Protective effects of Lactobacillus paracasei F19 in a rat model of oxidative and metabolic hepatic injury

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 299, Issue 3, 2010, Pages

  Nardone, Gerardo ^a   Compare, Debora ^a   Liguori, Eleonora ^a   Di Mauro, Valentina ^a   Rocco, Alba ^a   Barone, Michele ^b   Napoli, Anna ^b   Lapi, Dominga ^c   Iovene, Maria Rosaria ^d   Colantuoni, Antonio ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c UNIVERSITY OF PISA   (Italy)

^d SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Ischemia reperfusion; Lactobacillus paracasei F19; Nonalcoholic fatty liver disease; Probiotics

Indexed keywords

AMINOTRANSFERASE; CHOLINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MALONALDEHYDE; METHIONINE; PROBIOTIC AGENT; TUMOR NECROSIS FACTOR ALPHA; ENDOTOXIN;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; BIFIDOBACTERIUM; CONTROLLED STUDY; DIET; DIET SUPPLEMENTATION; DISEASE SEVERITY; ENTEROBACTERIACEAE; ENTEROCOCCUS; FATTY LIVER; HEPATITIS; INTESTINE MUCOSA; LACTOBACILLUS; LACTOBACILLUS PARACASEI; LACTOBACILLUS PARACASEI F19; LIVER INJURY; LIVER ISCHEMIA; LIVER NECROSIS; LIVER PROTECTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SHAM PROCEDURE; ANIMAL; BLOOD; FLUORESCENCE MICROSCOPY; LIVER; LIVER DISEASE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; VASCULARIZATION; WISTAR RAT;

ANIMALS; CHOLINE; DIET; ENDOTOXINS; LACTOBACILLUS; LIVER; LIVER DISEASES; METHIONINE; MICROSCOPY, FLUORESCENCE; OXIDATIVE STRESS; PROBIOTICS; RATS; RATS, WISTAR; REPERFUSION INJURY; TRANSAMINASES;

EID: 77957012999     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00188.2010     Document Type: Article

References (59)

