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Compound Probiotic Ameliorates Acute Alcoholic Liver Disease in Mice by Modulating Gut Microbiota and Maintaining Intestinal Barrier

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Abstract

Alcoholic liver disease (ALD) is a worldwide health threaten lack of effective treatment. Gut dysbiosis and concomitant augmented intestinal permeability are strongly implicated in the pathogenesis and progression of ALD. Research on the protective effect of probiotics on ALD is limited, and more effective intestinal microecological regulators and the related mechanisms still need to be further explored. In the present study, the protective effects and mechanisms of a compound probiotic against acute alcohol-induced liver injury in vivo were explod. It was showed that the compound probiotic ameliorated liver injury in acute ALD mice and stabilized the levels of ALT, AST, and TG in serum. The compound probiotic reversed acute alcohol-induced gut dysbiosis and maintained the intestinal barrier integrity by upregulating the production of mucus and the expression of tight junction (TJ) proteins and thus reduced LPS level in liver. Meanwhile, the compound probiotic reduced inflammation level by inhibiting TLR4/NF-κB signaling pathway and suppressed oxidative stress level in liver. Furthermore, the compound probiotic alleviated liver lipid accumulation by regulating fatty acid metabolism-associated genes and AMPK-PPARα signaling pathway. Noteworthy, fecal microbiota transplantation (FMT) realized comparable protective effect with that of compound probiotic. In conclusion, present study demonstrates the beneficial effects and underlying mechanism of the compound probiotic against acute alcohol-induced liver injury. It provides clues for development of novel strategy for treatment of ALD.

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References

  1. Zhou Y, Yuan G, Zhong F, He S (2022) Roles of the complement system in alcohol-induced liver disease. Clin Mol Hepatol 26(4):677–685. https://doi.org/10.3350/cmh.2020.0094

    Article  Google Scholar 

  2. Soleimani V, Delghandi PS, Moallem SA, Karimi G (2019) Safety and toxicity of silymarin, the major constituent of milk thistle extract: an updated review. Phytother Res 33(6):1627–1638. https://doi.org/10.1002/ptr.6361

    Article  CAS  Google Scholar 

  3. Federico A, Dallio M, Loguercio C (2017) Silymarin/silybin and chronic liver disease: a marriage of many years. Molecules 22(2):191. https://doi.org/10.3390/molecules22020191

    Article  CAS  Google Scholar 

  4. Gillessen A, Schmidt HH (2020) Silymarin as supportive treatment in liver diseases: a narrative review. Adv Ther 37(4):1279–1301. https://doi.org/10.1007/s12325-020-01251-y

    Article  Google Scholar 

  5. Chi X, Pan CQ, Liu S, Cheng D, Cao Z, Xing H (2020) Regulating intestinal microbiota in the prevention and treatment of alcohol-related liver disease. Can J Gastroenterol Hepatol 2020:6629196. https://doi.org/10.1155/2020/6629196

    Article  Google Scholar 

  6. Chang B, Fau - Sang L, Sang L Fau - Wang Y, Wang Y Fau - Tong J, Tong J Fau - Zhang D, Zhang D Fau - Wang B, Wang B, (2013) The protective effect of VSL#3 on intestinal permeability in a rat model of alcoholic intestinal injury. BMC Gastroenterol 13:151. https://doi.org/10.1186/1471-230X-13-151

    Article  CAS  Google Scholar 

  7. Hong M, Han DH, Hong J, Kim DJ, Suk KT (2019) Are probiotics effective in targeting alcoholic liver diseases? Probiotics Antimicrob Proteins 11(2):335–347. https://doi.org/10.1007/s12602-018-9419-6

    Article  CAS  Google Scholar 

  8. Rao R (2009) Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatology 50(2):638–644. https://doi.org/10.1002/hep.23009

    Article  CAS  Google Scholar 

  9. Lawrence T (2009) The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 1(6):a001651. https://doi.org/10.1101/cshperspect.a001651

