Lactobacillus rhamnosus GG treatment potentiates intestinal hypoxia-inducible factor, promotes intestinal integrity and ameliorates alcohol-induced liver injury

American Journal of Pathology

Volumn 179, Issue 6, 2011, Pages 2866-2875

  Wang, Yuhua ^a,b,d   Kirpich, Irina ^b,c   Liu, Yanlong ^b,d   Ma, Zhenhua ^b,e   Barve, Shirish ^b,c   McClain, Craig J ^b,c,f   Feng, Wenke ^b,c,d  

^a JILIN AGRICULTURAL UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d WENZHOU MEDICAL UNIVERSITY   (China)

^e XI'AN JIAOTONG UNIVERSITY   (China)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ALANINE AMINOTRANSFERASE; ALCOHOL; CHOLESTEROL; CLAUDIN 1; FATTY ACID; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INTESTINAL TREFOIL FACTOR; LIPOPOLYSACCHARIDE; MESSENGER RNA; OCCLUDIN; PROBIOTIC AGENT; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL; VASCULOTROPIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL LIVER DISEASE; ALCOHOLIC FATTY LIVER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL INFILTRATION; CELL MEMBRANE PERMEABILITY; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; ENDOTOXEMIA; FATTY ACID BLOOD LEVEL; GENE EXPRESSION; GENE SILENCING; ILEUM; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE FUNCTION; LACTOBACILLUS RHAMNOSUS; LIPID LIVER LEVEL; LIVER FUNCTION; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPPLEMENTATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; EPITHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; ILEUM; LACTOBACILLUS RHAMNOSUS; LIVER DISEASES, ALCOHOLIC; MALE; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION;

EID: 81255124178     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.08.039     Document Type: Article

References (55)