1. Albillos A, A, de la Hera. Multifactorial gut barrier failure in cirrhosis and bacterial translocation: working out the role of probiotics and antioxidants. J Hepatol 37: 523-526, 2002.
2. Bodera P. Influence of prebiotics on the human immune system (GALT). Recent Pat Inflamm Allergy Drug Discov 2: 149-153, 2008.
3. Busuttil RW, K, Tanaka. The utility of marginal donors in liver transplantation. Liver Transpl 9: 651-663, 2003.
4. Camargo, CA Jr, JF, Madden W, Gao RS, Selvan PA, Clavien. Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent. Hepatology 26: 1513-1520, 1997.
5. Carden DL, DN, Granger. Pathophysiology of ischaemia-reperfusion injury. J Pathol 190: 255-266, 2000.
6. Chang CS, GH, Chen HC, Lien HZ, Yeh. Small intestine dysmotility and bacterial overgrowth in cirrhotic patients with spontaneous bacterial peritonitis. Hepatology 28: 1187-1190, 1998.
7. Chiva M, G, Soriano I, Rochat C, Peralta F, Rochat T, Llovet B, Mirelis EJ, Schiffrin C, Guarner J, Balanzó. Effect of Lactobacillus johnsonii La1 and antioxidants on intestinal flora and bacterial translocation in rats with experimental cirrhosis. J Hepatol 37: 456-462, 2002.
8. Collado MC, E, Isolauri S, Salminen Y, Sanz. The impact of probiotic on gut health. Curr Drug Metab 10: 68-78, 2009.
9. Colletti LM, DG, Remick GD, Burtch SL, Kunkel RM, Strieter DA Jr, Campbell DA. Role of tumor necrosis factor-alpha in the pathophysiologic alterations after hepatic ischemia/reperfusion injury in the rat. J Clin Invest 85: 1936-1943, 1990.
10. Crittenden R, A, Laitila P, Forssell J, Mättö M, Saarela T, Mattila- Sandholm P, Myllärinen. Lactobacillus paracasei subsp. paracasei F19: survival, ecology and safety in the human intestinal tract: a survey of feeding studies within the PROBDEMO project. Microbiol Ecol Health Dis Suppl 3: 22-26, 2002.
11. Cutrin JC, D, Cantino F, Biasi E, Chiarpotto M, Salizzoni E, Andorno G, Massano G, Lanfranco M, Rizzetto A, Boveris G, Poli. Reperfusion damage to the bile canaliculi in transplanted human liver. Hepatology 24: 1053-1057, 1996.
12. DiBaise JK, H, Zhang MD, Crowell R, Krajmalnik-Brown GA, Decker BE, Rittmann. Gut microbiota and its possible relationship with obesity. Mayo Clin Proc 83: 460-469, 2008.
13. Drenick EJ, J, Fisler D, Johnson. Hepatic steatosis after intestinal bypass-prevention and reversal by metronidazole, irrespective of protein-calorie malnutrition. Gastroenterology 82: 535-548, 1982.
14. Eizaguirre I, NG, Urkia AB, Asensio I, Zubillaga P, Zubillaga C, Vidales JM, Garcia-Arenzana P, Aldazabal. Probiotic supplementation reduces the risk of bacterial translocation in experimental short bowel syndrome. J Pediatr Surg 37: 699-702, 2002.
15. Ewaschuk J, R, Endersby D, Thiel H, Diaz J, Backer M, Ma T, Churchill K, Madsen. Probiotic bacteria prevent hepatic damage and maintain colonic barrier function in a mouse model of sepsis. Hepatology 46: 841-850, 2007.
16. Farrell GC, Teoh RS, McCuskey NC. Hepatic microcirculation in fatty liver disease. Anat Rec 291: 684-692, 2008.
17. Galler SA, MB, Pitman. Morphological diagnostic procedures. In: Pathology of the Liver (4th ed.), edited by MacSween RMN, Burt AD, Portmann BC, Ishak KG, Scheuer PJ, and Anthony PP. London, UK: Churchill Livingstone, 2002, p. 943-960.
18. González-Flecha B, Cutrin A, Boveris JC. Time course and mechanism of oxidative stress and tissue damage in rat liver subjected to in vivo ischemia-reperfusion. J Clin Invest 91: 456-464, 1993.
19. Haga S, Remington N, Morita K, Terui M, Ozaki SJ. Hepatic ischemia induced immediate oxidative stress after reperfusion and determined the severity of the reperfusion-induced damage. Antioxid Redox Signal 11: 2563-2572, 2009.