    Article  CAS  Google Scholar 

  10. O’Shannessy DJ, Somers EB, Wang LC, Wang HW, Hsu R (2015) Expression of folate receptors alpha and beta in normal and cancerous gynecologic tissues: correlation of expression of the beta isoform with macrophage markers. Journal of Ovarian Research 8:29. https://doi.org/10.1186/s13048-015-0156-0

    Article  CAS  Google Scholar 

  11. You M, Arteel GE (2019) Effect of ethanol on lipid metabolism. J Hepatol 70(2):237–248. https://doi.org/10.1016/j.jhep.2018.10.037

    Article  CAS  Google Scholar 

  12. Jeon S, Carr R (2020) Alcohol effects on hepatic lipid metabolism. J Lipid Res 61(4):470–479. https://doi.org/10.1194/jlr.R119000547

    Article  CAS  Google Scholar 

  13. Kang Y, Kang X, Yang H, Liu H, Yang X, Liu Q, Tian H, Xue Y, Ren P, Kuang X, Cai Y, Tong M, Li L, Fan W (2022) Lactobacillus acidophilus ameliorates obesity in mice through modulation of gut microbiota dysbiosis and intestinal permeability. Pharmacol Res 175:106020. https://doi.org/10.1016/j.phrs.2021.106020

    Article  CAS  Google Scholar 

  14. Sharma BC, Singh J (2016) Probiotics in management of hepatic encephalopathy. Metab Brain Dis 31(6):1295–1301. https://doi.org/10.1007/s11011-016-9826-x

    Article  Google Scholar 

  15. Liu Y, Yin F, Huang L, Teng H, Shen T, Qin H (2021) Long-term and continuous administration of Bacillus subtilis during remission effectively maintains the remission of inflammatory bowel disease by protecting intestinal integrity, regulating epithelial proliferation, and reshaping microbial structure and function. Food Funct 12(5):2201–2210. https://doi.org/10.1039/d0fo02786c

    Article  CAS  Google Scholar 

  16. Liang Y, Liang S, Zhang Y, Deng Y, He Y, Chen Y, Liu C, Lin C, Yang Q (2019) Oral administration of compound probiotics ameliorates HFD-induced gut microbe dysbiosis and chronic metabolic inflammation via the G protein-coupled receptor 43 in non-alcoholic fatty liver disease rats. Probiotics Antimicrob Proteins 11(1):175–185. https://doi.org/10.1007/s12602-017-9378-3

    Article  CAS  Google Scholar 

  17. Huang E, Kim S, Park H, Park S, Ji Y, Todorov SD, Lim SD, Holzapfel WH (2021) Modulation of the gut microbiome and obesity biomarkers by Lactobacillus plantarum KC28 in a diet-induced obesity murine model. Probiotics Antimicrob Proteins 13(3):677–697. https://doi.org/10.1007/s12602-020-09720-0

    Article  CAS  Google Scholar 

  18. Nosova T, Jousimies-Somer H, Jokelainen K, Heine R, Salaspuro M (2000) Acetaldehyde production and metabolism by human indigenous and probiotic Lactobacillus and Bifidobacterium strains. Alcohol Alcohol 35(6):561–568. https://doi.org/10.1093/alcalc/35.6.561

    Article  CAS  Google Scholar 

  19. Jung SJ, Hwang JH, Park EO, Lee SO, Chung YJ, Chung MJ, Lim S, Lim TJ, Ha Y, Park BH, Chae SW (2021) Regulation of alcohol and acetaldehyde metabolism by a mixture of Lactobacillus and Bifidobacterium species in human. Nutrients 13(6):1875. https://doi.org/10.3390/nu13061875

    Article  CAS  Google Scholar 

  20. Gan Y, Chen X, Yi R, Zhao X (2021) Antioxidative and anti-inflammatory effects of Lactobacillus plantarum ZS62 on alcohol-induced subacute hepatic damage. Oxid Med Cell Longev 2021:7337988. https://doi.org/10.1155/2021/7337988

