Protective effect of Lactobacillus salivarius Li01 on thioacetamide‐induced acute liver injury and hyperammonaemia

The gut microbiota plays pivotal roles in liver disease onset and progression. The protective effects of Lactobacillus salivarius Li01 on liver diseases have been reported. In this study, we aimed to detect the protective effect of L. salivarius Li01 on thioacetamide (TAA)‐induced acute liver injury and hyperammonaemia. C57BL/6 mice were separated into three groups and given a gavage of L. salivarius Li01 or phosphate‐buffered saline for 7 days. Acute liver injury and hyperammonaemia were induced with an intraperitoneal TAA injection. L. salivarius Li01 decreased mortality and serum transaminase levels and improved histological liver damage caused by TAA. Serum inflammatory cytokine and chemokine and lipopolysaccharide‐binding protein (LBP) concentrations, nuclear factor κB (NFκB) pathway activation and macrophage and neutrophil infiltration into the liver were significantly alleviated by L. salivarius Li01. L. salivarius Li01 also reinforced gut barrier and reshaped the perturbed gut microbiota by upregulating Bacteroidetes and Akkermansia richness and downregulating Proteobacteria, Ruminococcaceae_UCG_014 and Helicobacter richness. Plasma and faecal ammonia levels declined noticeably in the Li01 group, accompanied by improvements in cognitive function, neuro‐inflammation and relative brain‐derived neurotrophic factor (BDNF) gene expression. Our results indicated that L. salivarius Li01 could be considered a potential probiotic in acute liver injury and hepatic encephalopathy (HE).

[1]  William M. Lee,et al.  Acute liver failure – Authors' reply , 2020, The Lancet.

[2]  X. Liao,et al.  Bacillus coagulans R11 maintained intestinal villus health and decreased intestinal injury in lead-exposed mice by regulating the intestinal microbiota and influenced the function of faecal microRNAs. , 2019, Environmental pollution.

[3]  Yu Wang,et al.  Lactobacillus rhamnosus Granules Dose-Dependently Balance Intestinal Microbiome Disorders and Ameliorate Chronic Alcohol-Induced Liver Injury. , 2019, Journal of medicinal food.

[4]  S. Saab,et al.  Hepatic Encephalopathy Challenges, Burden, and Diagnostic and Therapeutic Approach. , 2019, Clinics in liver disease.

[5]  T. Ninomiya,et al.  Serum Lipopolysaccharide‐Binding Protein Levels and the Incidence of Cardiovascular Disease in a General Japanese Population: The Hisayama Study , 2019, Journal of the American Heart Association.

[6]  Lanjuan Li,et al.  Administration of Akkermansia muciniphila Ameliorates Dextran Sulfate Sodium-Induced Ulcerative Colitis in Mice , 2019, Front. Microbiol..

[7]  Hailong Wu,et al.  CCL5 deficiency promotes liver repair by improving inflammation resolution and liver regeneration through M2 macrophage polarization , 2019, Cellular & Molecular Immunology.

[8]  A. Bäumler,et al.  Microbiota-Nourishing Immunity: A Guide to Understanding Our Microbial Self. , 2019, Immunity.

[9]  Wei Zhang,et al.  Fecal Microbiota and Its Correlation With Fatty Acids and Free Amino Acids Metabolism in Piglets After a Lactobacillus Strain Oral Administration , 2019, Front. Microbiol..

[10]  Seong-Tshool Hong,et al.  Elucidation of the anti-hyperammonemic mechanism of Lactobacillus amylovorus JBD401 by comparative genomic analysis , 2018, BMC Genomics.

[11]  R. Jalan,et al.  Targeting the gut-liver axis in liver disease. , 2017, Journal of hepatology.

[12]  M. Hattori,et al.  Commensal Lactobacillus Controls Immune Tolerance during Acute Liver Injury in Mice. , 2017, Cell reports.

[13]  Lanjuan Li,et al.  Protective Effect of Akkermansia muciniphila against Immune-Mediated Liver Injury in a Mouse Model , 2017, Front. Microbiol..

[14]  Lanjuan Li,et al.  Administration of Lactobacillus salivarius LI01 or Pediococcus pentosaceus LI05 prevents CCl4-induced liver cirrhosis by protecting the intestinal barrier in rats , 2017, Scientific Reports.

[15]  J. Tenhunen,et al.  HMGB1 and Extracellular Histones Significantly Contribute to Systemic Inflammation and Multiple Organ Failure in Acute Liver Failure , 2017, Mediators of inflammation.

[16]  H. Tilg,et al.  Recovery of ethanol-induced Akkermansia muciniphila depletion ameliorates alcoholic liver disease , 2017, Gut.

[17]  Pengfei Wu,et al.  Cationic Polystyrene Resolves Nonalcoholic Steatohepatitis, Obesity, and Metabolic Disorders by Promoting Eubiosis of Gut Microbiota and Decreasing Endotoxemia , 2017, Diabetes.

[18]  Soo Jin Kim,et al.  Reconstruction of LPS Transfer Cascade Reveals Structural Determinants within LBP, CD14, and TLR4‐MD2 for Efficient LPS Recognition and Transfer , 2017, Immunity.