20. He S, C, Atkinson F, Qiao K, Cianflone X, Chen S, Tomlinson. A complement-dependent balance between hepatic ischemia/reperfusion injury and liver regeneration in mice. J Clin Invest 19: 2304-2316, 2009.
21. Heilig HG, Zoetendal EE, Vaughan P, Marteau AD, Akkermans WM, de Vos EG. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68: 114-123, 2002.
22. Hong F, Radaeva HN, Pan Z, Tian R, Veech B, Gao S. Interleukin 6 alleviates hepatic steatosis and ischemia/reperfusion injury in mice with fatty liver disease. Hepatology 40: 933-941, 2004.
23. Jaeschke H, Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol 61: 647-653, 1997.
24. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284: G15-G26, 2003. (Pubitemid 36076246)
25. Jijon H, Backer H, Diaz H, Yeung D, Thiel C, McKaigney C, De Simone K, Madsen J. DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology 126: 1358-1373, 2004.
26. Lee SH, Culberson K, Korneszczuk MG, Clemens C. Differential mechanisms of hepatic vascular dysregulation with mild vs. moderate ischemia-reperfusion. Am J Physiol Gastrointest Liver Physiol 294: G1219-G1226, 2008.
27. Li Z, Yang H, Lin J, Huang PA, Watkins AB, Moser C, Desimone XY, Song AM, Diehl S. Probiotics and antibodies to TNF inhibit inflammatory activity and improve non-alcoholic fatty liver disease. Hepatology 37: 343-350, 2003.
28. Loguercio C, De Simone A, Federico F, Terracciano C, Tuccillo M, Di Chicco M, Cartenμ T. Gut-liver axis: a new point of attack to treat chronic liver damage? Am J Gastroenterol 97: 2144-2146, 2002.
29. Loguercio C, Federico C, Tuccillo F, Terracciano MV, D'Auria C, De Simone C, Del Vecchio Blanco A. Beneficial effects of a probiotic VSL#3 on parameters of liver dysfunction in chronic liver diseases. J Clin Gastroenterol 39: 540-543, 2005.
30. Medina J, Fernández-Salazar L, García-Buey R, Moreno-Otero LI. Pathogenesis and treatment of nonalcoholic steatohepatitis. Diabetes Care 27: 2057-2066, 2004.
31. Mehvar R. Role of TNF-alpha in liver ischaemia-reperfusion injury: new evidence or experimental artefact? Eur J Clin Invest 39: 527-528, 2009.
32. Miele L, Valenza G, La Torre M, Montalto G, Cammarota R, Ricci R, Mascianà A, Forgione ML, Gabrieli G, Perotti FM, Vecchio G, Rapaccini G, Gasbarrini CP, Day A, Grieco V. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 49: 1877-1887, 2009.
33. Minocha A. Probiotics for preventive health. Nutr Clin Pract 24: 227-241, 2009.
34. Mosher B, Dean J, Harkema D, Remick J, Palma E, Crockett R. Inhibition of Kupffer cells reduced CXC chemokine production and liver injury. J Surg Res 99: 201-10, 2001.
35. Nardone G, Rocco A. Probiotics: a potential target for the prevention and treatment of steatohepatitis. J Clin Gastroenterol 38, Suppl 6: S121-S122, 2004.
36. Pappo I, Bercovier E, Berry R, Gallilly E, Feigin HR, Freund H. Antitumor necrosis factor antibodies reduce hepatic steatosis during parenteral nutrition and bowel rest in the rat. J Parenter Enteral Nutr 19: 80-82, 1995.
37. Pappo I, Bercovier EM, Berry Y, Haviv R, Gallily HR, Freund H. Polymyxin B reduces cecal flora, TNF production and hepatic steatosis during total parenteral nutrition in the rat. J Surg Res 51: 106-112, 1991.
38. Petrof EO, Kojima MJ, Ropeleski MW, Musch Y, Tao C, De Simone EB, Chang K. Probiotics inhibit nuclear factor-kabbaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 127: 1474-1487, 2004.
39. Pevni D, Frolkis D, Schwartz I, Schwartz T, Chernichovski A, Kramer Y, Ben-Gal G, Uretzky I, Shapira A, Weinbroum I. New evidence for the role of TNF-alpha in liver ischaemia/reperfusion injury. Eur J Clin Invest 38: 649-655, 2008.
