Dentin R, Girard J, Postic C. Role of ChREBP in hepatic steatosis and insulin resistance. FEBS Lett. 2008;582:68-73.
60. Donnelly KL, Margosian MR, Sheth SS, Lusis AJ, Parks EJ. Increased lipogenesis and fatty acid reesterification contribute to hepatic triacylglycerol stores in hyperlipidemic Txnip2/2 mice. J Nutr. 2004;134:1475-80.
61. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest. 2005;115:1343-51.
62. Van Rooyen DM, Farrell GC. SREBP-2: a link between insulin resistance, hepatic cholesterol, and inflammation in NASH. J Gastroenterol Hepatol. 2011;26:789-92.
63. Thompson WL, Van Eldik LJ. Inflammatory cytokines stimulate the chemokines CCL2/MCP-1 and CCL7/MCP-3 through NFkB and MAPK dependent pathways in rat astrocytes. Brain Res. 2009;1287:47-57.
64. Olefsky JM, Glass CK. Macrophages, inflammation and insulin resistance. Annu Rev Physiol. 2010;72:219-46.