    Article  CAS  Google Scholar 

  21. Li H, Shi J, Zhao L, Guan J, Liu F, Huo G, Li B (2021) Lactobacillus plantarum KLDS1.0344 and Lactobacillus acidophilus KLDS1.0901 mixture prevents chronic alcoholic liver injury in mice by protecting the intestinal barrier and regulating gut microbiota and liver-related pathways. J Agric Food Chem 69(1):183–197. https://doi.org/10.1021/acs.jafc.0c06346

  22. Li X, Liu Y, Guo X, Ma Y, Zhang H, Liang H (2021) Effect of Lactobacillus casei on lipid metabolism and intestinal microflora in patients with alcoholic liver injury. Eur J Clin Nutr 75(8):1227–1236. https://doi.org/10.1038/s41430-020-00852-8

    Article  CAS  Google Scholar 

  23. Yi R, Tan F, Liao W, Wang Q, Mu J, Zhou X, Yang Z, Zhao X (2019) Isolation and identification of Lactobacillus plantarum HFY05 from natural fermented yak yogurt and its effect on alcoholic liver injury in mice. Microorganisms 7(11):530. https://doi.org/10.3390/microorganisms7110530

    Article  CAS  Google Scholar 

  24. Horvath A, Durdevic M, Leber B, di Vora K, Rainer F, Krones E, Douschan P, Spindelboeck W, Durchschein F, Zollner G, Stauber RE, Fickert P, Stiegler P, Stadlbauer V (2020) Changes in the intestinal microbiome during a multispecies probiotic intervention in compensated cirrhosis. Nutrients 12 (6). https://doi.org/10.3390/nu12061874

  25. Mennigen R, Bruewer M (2009) Effect of probiotics on intestinal barrier function. Ann N Y Acad Sci 1165:183–189. https://doi.org/10.1111/j.1749-6632.2009.04059.x

    Article  Google Scholar 

  26. Khailova L, Baird CH, Rush AA, Barnes C, Wischmeyer PE (2017) Lactobacillus rhamnosus GG treatment improves intestinal permeability and modulates inflammatory response and homeostasis of spleen and colon in experimental model of Pseudomonas aeruginosa pneumonia. Clin Nutr 36(6):1549–1557. https://doi.org/10.1016/j.clnu.2016.09.025

    Article  CAS  Google Scholar 

  27. Putaala H, Salusjärvi T, Nordström M, Saarinen M, Ouwehand AC, Bech Hansen E, Rautonen N (2008) Effect of four probiotic strains and Escherichia coli O157:H7 on tight junction integrity and cyclo-oxygenase expression. Res Microbiol 159(9–10):692–698. https://doi.org/10.1016/j.resmic.2008.08.002

    Article  CAS  Google Scholar 

  28. Liu Q, Tian H, Kang Y, Tian Y, Li L, Kang X, Yang H, Wang Y, Tian J, Zhang F, Tong M, Cai H, Fan W (2021) Probiotics alleviate autoimmune hepatitis in mice through modulation of gut microbiota and intestinal permeability. J Nutr Biochem 98:108863. https://doi.org/10.1016/j.jnutbio.2021.108863

    Article  CAS  Google Scholar 

  29. Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890. https://doi.org/10.1093/bioinformatics/bty560

    Article  CAS  Google Scholar 

  30. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  Google Scholar 

  31. Peacock A, Leung J, Larney S, Colledge S, Hickman M, Rehm J, Giovino GA, West R, Hall W, Griffiths P, Ali R, Gowing L, Marsden J, Ferrari AJ, Grebely J, Farrell M, Degenhardt L (2018) Global statistics on alcohol, tobacco and illicit drug use: 2017 status report. Addiction 113(10):1905–1926. https://doi.org/10.1111/add.14234

    Article  Google Scholar 

  32. Seitz HK, Bataller R, Cortez-Pinto H, Gao B, Gual A, Lackner C, Mathurin P, Mueller S, Szabo G, Tsukamoto H (2018) Alcoholic liver disease. Nat Rev Dis Primers 4(1):16. https://doi.org/10.1038/s41572-018-0014-7

