Lactobacillus rhamnosus CCFM1107 treatment ameliorates alcohol-induced liver injury in a mouse model of chronic alcohol feeding

Journal of Microbiology

Volumn 53, Issue 12, 2015, Pages 856-863

  Tian, Fengwei ^a   Chi, Feifei ^a   Wang, Gang ^a   Liu, Xiaoming ^a   Zhang, Qiuxiang ^a   Chen, Yongquan ^a   Zhang, Hao ^a   Chen, Wei ^a,b  

^a JIANGNAN UNIVERSITY   (China)

^b BEIJING TECHNOLOGY AND BUSINESS UNIVERSITY   (China)

Author keywords

alcoholic liver injury; endotoxin; intestinal flora; oxidative stress; probiotics

Indexed keywords

ALANINE AMINOTRANSFERASE; ALCOHOL; CHOLESTEROL; ENDOTOXIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HERBACEOUS AGENT; MALONALDEHYDE; PROBIOTIC AGENT; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL;

ANIMAL; BIOLOGICAL THERAPY; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; DYSBIOSIS; FATTY LIVER, ALCOHOLIC; INTESTINE FLORA; LACTOBACILLUS RHAMNOSUS; LIVER; MALE; MOUSE; OXIDATIVE STRESS; PATHOLOGY; PROCEDURES;

ALANINE TRANSAMINASE; ANIMALS; BIOLOGICAL THERAPY; CHOLESTEROL; DISEASE MODELS, ANIMAL; DRUGS, CHINESE HERBAL; DYSBIOSIS; ENDOTOXINS; ETHANOL; FATTY LIVER, ALCOHOLIC; GASTROINTESTINAL MICROBIOME; GLUTATHIONE; GLUTATHIONE PEROXIDASE; LACTOBACILLUS RHAMNOSUS; LIVER; MALE; MALONDIALDEHYDE; MICE; OXIDATIVE STRESS; PROBIOTICS; SUPEROXIDE DISMUTASE; TRIGLYCERIDES;

EID: 84949204841     PISSN: 12258873     EISSN: 19763794     Source Type: Journal    
DOI: 10.1007/s12275-015-5239-5     Document Type: Article

References (57)