1. J.I. Beier, and C.J. McClain Mechanisms and cell signaling in alcoholic liver disease Biol Chem 391 2010 1249 1264
2. T.H. Frazier, A.M. Stocker, N.A. Kershner, L.S. Marsano, and C.J. McClain Treatment of alcoholic liver disease Therap Adv Gastroenterol 4 2011 63 81
3. C.J. McClain, Z. Song, S.S. Barve, D.B. Hill, and I. Deaciuc Recent advances in alcoholic liver disease IV. Dysregulated cytokine metabolism in alcoholic liver disease Am J Physiol Gastrointest Liver Physiol 287 2004 G497 G502
4. I.A. Kirpich, N.V. Solovieva, S.N. Leikhter, N.A. Shidakova, O.V. Lebedeva, P.I. Sidorov, T.A. Bazhukova, A.G. Soloviev, S.S. Barve, C.J. McClain, and M. Cave Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study Alcohol 42 2008 675 682
5. R.K. Rao Acetaldehyde-induced barrier disruption and paracellular permeability in Caco-2 cell monolayer Methods Mol Biol 447 2008 171 183
6. A. Parlesak, C. Schafer, T. Schutz, J.C. Bode, and C. Bode Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease J Hepatol 32 2000 742 747 (Pubitemid 30262733)
7. Y. Adachi, L.E. Moore, B.U. Bradford, W. Gao, and R.G. Thurman Antibiotics prevent liver injury in rats following long-term exposure to ethanol Gastroenterology 108 1995 218 224
8. C.B. Forsyth, A. Farhadi, S.M. Jakate, Y. Tang, M. Shaikh, and A. Keshavarzian Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis Alcohol 43 2009 163 172
9. A.W. Yan, E. Fouts, J. Brandl, P. Starkel, M. Torralba, E. Schott, H. Tsukamoto, E. Nelson, A. Brenner, and B. Schnabl Enteric dysbiosis associated with a mouse model of alcoholic liver disease Hepatology 53 2011 96 105
10. E. Mutlu, A. Keshavarzian, P. Engen, C.B. Forsyth, M. Sikaroodi, and P. Gillevet Intestinal dysbiosis: a possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats Alcohol Clin Exp Res 33 2009 1836 1846
11. A. Hartsock, and W.J. Nelson Adherens and tight junctions: structure, function and connections to the actin cytoskeleton Biochim Biophys Acta 1778 2008 660 669 (Pubitemid 351317795)
12. M.G. Laukoetter, M. Bruewer, and A. Nusrat Regulation of the intestinal epithelial barrier by the apical junctional complex Curr Opin Gastroenterol 22 2006 85 89 (Pubitemid 44090070)
13. C.T. Taylor, and S.P. Colgan Hypoxia and gastrointestinal disease J Mol Med 85 2007 1295 1300 (Pubitemid 50004090)
14. J.R. Turner Intestinal mucosal barrier function in health and disease Nat Rev Immunol 9 2009 799 809
15. G.L. Wang, B.H. Jiang, E.A. Rue, and G.L. Semenza Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension Proc Natl Acad Sci USA 92 1995 5510 5514
16. W.G. Kaelin Jr, and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol Cell 30 2008 393 402 (Pubitemid 351681994)
17. G. Semenza Signal transduction to hypoxia-inducible factor 1 Biochem Pharmacol 64 2002 993 998 (Pubitemid 35232274)
18. G.L. Semenza Hypoxia-inducible factor 1 (HIF-1) pathway Sci STKE 2007 407 2007 cm8
19. G.T. Furuta, J.R. Turner, C.T. Taylor, R.M. Hershberg, K. Comerford, S. Narravula, D.K. Podolsky, and S.P. Colgan Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia J Exp Med 193 2001 1027 1034 (Pubitemid 32436196)
20. J. Karhausen, G.T. Furuta, J.E. Tomaszewski, R.S. Johnson, S.P. Colgan, and V.H. Haase Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis J Clin Invest 114 2004 1098 1106 (Pubitemid 39578699)
21. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408 (Pubitemid 34164012)
22. W. Feng, F. Ye, W. Xue, Z. Zhou, and Y.J. Kang Copper regulation of hypoxia-inducible factor-1 activity Mol Pharmacol 75 2009 174 182
23. W. Xue, Q. Liu, L. Cai, Z. Wang, and W. Feng Stable overexpression of human metallothionein-IIA in a heart-derived cell line confers oxidative protection Toxicol Lett 188 2009 70 76
24. A.A. Nanji, U. Khettry, and S.M. Sadrzadeh Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease) Proc Soc Exp Biol Med 205 1994 243 247 (Pubitemid 24108319)
25. F. Marotta, R. Barreto, C.C. Wu, Y. Naito, F. Gelosa, A. Lorenzetti, M. Yoshioka, and E. Fesce Experimental acute alcohol pancreatitis-related liver damage and endotoxemia: synbiotics but not metronidazole have a protective effect Chin J Dig Dis 6 2005 193 197
26. E. Isolauri, H. Majamaa, T. Arvola, I. Rantala, E. Virtanen, and H. Arvilommi Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in suckling rats Gastroenterology 105 1993 1643 1650 (Pubitemid 24002779)
27. K.L. Madsen, J.S. Doyle, L.D. Jewell, M.M. Tavernini, and R.N. Fedorak Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice Gastroenterology 116 1999 1107 1114 (Pubitemid 29203020)
28. M. Schultz, C. Veltkamp, L.A. Dieleman, W.B. Grenther, P.B. Wyrick, S.L. Tonkonogy, and R.B. Sartor Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice Inflamm Bowel Dis 8 2002 71 80 (Pubitemid 34213503)
29. H. Eutamene, F. Lamine, C. Chabo, V. Theodorou, F. Rochat, G.E. Bergonzelli, I. Corthesy-Theulaz, J. Fioramonti, and L. Bueno Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats J Nutr 137 2007 1901 1907 (Pubitemid 47292737)
30. H. Eutamene, and L. Bueno Role of probiotics in correcting abnormalities of colonic flora induced by stress Gut 56 2007 1495 1497 (Pubitemid 350033182)