    Article  Google Scholar 

  33. Qamar N, Castano D, Patt C, Chu T, Cottrell J, Chang SL (2019) Meta-analysis of alcohol induced gut dysbiosis and the resulting behavioral impact. Behav Brain Res 376:112196. https://doi.org/10.1016/j.bbr.2019.112196

    Article  CAS  Google Scholar 

  34. Hartmann P, Seebauer CT, Schnabl B (2015) Alcoholic liver disease: the gut microbiome and liver cross talk. Alcohol Clin Exp Res 39(5):763–775. https://doi.org/10.1111/acer.12704

    Article  Google Scholar 

  35. Zhang D, Hao X, Xu L, Cui J, Xue L, Tian Z (2017) Intestinal flora imbalance promotes alcohol-induced liver fibrosis by the TGFβ/smad signaling pathway in mice. Oncol Lett 14(4):4511–4516. https://doi.org/10.3892/ol.2017.6762

    Article  CAS  Google Scholar 

  36. Fairfield B, Schnabl B (2021) Gut dysbiosis as a driver in alcohol-induced liver injury. Jhep Reports 3(2):100220. https://doi.org/10.1016/j.jhepr.2020.100220

    Article  Google Scholar 

  37. Wrzosek L, Ciocan D, Hugot C, Spatz M, Dupeux M, Houron C, Lievin-Le Moal V, Puchois V, Ferrere G, Trainel N, Mercier-Nome F, Durand S, Kroemer G, Voican CS, Emond P, Straube M, Sokol H, Perlemuter G, Cassard AM (2021) Microbiota tryptophan metabolism induces aryl hydrocarbon receptor activation and improves alcohol-induced liver injury. Gut 70(7):1299–1308. https://doi.org/10.1136/gutjnl-2020-321565

    Article  CAS  Google Scholar 

  38. Xu L, Huang Q, Tan X, Zhao Q, Wu J, Liao H, Ai W, Liu Y, Lai Z, Fu L (2021) Patchouli alcohol ameliorates acute liver injury via inhibiting oxidative stress and gut-origin LPS leakage in rats. Int Immunopharmacol 98:107897. https://doi.org/10.1016/j.intimp.2021.107897

    Article  CAS  Google Scholar 

  39. Li B, Mao Q, Zhou D, Luo M, Gan R, Li H, Huang S, Saimaiti A, Shang A, Li H (2021) Effects of tea against alcoholic fatty liver disease by modulating gut microbiota in chronic alcohol-exposed mice. Foods 10(6):1232. https://doi.org/10.3390/foods10061232

    Article  CAS  Google Scholar 

  40. Yue R, Wei X, Zhao J, Zhou Z, Zhong W (2020) Essential role of IFN-gamma in regulating gut antimicrobial peptides and microbiota to protect against alcohol-induced bacterial translocation and hepatic inflammation in mice. Front Physiol 11:629141. https://doi.org/10.3389/fphys.2020.629141

    Article  Google Scholar 

  41. Singhal R, Donde H, Ghare S, Stocke K, Zhang J, Vadhanam M, Reddy S, Gobejishvili L, Chilton P, Joshi-Barve S, Feng W, McClain C, Hoffman K, Petrosino J, Vital M, Barve S (2021) Decrease in acetyl-CoA pathway utilizing butyrate-producing bacteria is a key pathogenic feature of alcohol-induced functional gut microbial dysbiosis and development of liver disease in mice. Gut Microbes 13(1):1946367. https://doi.org/10.1080/19490976.2021.1946367

    Article  CAS  Google Scholar 

  42. Zhang T, Li J, Liu CP, Guo M, Gao CL, Zhou LP, Long Y, Xu Y (2021) Butyrate ameliorates alcoholic fatty liver disease via reducing endotoxemia and inhibiting liver gasdermin D-mediated pyroptosis. Ann Transl Med 9 (10):873. https://doi.org/10.21037/atm-21-2158