1. Adawi, D., Ahrné, S., and Molin, G. 2001. Effects of different probiotic strains of Lactobacillus and Bifidobacterium on bacterial translocation and liver injury in an acute liver injury model. Int. J. Food Microbiol.70, 213–220.
2. Afec, R.F. 1989. Probiotics in man and animals. J. Appl. Microbiol.66, 365–378.
3. Ahotupa, M., Saxelin, M., and Korpela, R. 1996. Antioxidative properties of Lactobacillus GG. Nutr. Today31, 51S.
4. Ajmo, J.M., Liang, X., Rogers, C.Q., Pennock, B., and You, M. 2008. Resveratrol alleviates alcoholic fatty liver in mice. Am. J. Physiol. Gastrointest. Liver Physiol.295, G833–G842.
5. Albano, E. 2006. Alcohol, oxidative stress and free radical damage. Proc. Nutr. Soc.65, 278–290.
6. Albano, E. 2008. Oxidative mechanisms in the pathogenesis of alcoholic liver disease. Mol. Aspects Med.29, 9–16.
7. Bailey, S.M. and Cunningham, C.C. 2002. Contribution of mitochondria to oxidative stress associated with alcoholic liver disease. Free Rad. Biol. Med.32, 11–16.
8. Bardag-Gorce, F., Yuan, Q.X., Li, J., French, B.A., Fang, C., Ingelman-Sundberg, M., and French, S.W. 2000. The effect of ethanol-induced cytochrome p4502E1 on the inhibition of proteasome activity by alcohol. Biochem. Biophys. Res. Commun.279, 23–29.
9. Bruzzese, E., Raia, V., Gaudiello, G., Polito, G., Buccigrossi, V., Formicola, V., and Guarino, A. 2004. Intestinal inflammation is a frequent feature of cystic fibrosis and is reduced by probiotic administration. Aliment. Pharmacol. Ther.20, 813–819.
10. Cesaratto, L., Vascotto, C., Calligaris, S., and Tell, G. 2004. The importance of redox state in liver damage. Ann. Hepatol.3, 86–92.
11. Dey, A. and Cederbaum, A.I. 2006. Alcohol and oxidative liver injury. Hepatology43, S63–S74.
12. Donohue, T.M. 2002. The ubiquitin-proteasome system and its role in ethanol-induced disorders. Addict. Biol.7, 15–28.
13. El-Assal, O., Hong, F., Kim, W.H., Radaeva, S., and Gao, B. 2004. IL-6-deficient mice are susceptible to ethanol-induced hepatic steatosis: IL-6 protects against ethanol-induced oxidative stress and mitochondrial permeability transition in the liver. Cell Mol. Immunol.1, 205–211.
14. Ewaschuk, J.B. and Dieleman, L.A. 2006. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J. Gastroenterol.12, 5941.
15. Fernandes, C., Shahani, K., and Amer, M. 1987. Therapeutic role of dietary lactobacilli and lactobacillic fermented dairy products. FEMS Microbiol. Lett.46, 343–356.
16. Fernández-Checa, J.C., Colell, A., and García-Ruiz, C. 2002. S-Adenosyl-L-methionine and mitochondrial reduced glutathione depletion in alcoholic liver disease. Alcohol.27, 179–183.
17. Fernandez-Checa, J.C. and Kaplowitz, N. 2005. Hepatic mitochondrial glutathione: transport and role in disease and toxicity. Toxicol. Appl. Pharmacol.204, 263–273.
18. Forsyth, C.B., Farhadi, A., Jakate, S.M., Tang, Y., Shaikh, M., and Keshavarzian, A. 2009. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol.43, 163–172.
19. Fukui, H. 2005. Relation of endotoxin, endotoxin binding proteins and macrophages to severe alcoholic liver injury and multiple organ failure. Alcohol. Clin. Exp. Res.29, 172S–179S.
20. Gao, B. and Bataller, R. 2011. Alcoholic liver disease: pathogenesis and new therapeutic targets. Gastroenterology141, 1572–1585.
21. Han, D., Hanawa, N., Saberi, B., and Kaplowitz, N. 2006. Mechanisms of liver injury. III. Role of glutathione redox status in liver injury. Am. J. Physiol. Gastrointest. Liver Physiol.291, G1–G7.
22. Hines, I.N. and Wheeler, M.D. 2004. Recent advances in alcoholic liver disease III. Role of the innate immune response in alcoholic hepatitis. Am. J. Physiol. Gastrointest. Liver Physiol.287, G310–G314.
23. Iimuro, Y., Bradford, B.U., Yamashina, S., Rusyn, I., Nakagami, M., Enomoto, N., Kono, H., Frey, W., Forman, D., and Brenner, D. 2000. The glutathione precursor L-2-oxothiazolidine-4-carboxylic acid protects against liver injury due to chronic enteral ethanol exposure in the rat. Hepatology31, 391–398.
24. Kasravi, F.B., Adawi, D., Molin, G., Bengmark, S., and Jeppsson, B. 1997. Effect of oral supplementation of lactobacilli on bacterial translocation in acute liver injury induced by D-galactosamine. J. Hepatol.26, 417–424.
25. Kirpich, I.A., Solovieva, N.V., Leikhter, S.N., Shidakova, N.A., Lebedeva, O.V., Sidorov, P.I., Bazhukova, T.A., Soloviev, A.G., Barve, S.S., and McClain, C.J. 2008. Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study. Alcohol.42, 675–682.
26. Korpela, R., Peuhkuri, K., Lahteenmaki, T., Sievi, E., Saxelin, M., and Vapaatalo, H. 1997. Lactobacillus rhamnosus GG shows antioxidative properties in vascular endothelial cell culture. Milchwissenschaft52, 503–505.
27. Lieber, C.S. 1997. Cytochrome P-4502E1: its physiological and pathological role. Physiol. Rev.77, 517–544.
28. Matuskova, Z., Siller, M., Tunkova, A., Anzenbacherova, E., Zacharova, A., Tlaskalova-Hogenova, H., Zidek, Z., and Anzenbacher, P. 2010. Effects of Lactobacillus casei on the expression and the activity of cytochromes P450 and on the CYP mRNA level in the intestine and the liver of male rats. Neuro Endocrinol. Lett.32, 8–14.