[19]  Lanjuan Li,et al.  Integrated transcriptomic and proteomic analysis of the bile stress response in probiotic Lactobacillus salivarius LI01. , 2017, Journal of proteomics.

[20]  Y. Fathollahi,et al.  Effect of low frequency stimulation on impaired spontaneous alternation behavior of kindled rats in Y-maze test , 2016, Epilepsy Research.

[21]  M. Morgan,et al.  Nonabsorbable disaccharides for hepatic encephalopathy: A systematic review and meta‐analysis , 2016, Hepatology.

[22]  K. Cadwell,et al.  Intrinsic Defense Mechanisms of the Intestinal Epithelium. , 2016, Cell host & microbe.

[23]  J. Bajaj,et al.  Covert and Overt Hepatic Encephalopathy: Diagnosis and Management. , 2015, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[24]  Kyle Bittinger,et al.  Engineering the gut microbiota to treat hyperammonemia. , 2015, The Journal of clinical investigation.

[25]  William M. Lee,et al.  Acute liver failure: A curable disease by 2024? , 2015, Journal of hepatology.

[26]  A. Levine,et al.  Progressive Proximal-to-Distal Reduction in Expression of the Tight Junction Complex in Colonic Epithelium of Virally-Suppressed HIV+ Individuals , 2014, PLoS pathogens.

[27]  Andmorgan R. Fisher,et al.  Altered profile of human gut microbiome is associated with cirrhosis and its complications. , 2014, Journal of hepatology.

[28]  L. Lv,et al.  Administration of Lactobacillus salivarius LI01 or Pediococcus pentosaceus LI05 improves acute liver injury induced by d-galactosamine in rats , 2014, Applied Microbiology and Biotechnology.

[29]  G. Ramadori,et al.  Induction of chemokines and cytokines before neutrophils and macrophage recruitment in different regions of rat liver after TAA administration , 2014, Laboratory Investigation.

[30]  F. Schliess,et al.  Osmotic and oxidative/nitrosative stress in ammonia toxicity and hepatic encephalopathy. , 2013, Archives of biochemistry and biophysics.

[31]  A. Abu-Hanna,et al.  Systematic review: acute liver failure – one disease, more than 40 definitions , 2012, Alimentary pharmacology & therapeutics.

[32]  E. Selçuk,et al.  Effects of Rifaximin on Bacterial Translocation in Thioacetamide-Induced Liver Injury in Rats , 2012, Inflammation.

[33]  J. O'grady.  Liver transplantation for acute liver failure. , 2012, Best practice & research. Clinical gastroenterology.

[34]  Rodney D. Newberry,et al.  Goblet cells deliver luminal antigen to CD103+ DCs in the small intestine , 2012, Nature.

[35]  A. Leite-Moreira,et al.  The role of lipopolysaccharide/toll-like receptor 4 signaling in chronic liver diseases , 2010, Hepatology international.

[36]  M. Çakır,et al.  Liver transplantation for acute liver failure due to toxic agent ingestion in children , 2009, Pediatric transplantation.

[37]  J. Devière,et al.  Control of acute, chronic, and constitutive hyperammonemia by wild‐type and genetically engineered Lactobacillus plantarum in rodents , 2008, Hepatology.

[38]  C. Dejong,et al.  The gut does not contribute to systemic ammonia release in humans without portosystemic shunting. , 2008, American journal of physiology. Gastrointestinal and liver physiology.

[39]  W. Burchert,et al.  Correlations between magnetic resonance spectroscopy alterations and cerebral ammonia and glucose metabolism in cirrhotic patients with and without hepatic encephalopathy , 2007, Gut.

[40]  H. Jaeschke,et al.  Role of neutrophils in acute inflammatory liver injury , 2006, Liver international : official journal of the International Association for the Study of the Liver.

[41]  R. Medzhitov,et al.  Phosphoinositide-Mediated Adaptor Recruitment Controls Toll-like Receptor Signaling , 2006, Cell.

[42]  N. Weizman,et al.  Curcumin ameliorates acute thioacetamide‐induced hepatotoxicity , 2006, Journal of gastroenterology and hepatology.

[43]  C. Potten,et al.  Accelerated Intestinal Epithelial Cell Turnover: A New Mechanism of Parasite Expulsion , 2005, Science.

[44]  A. Gressner,et al.  Induction of neutrophil-attracting chemokines in transforming rat hepatic stellate cells. , 1997, Gastroenterology.

[45]  M. Norenberg.  Astrocytic-Ammonia Interactions in Hepatic Encephalopathy , 1996, Seminars in liver disease.

[46]  H. Thoenen,et al.  Molecular cloning and expression of brain-derived neurotrophic factor , 1989, Nature.

[47]  H. Thoenen,et al.  Purification of a new neurotrophic factor from mammalian brain. , 1982, The EMBO journal.

[48]  Neil Kaplowitz,et al.  Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis , 1981, Hepatology.

[49]  T. Nabeshima,et al.  Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation , 2003, Molecular Psychiatry.

[50]  K. Böker,et al.  [Acute liver failure]. , 2001, Der Internist.

[51]  A. Blei,et al.  Hepatic encephalopathy , 2001, American Journal of Gastroenterology.