  43. Soliman AR, Ahmed RM, Abdalla A, Soliman M, Saeed M (2018) Impact of Enterobacteriaceae bacteremia on survival in patients with hepatorenal failure. Saudi J Kidney Dis Transpl 29(6):1311–1319. https://doi.org/10.4103/1319-2442.248293

    Article  Google Scholar 

  44. Cuevas-Sierra A, Riezu-Boj JI, Guruceaga E, Milagro FI, Martínez JA (2020) Sex-specific associations between gut Prevotellaceae and host genetics on adiposity. Microorganisms 8(6):938. https://doi.org/10.3390/microorganisms8060938

    Article  CAS  Google Scholar 

  45. Luo L, Zhang J, Liu M, Qiu S, Yi S, Yu W, Liu T, Huang X, Ning F (2021) Monofloral Triadica Cochinchinensis honey polyphenols improve alcohol-induced liver disease by regulating the gut microbiota of mice. Front Immunol 12:673903. https://doi.org/10.3389/fimmu.2021.673903

    Article  CAS  Google Scholar 

  46. Haber PS, Kortt NC (2021) Alcohol use disorder and the gut. Addiction 116(3):658–667. https://doi.org/10.1111/add.15147

    Article  Google Scholar 

  47. Lamas-Paz A, Moran L, Peng J, Salinas B, Lopez-Alcantara N, Sydor S, Vilchez-Vargas R, Asensio I, Hao F, Zheng K, Martin-Adrados B, Moreno L, Cogolludo A, Gomez Del Moral M, Bechmann L, Martinez-Naves E, Vaquero J, Banares R, Nevzorova YA, Cubero FJ (2020) Intestinal epithelial cell-derived extracellular vesicles modulate hepatic injury via the gut-liver axis during acute alcohol injury. Front Pharmacol 11:603771. https://doi.org/10.3389/fphar.2020.603771

    Article  CAS  Google Scholar 

  48. Fukui H (2016) Increased intestinal permeability and decreased barrier function: does it really influence the risk of inflammation? Inflamm Intest Dis 1(3):135–145. https://doi.org/10.1159/000447252

    Article  Google Scholar 

  49. Sharma L, Riva A (2020) Intestinal barrier function in health and disease-any role of SARS-CoV-2? Microorganisms 8(11):1744. https://doi.org/10.3390/microorganisms8111744

    Article  CAS  Google Scholar 

  50. Nowak AJ, Relja B (2020) The impact of acute or chronic alcohol intake on the NF-kappaB signaling pathway in alcohol-related liver disease. Int J Mol Sci 2121(24):9407. https://doi.org/10.3390/ijms21249407

    Article  CAS  Google Scholar 

  51. Feng G, Yang X, Li Y, Wang X, Tan S, Chen F (2018) LPS enhances platelets aggregation via TLR4, which is related to mitochondria damage caused by intracellular ROS, but not extracellular ROS. Cell Immunol 328:86–92. https://doi.org/10.1016/j.cellimm.2018.04.002

    Article  CAS  Google Scholar 

  52. Fu P, Epshtein Y, Ramchandran R, Mascarenhas JB, Cress AE, Jacobson J, Garcia JGN, Natarajan V (2021) Essential role for paxillin tyrosine phosphorylation in LPS-induced mitochondrial fission, ROS generation and lung endothelial barrier loss. Sci Rep 11(1):17546. https://doi.org/10.1038/s41598-021-97006-y

    Article  CAS  Google Scholar 

  53. Carling D (2017) AMPK signalling in health and disease. Curr Opin Cell Biol 45:31–37. https://doi.org/10.1016/j.ceb.2017.01.005

    Article  CAS  Google Scholar 

  54. Herzig S, Shaw RJ (2018) AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19(2):121–135. https://doi.org/10.1038/nrm.2017.95

    Article  CAS  Google Scholar 

  55. Grygiel-Górniak B (2014) Peroxisome proliferator-activated receptors and their ligands: nutritional and clinical implications–a review. Nutr J 13:17. https://doi.org/10.1186/1475-2891-13-17

