DOI QR코드

DOI QR Code

Effects of Korean Red Ginseng (Panax ginseng), urushiol (Rhus vernicifera Stokes), and probiotics (Lactobacillus rhamnosus R0011 and Lactobacillus acidophilus R0052) on the gut-liver axis of alcoholic liver disease

  • Bang, Chang Seok (Department of Internal Medicine, Hallym University College of Medicine) ;
  • Hong, So Hyung (Department of Molecular Medicine, Hallym University College of Medicine) ;
  • Suk, Ki Tae (Department of Internal Medicine, Hallym University College of Medicine) ;
  • Kim, Jin Bong (Department of Internal Medicine, Hallym University College of Medicine) ;
  • Han, Sang Hak (Department of Pathology, Hallym University College of Medicine) ;
  • Sung, Hotaik (Department of Biology, Stanford University) ;
  • Kim, Eun Ji (Center for Efficacy Assessment and Development of Functional Foods and Drugs, Hallym University) ;
  • Kim, Myoung Jo (College of Agriculture and Life Science, Kangwon National University) ;
  • Kim, Moon Young (Department of Internal Medicine, Yonsei University Wonju College of Medicine) ;
  • Baik, Soon Koo (Department of Internal Medicine, Yonsei University Wonju College of Medicine) ;
  • Kim, Dong Joon (Department of Internal Medicine, Hallym University College of Medicine)
  • 투고 : 2014.04.04
  • 심사 : 2014.04.17
  • 발행 : 2014.07.15

초록

Background: Roles of immune reaction and toll-like receptor-4 (TLR-4) have widely been established in the pathogenesis of alcoholic liver disease (ALD). Methods: We evaluated the biologic efficacy of Korean Red Ginseng (KRG), urushiol, and probiotics (Lactobacillus rhamnosus R0011 and Lactobacillus acidophilus R0052) in mouse models of ALD. Sixty C57BL/6 mice were equally divided into six feeding groups for 10 weeks: normal diet, alcohol, control, alcohol + KRG, alcohol + urushiol, and alcohol + probiotics. Alcohol was administered via a LiebereDeCarli liquid diet containing 10% alcohol. TLR-4 expression, proinflammatory cytokines, and histology, as well as the results of liver function tests were evaluated and compared. Results: No between-group differences were observed with regard to liver function. TLR-4 levels were significantly lower in the KRG, urushiol, and probiotics groups than in the alcohol group ($0.37{\pm}0.06ng/mL$, $0.39{\pm}0.12ng/mL$, and $0.33{\pm}0.07ng/mL$, respectively, vs. $0.88{\pm}0.31ng/mL$; p < 0.05). Interleukin-$1{\beta}$ levels in liver tissues were decreased among the probiotics and KRG groups. The tumor necrosis factor-${\alpha}$ level of liver tissue was decreased in the KRG group. Conclusion: The pathological findings showed that alcohol-induced steatosis was significantly reduced by KRG and urushiol. As these agents improve immunologic capacity, they may be considered in potential anti-ALD treatments.