31. M. Zareie, K. Johnson-Henry, J. Jury, P.C. Yang, B.Y. Ngan, D.M. McKay, J.D. Soderholm, M.H. Perdue, and P.M. Sherman Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress Gut 55 2006 1553 1560 (Pubitemid 44629200)
32. W. Zhong, Y. Zhao, C.J. McClain, Y.J. Kang, and Z. Zhou Inactivation of hepatocyte nuclear factor-4{alpha} mediates alcohol-induced down-regulation of intestinal tight junction proteins Am J Physiol Gastrointest Liver Physiol 299 2010 G643 G651
33. W. Zhong, C.J. McClain, M. Cave, Y.J. Kang, and Z. Zhou The role of zinc deficiency in alcohol-induced intestinal barrier dysfunction Am J Physiol Gastrointest Liver Physiol 298 2010 G625 G633
34. J.B. Ewaschuk, and L.A. Dieleman Probiotics and prebiotics in chronic inflammatory bowel diseases World J Gastroenterol 12 2006 5941 5950 (Pubitemid 44608471)
35. E. Miyauchi, H. Morita, and S. Tanabe Lactobacillus rhamnosus alleviates intestinal barrier dysfunction in part by increasing expression of zonula occludens-1 and myosin light-chain kinase in vivo J Dairy Sci 92 2009 2400 2408
36. W. Feleszko, J. Jaworska, R.D. Rha, S. Steinhausen, A. Avagyan, A. Jaudszus, B. Ahrens, D.A. Groneberg, U. Wahn, and E. Hamelmann Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma Clin Exp Allergy 37 2007 498 505 (Pubitemid 46537735)
37. X. Ma, J. Hua, and Z. Li Probiotics improve high fat diet-induced hepatic steatosis and insulin resistance by increasing hepatic NKT cells J Hepatol 49 2008 821 830
38. T. Nakajima, T. Ueda, Y. Takeyama, T. Yasuda, M. Shinzeki, H. Sawa, and Y. Kuroda Protective effects of vascular endothelial growth factor on intestinal epithelial apoptosis and bacterial translocation in experimental severe acute pancreatitis Pancreas 34 2007 410 416 (Pubitemid 46725781)
39. S. Kjellev The trefoil factor family-small peptides with multiple functionalities Cell Mol Life Sci 66 2009 1350 1369
40. S.P. Colgan, and C.T. Taylor Hypoxia: an alarm signal during intestinal inflammation Nat Rev Gastroenterol Hepatol 7 2010 281 287
41. K.M. Comerford, T.J. Wallace, J. Karhausen, N.A. Louis, M.C. Montalto, and S.P. Colgan Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene Cancer Res 62 2002 3387 3394 (Pubitemid 34651384)
42. K. Synnestvedt, G.T. Furuta, K.M. Comerford, N. Louis, J. Karhausen, H.K. Eltzschig, K.R. Hansen, L.F. Thompson, and S.P. Colgan Ecto-5′- nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia J Clin Invest 110 2002 993 1002
43. H.K. Eltzschig, J.C. Ibla, G.T. Furuta, M.O. Leonard, K.A. Jacobson, K. Enjyoji, S.C. Robson, and S.P. Colgan Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors J Exp Med 198 2003 783 796 (Pubitemid 37087777)
44. I.V. Deaciuc, Z. Song, and C.J. McClain Lessons from large-scale gene profiling of the liver in alcoholic liver disease Hepatol Res 31 2005 187 192 (Pubitemid 40724073)
45. I.V. Deaciuc, D.E. Doherty, R. Burikhanov, E.Y. Lee, A.J. Stromberg, X. Peng, and W.J. DE Villiers Large-scale gene profiling of the liver in a mouse model of chronic, intragastric ethanol infusion J Hepatol 40 2004 219 227 (Pubitemid 38115825)
46. D. Bagchi, O.R. Carryl, M.X. Tran, R.L. Krohn, D.J. Bagchi, A. Garg, M. Bagchi, S. Mitra, and S.J. Stohs Stress, diet and alcohol-induced oxidative gastrointestinal mucosal injury in rats and protection by bismuth subsalicylate J Appl Toxicol 18 1998 3 13 (Pubitemid 28101512)
47. A. Keshavarzian, S. Choudhary, E.W. Holmes, S. Yong, A. Banan, S. Jakate, and J.Z. Fields Preventing gut leakiness by oats supplementation ameliorates alcohol-induced liver damage in rats J Pharmacol Exp Ther 299 2001 442 448 (Pubitemid 32979654)
48. A. Keshavarzian, A. Farhadi, C.B. Forsyth, J. Rangan, S. Jakate, M. Shaikh, A. Banan, and J.Z. Fields Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats J Hepatol 50 2009 538 547
49. T.Y. Ma, D. Nguyen, V. Bui, H. Nguyen, and N. Hoa Ethanol modulation of intestinal epithelial tight junction barrier Am J Physiol 276 1999 G965 G974
50. F. Yan, H. Cao, T.L. Cover, R. Whitehead, M.K. Washington, and D.B. Polk Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth Gastroenterology 132 2007 562 575 (Pubitemid 46274659)
51. A. Seth, F. Yan, D.B. Polk, and R.K. Rao Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism Am J Physiol Gastrointest Liver Physiol 294 2008 G1060 G1069
52. C.L. Ohland, and W.K. Macnaughton Probiotic bacteria and intestinal epithelial barrier function Am J Physiol Gastrointest Liver Physiol 298 2010 G807 G819
53. E.O. Petrof, K. Kojima, M.J. Ropeleski, M.W. Musch, Y. Tao, S.C. De, and E.B. Chang Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition Gastroenterology 127 2004 1474 1487 (Pubitemid 39457773)
54. J.M. Kim, J.S. Kim, Y.J. Kim, Y.K. Oh, I.Y. Kim, Y.J. Chee, J.S. Han, and H.C. Jung Conjugated linoleic acids produced by Lactobacillus dissociates IKK-gamma and Hsp90 complex in Helicobacter pylori-infected gastric epithelial cells Lab Invest 88 2008 541 552 (Pubitemid 351581451)
55. C.S. Eun, Y.S. Kim, D.S. Han, J.H. Choi, A.R. Lee, and Y.K. Park Lactobacillus casei prevents impaired barrier function in intestinal epithelial cells APMIS 119 2011 49 56