    Article  CAS  Google Scholar 

  56. Yue R, Chen GY, Xie G, Hao L, Guo W, Sun X, Jia W, Zhang Q, Zhou Z, Zhong W (2021) Activation of PPARalpha-catalase pathway reverses alcoholic liver injury via upregulating NAD synthesis and accelerating alcohol clearance. Free Radic Biol Med 174:249–263. https://doi.org/10.1016/j.freeradbiomed.2021.08.005

    Article  CAS  Google Scholar 

  57. Chen X, Xu Y, Denning KL, Grigore A, Lu Y (2021) PPARalpha agonist WY-14,643 enhances ethanol metabolism in mice: role of catalase. Free Radic Biol Med 169:283–293. https://doi.org/10.1016/j.freeradbiomed.2021.04.018

    Article  CAS  Google Scholar 

  58. Frisard MI, McMillan RP, Marchand J, Wahlberg KA, Wu Y, Voelker KA, Heilbronn L, Haynie K, Muoio B, Li L, Hulver MW (2010) Toll-like receptor 4 modulates skeletal muscle substrate metabolism. Am J Physiol Endocrinol Metab 298(5):E988–E998. https://doi.org/10.1152/ajpendo.00307.2009

    Article  CAS  Google Scholar 

  59. Frisard MI, Wu Y, McMillan RP, Voelker KA, Wahlberg KA, Anderson AS, Boutagy N, Resendes K, Ravussin E, Hulver MW (2015) Low levels of lipopolysaccharide modulate mitochondrial oxygen consumption in skeletal muscle. Metabolism 64(3):416–427. https://doi.org/10.1016/j.metabol.2014.11.007

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Zhongke Yikang for providing the compound probiotic. We are grateful to Laboratory of Tai Yuan Hospital of Traditional Chinese Medicine for testing the concentration of transaminase.

Funding

This project has received funding from Scientific Research Funding Project for Returned Overseas Students in Shanxi Province (probiotics alleviate the cytokine storm by inhibiting the TLR4-dependent NF-κB signaling pathway, 2020–079) and Shanxi Provincial Natural Fund Project (probiotics to relieve autoimmune hepatitis and its mechanism, 201901D111194).

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Authors and Affiliations

  1. Department of Microbiology and Immunology, Shanxi Medical University, Jinzhong, 030619, China

    Haixia Liu, Xing Kang, Xiaodan Yang, Hao Yang, Xiaoyu Kuang, Peng Ren, Huan Yan, Xiaorong Shen, Yongbo Kang, Lin Li, Mingwei Tong & Weiping Fan

  2. Key Laboratory of Cellular Physiology, Ministry of Education, Shanxi Medical University, Taiyuan, China

    Haixia Liu, Xing Kang, Xiaodan Yang, Hao Yang, Xiaoyu Kuang, Peng Ren, Huan Yan, Xiaorong Shen, Yongbo Kang, Lin Li, Xiaohui Wang, Linzhi Guo, Mingwei Tong & Weiping Fan

  3. Laboratory of Morphology, Shanxi Medical University, Jinzhong, 030619, China

    Xiaohui Wang & Linzhi Guo

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  1. Haixia Liu
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Contributions

Weiping Fan is responsible for funding acquisition, project administration, and supervision; Haixia Liu is responsible for conceptualization, data curation, formal analysis, investigation, and writing-original draft; Xing Kang carries out works of investigation, validation, and visualization; Xiaodan Yang, Hao Yang, Xiaoyu Kuang, Peng Ren, Huan Yan, and Xiaorong Shen carry out the methodology work; Weiping Fan, Yongbo Kang, Lin Li, and Mingwei Tong carry out the writing-review and editing work; Xiaohui Wang and Linzhi Guo is responsible for resources.

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Liu, H., Kang, X., Yang, X. et al. Compound Probiotic Ameliorates Acute Alcoholic Liver Disease in Mice by Modulating Gut Microbiota and Maintaining Intestinal Barrier. Probiotics & Antimicro. Prot. 15, 185–201 (2023). https://doi.org/10.1007/s12602-022-10005-x

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