Bifidobacterium adolescentis protects from the development of nonalcoholic steatohepatitis in a mouse model

Journal of Nutritional Biochemistry

Volumn 25, Issue 2, 2014, Pages 118-125

  Reichold, Astrid ^a   Brenner, Sibylle A ^a   Spruss, Astrid ^a   Förster Fromme, Karin ^a   Bergheim, Ina ^b   Bischoff, Stephan C ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Nonalcoholic steatohepatitis; Obesity; Probiotics; Toll like receptor 4

Indexed keywords

ENDOTOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; OCCLUDIN; PROBIOTIC AGENT; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIFIDOBACTERIUM ADOLESCENTIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIPID PEROXIDATION; LIVER HISTOLOGY; LIVER INJURY; LIVER PROTECTION; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN;

NONALCOHOLIC STEATOHEPATITIS; OBESITY; PROBIOTICS; TOLL-LIKE RECEPTOR 4;

ANIMALS; BASE SEQUENCE; BIFIDOBACTERIUM; DISEASE MODELS, ANIMAL; DNA PRIMERS; FATTY LIVER; LIPID PEROXIDATION; MICE; MICE, INBRED C57BL;

EID: 84892502150     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2013.09.011     Document Type: Article

References (46)

1. Bedogni G., Miglioli L., Masutti F., Tiribelli C., Marchesini G., Bellentani S. Prevalence of and risk factors for nonalcoholic fatty liver disease: the Dionysos nutrition and liver study. Hepatology 2005, 42:44-52.
2. Tilg H., Kaser A. Treatment strategies in nonalcoholic fatty liver disease. Nat Clin Pract Gastroenterol Hepatol 2005, 2:148-155.
3. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002, 346:1221-1231.
4. Yang S.Q., Lin H.Z., Mandal A.K., Huang J., Diehl A.M. Disrupted signaling and inhibited regeneration in obese mice with fatty livers: implications for nonalcoholic fatty liver disease pathophysiology. Hepatology 2001, 34:694-706.
5. Rolo A.P., Teodoro J.S., Palmeira C.M. Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis. Free Radic Biol Med 2012, 52:59-69.
6. Loguercio C., Federico A., Tuccillo C., Terracciano F., D'Auria M.V., De Simone C., et al. Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases. J Clin Gastroenterol 2005, 39:540-543.
7. Min A.K., Kim M.K., Kim H.S., Seo H.Y., Lee K.U., Kim J.G., et al. Alpha-lipoic acid attenuates methionine choline deficient diet-induced steatohepatitis in C57BL/6 mice. Life Sci 2012, 90:200-205.
8. Mantena S.K., Vaughn D.P., Andringa K.K., Eccleston H.B., King A.L., Abrams G.A., et al. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo. Biochem J 2009, 417:183-193.
9. Malaguarnera L., Madeddu R., Palio E., Arena N., Malaguarnera M. Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J Hepatol 2005, 42:585-591.
10. Kathirvel E., Chen P., Morgan K., French S.W., Morgan T.R. Oxidative stress and regulation of anti-oxidant enzymes in cytochrome P4502E1 transgenic mouse model of non-alcoholic fatty liver. J Gastroenterol Hepatol 2010, 25:1136-1143.
11. Benhamed F., Denechaud P.D., Lemoine M., Robichon C., Moldes M., Bertrand-Michel J., et al. The lipogenic transcription factor ChREBP dissociates hepatic steatosis from insulin resistance in mice and humans. J Clin Invest 2012, 122:2176-2194.
12. Sung K.C., Wild S.H., Kwag H.J., Byrne C.D. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care 2012, 35:2359-2364.
13. Spruss A., Bergheim I. Dietary fructose and intestinal barrier: potential risk factor in the pathogenesis of nonalcoholic fatty liver disease. J Nutr Biochem 2009, 20:657-662.
14. Bode C., Kugler V., Bode J.C. Endotoxemia in patients with alcoholic and non-alcoholic cirrhosis and in subjects with no evidence of chronic liver disease following acute alcohol excess. J Hepatol 1987, 4:8-14.
15. Thuy S., Ladurner R., Volynets V., Wagner S., Strahl S., Konigsrainer A., et al. Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J Nutr 2008, 138:1452-1455.
16. Volynets V., Kuper M.A., Strahl S., Maier I.B., Spruss A., Wagnerberger S., et al. Nutrition, intestinal permeability, and blood ethanol levels are altered in patients with nonalcoholic fatty liver disease (NAFLD). Dig Dis Sci 2012, 57:1932-1941.
17. Cani P.D., Neyrinck A.M., Fava F., Knauf C., Burcelin R.G., Tuohy K.M., et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007, 50:2374-2383.
18. Bergheim I., Weber S., Vos M., Kramer S., Volynets V., Kaserouni S., et al. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol 2008, 48:983-992.
19. Esposito E., Iacono A., Bianco G., Autore G., Cuzzocrea S., Vajro P., et al. Probiotics reduce the inflammatory response induced by a high-fat diet in the liver of young rats. J Nutr 2009, 139:905-911.
20. Ma X., Hua J., Li Z. Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells. J Hepatol 2008, 49:821-830.