29. McClain, C.J., Barve, S., Deaciuc, I., Kugelmas, M., and Hill, D. 1997. Cytokines and alcoholic liver disease. Alcohol Health Res. World21, 317–320.
30. Mutlu, E., Keshavarzian, A., Engen, P., Forsyth, C.B., Sikaroodi, M., and Gillevet, P. 2009. Intestinal dysbiosis: A possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin. Exp. Res.33, 1836–1846.
31. Nanji, A.A. 2002. Role of Kupffer cells in alcoholic hepatitis. Alcohol27, 13–15.
32. Nanji, A.A., Khettry, U., and Sadrzadeh, S.H. 1994. Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease). Proc. Soc. Exp. Biol. Med.205, 243–247.
33. Nanji, A.A., Yang, E.K., Fogt, F., Sadrzadeh, S., and Dannenberg, A.J. 1996. Medium chain triglycerides and vitamin E reduce the severity of established experimental alcoholic liver disease. J. Pharmacol. Exp. Ther.277, 1694–1700.
34. Nielsen, F., Mikkelsen, B.B., Nielsen, J.B., Andersen, H.R., and Grandjean, P. 1997. Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clin. Chem.43, 1209–1214.
35. O’Shea, R.S., Dasarathy, S., and McCullough, A.J. 2010. Alcoholic liver disease. Hepatology51, 307–328.
36. Osman, N., Adawi, D., Ahrne, S., Jeppsson, B., and Molin, G. 2007. Endotoxin-and d-galactosamine-induced liver injury improved by the administration of Lactobacillus, Bifidobacterium and blueberry. Dig. Liver Dis.39, 849–856.
37. Palmer, M. 2004. Doctor Melissa Palmer’s Guide to Hepatitis and Liver Disease. Penguin.com.
38. Pan, M., Cederbaum, A.I., Zhang, Y.L., Ginsberg, H.N., Williams, K.J., and Fisher, E.A. 2004. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J. Clin. Invest.113, 1277–1287.
39. Parlesak, A., Schäfer, C., Schütz, T., Bode, J.C., and Bode, C. 2000. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J. Hepatol.32, 742–747.
40. Petrasek, J., Mandrekar, P., and Szabo, G. 2010. Toll-like receptors in the pathogenesis of alcoholic liver disease. Gastroenterol. Res. Pract.2010, doi: 10.1155/2010/710381.
41. Rao, R., Seth, A., and Sheth, P. 2004. Recent advances in alcoholic liver disease I. Role of intestinal permeability and endotoxemia in alcoholic liver disease. Am. J. Physiol. Gastrointest. Liver Physiol.286, G881–G884.
42. Rishi, P., Bharrhan, S., Singh, G., and Kaur, I.P. 2011. Effect of Lactobacillus plantarum and l-arginine against endotoxin-induced liver injury in a rat model. Life Sci.89, 847–853.
43. Rishi, P., Mavi, S.K., Bharrhan, S., Shukla, G., and Tewari, R. 2009. Protective efficacy of probiotic alone or in conjunction with a prebiotic in Salmonella-induced liver damage. FEMS Microbiol. Ecol.69, 222–230.
44. Schnabl, B. and Brenner, D.A. 2014. Interactions between the intestinal microbiome and liver diseases. Gastroenterology146, 1513–1524.
45. Segawa, S., Wakita, Y., Hirata, H., and Watari, J. 2008. Oral administration of heat-killed Lactobacillus brevis SBC8803 ameliorates alcoholic liver disease in ethanol-containing diet-fed C57BL/6N mice. Int. J. Food Microbiol.128, 371–377.
46. Sharan, S. and Kansal, V.K. 2011. Effect of feeding probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum on enzymes that catalyze carcinogen activation and detoxification in rats. Milchwissenschaft60, 244–247.
47. Song, F., Xie, M.L., Zhu, L.J., Zhang, K.P., Xue, J., and Gu, Z.L. 2006. Experimental study of osthole on treatment of hyperlipidemic and alcoholic fatty liver in animals. World J. Gastroenterol.12, 4359.
48. Sun, F., Xie, M., Zhu, L., Xue, J., and Gu, Z. 2009. Inhibitory effect of osthole on alcohol-induced fatty liver in mice. Dig. Liver Dis.41, 127–133.
49. Szabo, G. and Bala, S. 2010. Alcoholic liver disease and the gutliver axis. World J. Gastroenterol.16, 1321–1329.
50. Tilg, H., Moschen, A.R., and Kaneider, N.C. 2011. Pathways of liver injury in alcoholic liver disease. J. Hepatol.55, 1159–1161.
51. Uesugi, T., Froh, M., Arteel, G.E., Bradford, B.U., and Thurman, R.G. 2001. Toll-like receptor 4 is involved in the mechanism of early alcohol-induced liver injury in mice. Hepatology34, 101–108.
52. Versalovic, J. 2007. Probiotics: intestinal gatekeeping, immunomodulation, and hepatic injury. Hepatology46, 618–621.
53. Wu, D. and Cederbaum, A.I. 2003. Alcohol, oxidative stress, and free radical damage. Alcohol Res. Health27, 277–284.
54. Xing, H.C., Li, L.J., Xu, K.J., Shen, T., Chen, Y.B., Sheng, J.F., Chen, Y., Fu, S.Z., Chen, C.L., and Wang, J.G. 2006. Protective role of supplement with foreign Bifidobacterium and Lactobacillus in experimental hepatic ischemia-reperfusion injury. J. Gastroenterol. Hepatol.21, 647–656.
55. Yan, A.W., Fouts, D.E., Brandl, J., Stärkel, P., Torralba, M., Schott, E., Tsukamoto, H., Nelson, K.E., Brenner, D.A., and Schnabl, B. 2011. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology53, 96–105.
56. Yoseph, B.P., Breed, E., Overgaard, C.E., Ward, C.J., Liang, Z., Wagener, M.E., Lexcen, D.R., Lusczek, E.R., Beilman, G.J., Burd, E.M.,et al. 2013. Chronic alcohol ingestion increases mortality and organ injury in a murine model of septic peritonitis. PLoS One8, e62792.
57. Yuan, L. and Kaplowitz, N. 2009. Glutathione in liver diseases and hepatotoxicity. Mol. Aspects Med.30, 29–41.