40. Pineiro M, Asp G, Reid S, Macfarlane L, Morelli O, Brunser K, Tuohy NG. FAO Technical meeting on prebiotics. J Clin Gastroenterol 42, Suppl 3: S156-S159, 2008.
41. Rahman SM, Schroeder-Gloeckler RC, Janssen H, Jiang I, Qadri KN, Maclean JE, Friedman JM. CCAAT/enhancing binding protein beta deletion in mice attenuates inflammation, endoplasmic reticulum stress, and lipid accumulation in diet-induced nonalcoholic steatohepatitis. Hepatology 45: 1108-1117, 2007.
42. Remick DG, Colletti WA, Scales KR, McCurry, DA Jr, Campbell LM. Cytokines and extrahepatic sequelae of ischemia-reperfusion injury to the liver. Ann NY Acad Sci 723: 271-283, 1994.
43. Sabaté JM, Jouët F, Harnois C, Mechler S, Msika M, Grossin B, Coffin P. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes Surg 18: 371-377, 2008.
44. Schrezenmeir J, de Vrese M. Probiotics, prebiotics, and synbiotics-approaching a definition. Am J Clin Nutr 73, Suppl 2: 361S-364S, 2001.
45. Selzner N, Rudiger R, Graf PA, Clavien H. Protective strategies against ischemic injury of the liver. Gastroenterology 125: 917-936, 2003.
46. Siebler J, Galle MM, Weber PR. The gut-liver axis: endotoxemia, inflammation, insulin resistance and NASH. J Hepatol 48: 1030-1034, 2008.
47. Su GL. Lipopolysaccharide in liver injury: molecular mechanisms of Kupffer cell activation. Am J Physiol Gastrointest Liver Physiol 283: G256-G265, 2002.
48. Sullivan A, Johansson B, Svenungsson CE, Nord A. Effect of Lactobacillus F19 on the emergence of antibiotic-resistant microorganisms in the intestinal microflora. J Antimicrob Chemother 54: 791-797, 2004.
49. Sumimoto K, Matsura JI, Oku Y, Fukuda K, Yamada K, Dohi T. Protective effect of UW solution on postischemic injury in rat liver: suppression of reduction in hepatic antioxidants during reperfusion. Transplantation 62: 1391-1398, 1996.
50. Tacke F, Luedde C, Trautwein T. Inflammatory pathways in liver homeostasis and liver injury. Clin Rev Allerg Immunol 36: 4-12, 2009.
51. Tanaka Y, Chen JM, Maher CD, Klaassen C. Ischemia-reperfusion of rat livers decreases liver and increases kidney multidrug resistance associated protein 2 (Mrp2). Toxicol Sci 101: 171-178, 2008.
52. Teoh NC, Farrell GC. Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol 18: 891-902, 2003.
53. Tilg H, Trehu MB, Atkins CA, Dinarello JW, Mier E. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83: 113-118, 1994.
54. Tuohy KM, Probert CW, Smejkal GR, Gibson HM. Using probiotics and prebiotics to improve gut health. Drug Discov Today 8: 692-700, 2003.
55. Velayudham A, Dolganiuc M, Ellis J, Petrasek K, Kodys P, Mandrekar G, Szabo A. VSL#3 probiotic treatment attenuates fibrosis without changes in steatohepatitis in a diet-induced nonalcoholic steatohepatitis model in mice. Hepatology 49: 989-997, 2009.
56. Wang L, S, Srinivasan AL, Theiss D, Merlin Sitaraman SV. Interleukin- 6 induces keratin expression in intestinal epithelial cells: potential role of keratin-8 in interleukin-6-induced barrier function alterations. J Biol Chem 282: 8219-8227, 2007.
57. Wanner GA, Ertel P, Müller Y, Höfer R, Leiderer MD, Menger K, Messmer W. Liver ischemia and reperfusion induces a systemic inflammatory response through Kupffer cell activation. Shock 5: 34-40, 1996.
58. Xing HC, Li Xu KJ, T Shen YB, Chen JF, Sheng Y, Chen SZ, Fu CL, Chen JG, Wang D, Yan FW, Dai SS, Zheng LJ. Protective role of supplement with foreign Bifidobacterium and Lactobacillus in experimental hepatic ischemia-reperfusion injury. J Gastroenterol Hepatol 21: 647-656, 2006.
59. Zhao HF, Zhang GW, Zhou JH, Lin ZL, Cui XH, Li J. Biliary tract injury caused by different relative warm ischemia time in liver transplantation in rats. Hepatobiliary Pancreat Dis Int 8: 247-254, 2009.