21. Li Z., Yang S., Lin H., Huang J., Watkins P.A., Moser A.B., et al. Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 2003, 37:343-350.
22. Griffiths E.A., Duffy L.C., Schanbacher F.L., Qiao H., Dryja D., Leavens A., et al. In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice. Dig Dis Sci 2004, 49:579-589.
23. Wang Z., Xiao G., Yao Y., Guo S., Lu K., Sheng Z. The role of bifidobacteria in gut barrier function after thermal injury in rats. J Trauma 2006, 61:650-657.
24. Perdigon G., Alvarez S., Rachid M., Aguero G., Gobbato N. Immune system stimulation by probiotics. J Dairy Sci 1995, 78:1597-1606.
25. Schiffrin E.J., Rochat F., Link-Amster H., Aeschlimann J.M., Donnet-Hughes A. Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. J Dairy Sci 1995, 78:491-497.
26. Link-Amster H., Rochat F., Saudan K.Y., Mignot O., Aeschlimann J.M. Modulation of a specific humoral immune response and changes in intestinal flora mediated through fermented milk intake. FEMS Immunol Med Microbiol 1994, 10:55-63.
27. Frick J.S., Fink K., Kahl F., Niemiec M.J., Quitadamo M., Schenk K., et al. Identification of commensal bacterial strains that modulate Yersinia enterocolitica and dextran sodium sulfate-induced inflammatory responses: implications for the development of probiotics. Infect Immun 2007, 75:3490-3497.
28. Kanuri G., Weber S., Volynets V., Spruss A., Bischoff S.C., Bergheim I. Cinnamon extract protects against acute alcohol-induced liver steatosis in mice. J Nutr 2009, 139:482-487.
29. Kleiner D.E., Brunt E.M., Van Natta M., Behling C., Contos M.J., Cummings O.W., et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005, 41:1313-1321.
30. Spruss A., Kanuri G., Uebel K., Bischoff S.C., Bergheim I. Role of the inducible nitric oxide synthase in the onset of fructose-induced steatosis in mice. Antioxid Redox Signal 2011, 14:2121-2135.
31. Kelly C.J., Colgan S.P., Frank D.N. Of microbes and meals: the health consequences of dietary endotoxemia. Nutr Clin Pract 2012, 27:215-225.
32. Pendyala S, Walker JM, Holt PR. A high-fat diet is associated with endotoxemia that originates from the gut. Gastroenterology. 2012;142:1100,1101.e2.
33. Segawa S., Wakita Y., Hirata H., Watari J. Oral administration of heat-killed lactobacillus brevis SBC8803 ameliorates alcoholic liver disease in ethanol-containing diet-fed C57BL/6N mice. Int J Food Microbiol 2008, 128:371-377.
34. Purohit V., Bode J.C., Bode C., Brenner D.A., Choudhry M.A., Hamilton F., et al. Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol 2008, 42:349-361.
35. Charlton M., Krishnan A., Viker K., Sanderson S., Cazanave S., McConico A., et al. Fast food diet mouse: novel small animal model of NASH with ballooning, progressive fibrosis, and high physiological fidelity to the human condition. Am J Physiol Gastrointest Liver Physiol 2011, 301:G825-G834.
36. Kohli R., Kirby M., Xanthakos S.A., Softic S., Feldstein A.E., Saxena V., et al. High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis. Hepatology 2010, 52:934-944.
37. Spruss A., Kanuri G., Stahl C., Bischoff S.C., Bergheim I. Metformin protects against the development of fructose-induced steatosis in mice: role of the intestinal barrier function. Lab Invest 2012, 92:1020-1032.
38. Samuel V.T. Fructose induced lipogenesis: from sugar to fat to insulin resistance. Trends Endocrinol Metab 2011, 22:60-65.
39. Patel A., Harrison S.A. Hepatitis C virus infection and nonalcoholic steatohepatitis. Gastroenterol Hepatol 2012, 8:305-312.
40. Wu J., Wang X., Cai W., Hong L., Tang Q. Bifidobacterium adolescentis supplementation ameliorates parenteral nutrition-induced liver injury in infant rabbits. Dig Dis Sci 2010, 55:2814-2820.
41. Chen J., Wang R., Li X.F., Wang R.L. Bifidobacterium adolescentis supplementation ameliorates visceral fat accumulation and insulin sensitivity in an experimental model of the metabolic syndrome. Br J Nutr 2011, 107:1429-1434.
42. Lin M.Y., Yen C.L. Antioxidative ability of lactic acid bacteria. J Agric Food Chem 1999, 47:1460-1466.
43. Lin M.Y., Chang F.J. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 2000, 45:1617-1622.
44. Kaizu H., Sasaki M., Nakajima H., Suzuki Y. Effect of antioxidative lactic acid bacteria on rats fed a diet deficient in vitamin E. J Dairy Sci 1993, 76:2493-2499.
45. Koyama T., Kirjavainen P.V., Fisher C., Anukam K., Summers K., Hekmat S., et al. Development and pilot evaluation of a novel probiotic mixture for the management of seasonal allergic rhinitis. Can J Microbiol 2010, 56:730-738.
46. Ramirez-Farias C., Slezak K., Fuller Z., Duncan A., Holtrop G., Louis P. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 2009, 101:541-550.