키워드

참고문헌

  1. Pares A, Caballeria J, Bruguera M, Torres M, Rodes J. Histological course of alcoholic hepatitis. Influence of abstinence, sex and extent of hepatic damage. J Hepatol 1986;2:33-42. https://doi.org/10.1016/S0168-8278(86)80006-X
  2. Korean Association for the Study of the Liver. KASL clinical practice guidelines: management of alcoholic liver disease. Clin Mol Hepatol 2013;19: 216-54. https://doi.org/10.3350/cmh.2013.19.3.216
  3. Trabut JB, Thepot V, Terris B, Sogni P, Nalpas B, Pol S. Prognosis assessment of alcoholic liver disease: how and why? Presse Med 2014;43:124-34. https://doi.org/10.1016/j.lpm.2013.04.016
  4. Roh YS, Seki E. Toll-like receptors in alcoholic liver disease, non-alcoholic steatohepatitis and carcinogenesis. J Gastroenterol Hepatol 2013;28(Suppl. 1): 38-42.
  5. Petrasek J, Mandrekar P, Szabo G. Toll-like receptors in the pathogenesis of alcoholic liver disease. Gastroenterol Res Pract 2010;2010.
  6. Frazier TH, Stocker AM, Kershner NA, Marsano LS, McClain CJ. Treatment of alcoholic liver disease. Therap Adv Gastroenterol 2011;4:63-81. https://doi.org/10.1177/1756283X10378925
  7. Liu Q, Duan ZP, Ha DK, Bengmark S, Kurtovic J, Riordan SM. Synbiotic modulation of gut flora: effect on minimal hepatic encephalopathy in patients with cirrhosis. Hepatology 2004;39:1441-9. https://doi.org/10.1002/hep.20194
  8. Nanji AA, Khettry U, Sadrzadeh SM. Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease). Proc Soc Exp Biol Med 1994;205:243-7. https://doi.org/10.3181/00379727-205-43703
  9. Kirpich IA, Solovieva NV, Leikhter SN, Shidakova NA, Lebedeva OV, Sidorov PI, Bazhukova TA, Soloviev AG, Barve SS, McClain CJ, et al. Probiotics restore bowel flora and improve liver enzymes in human alcohol-induced liver injury: a pilot study. Alcohol 2008;42:675-82. https://doi.org/10.1016/j.alcohol.2008.08.006
  10. Foster LM, Tompkins TA, Dahl WJ. A comprehensive post-market review of studies on a probiotic product containing Lactobacillus helveticus R0052 and Lactobacillus rhamnosus R0011. Benef Microbes 2011;2:319-34. https://doi.org/10.3920/BM2011.0032
  11. Park HM, Kim SJ, Mun AR, Go HK, Kim GB, Kim SZ, Jang SI, Lee SJ, Kim JS, Kang HS. Korean Red Ginseng and its primary ginsenosides inhibit ethanolinduced oxidative injury by suppression of the MAPK pathway in TIB-73 cells. J Ethnopharmacol 2012;141:1071-6. https://doi.org/10.1016/j.jep.2012.03.038
  12. Lee IA, Hyam SR, Jang SE, Han MJ, Kim DH. Ginsenoside Re ameliorates inflammation by inhibiting the binding of lipopolysaccharide to TLR4 on macrophages. J Agric Food Chem 2012;60:9595-602. https://doi.org/10.1021/jf301372g
  13. Kang S, Min H. Ginseng, the immunity boost': the effects of Panax ginseng on immune system. J Ginseng Res 2012;36:354-68. https://doi.org/10.5142/jgr.2012.36.4.354
  14. Suk KT, Kim HS, Kim MY, Kim JW, Uh Y, Jang IH, Kim SK, Choi EH, Kim MJ, Joo JS, et al. In vitro antibacterial and morphological effects of the urushiol component of the sap of the Korean lacquer tree (Rhus vernicifera Stokes) on Helicobacter pylori. J Korean Med Sci 2010;25:399-404.
  15. Suk KT, Baik SK, Kim HS, Park SM, Paeng KJ, Uh Y, Jang IH, Cho MY, Choi EH, Kim MJ, et al. Antibacterial effects of the urushiol component in the sap of the lacquer tree (Rhus verniciflua Stokes) on Helicobacter pylori. Helicobacter 2011;16:434-43. https://doi.org/10.1111/j.1523-5378.2011.00864.x
  16. Tiniakos DG. Nonalcoholic fatty liver disease/nonalcoholic steatohepatitis: histological diagnostic criteria and scoring systems. Eur J Gastroenterol Hepatol 2010;22:643-50.
  17. Seo YS, Shah VH. The role of guteliver axis in the pathogenesis of liver cirrhosis and portal hypertension. Clin Mol Hepatol 2012;18:337-46. https://doi.org/10.3350/cmh.2012.18.4.337
  18. Hritz I, Mandrekar P, Velayudham A, Catalano D, Dolganiuc A, Kodys K, KurtJones E, Szabo G. The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 2008;48:1224-31. https://doi.org/10.1002/hep.22470
  19. Mandrekar P, Bala S, Catalano D, Kodys K, Szabo G. The opposite effects of acute and chronic alcohol on lipopolysaccharide-induced inflammation are linked to IRAK-M in human monocytes. J Immunol 2009;183:1320-7. https://doi.org/10.4049/jimmunol.0803206
  20. Wang Y, Li Y, Xie J, Zhang Y, Wang J, Sun X, Zhang H. Protective effects of probiotic Lactobacillus casei Zhang against endotoxin- and d-galactosamineinduced liver injury in rats via anti-oxidative and anti-inflammatory capacities. Int Immunopharmacol 2013;15:30-7. https://doi.org/10.1016/j.intimp.2012.10.026
  21. Peng XD, Dai LL, Huang CQ, He CM, Yang B, Chen LJ. Relationship between anti-fibrotic effect of Panax notoginseng saponins and serum cytokines in rat hepatic fibrosis. Biochem Biophys Res Commun 2009;388: 31-4. https://doi.org/10.1016/j.bbrc.2009.07.099
  22. Rhule A, Rase B, Smith JR, Shepherd DM. Toll-like receptor ligand-induced activation of murine DC2.4 cells is attenuated by Panax notoginseng. J Ethnopharmacol 2008;116:179-86. https://doi.org/10.1016/j.jep.2007.11.019
  23. Yayeh T, Jung KH, Jeong HY, Park JH, Song YB, Kwak YS, Kang HS, Cho JY, Oh JW, Kim SK, et al. Korean Red Ginseng saponin fraction downregulates proinflammatory mediators in LPS stimulated RAW264.7 cells and protects mice against endotoxic shock. J Ginseng Res 2012;36:263-9. https://doi.org/10.5142/jgr.2012.36.3.263
  24. Park SM, Choi MS, Sohn NW, Shin JW. Ginsenoside Rg3 attenuates microglia activation following systemic lipopolysaccharide treatment in mice. Biol Pharm Bull 2012;35:1546-52. https://doi.org/10.1248/bpb.b12-00393
  25. Wang B, Feng G, Tang C, Wang L, Cheng H, Zhang Y, Ma J, Shi M, Zhao G. Ginsenoside Rd maintains adult neural stem cell proliferation during leadimpaired neurogenesis. Neurol Sci 2013;34:1181-8. https://doi.org/10.1007/s10072-012-1215-6
  26. Zwolinska-Wcislo M, Brzozowski T, Budak A, Kwiecien S, Sliwowski Z, Drozdowicz D, Trojanowska D, Rudnicka-Sosin L, Mach T, Konturek SJ, et al. Effect of Candida colonization on human ulcerative colitis and the healing of inflammatory changes of the colon in the experimental model of colitis ulcerosa. J Physiol Pharmacol 2009;60:107-18.
  27. Bertola A, Mathews S, Ki SH, Wang H, Gao B. Mouse model of chronic and binge ethanol feeding (the NIAAA model). Nat Protoc 2013;8:627-37. https://doi.org/10.1038/nprot.2013.032

피인용 문헌

  1. Effect of microbial cell preparation on renal profile and liver function among type 2 diabetics: a randomized controlled trial vol.15, pp.None, 2014, https://doi.org/10.1186/s12906-015-0952-5
  2. Probiotics ( Lactobacillus rhamnosus R0011 and acidophilus R0052 ) Reduce the Expression of Toll-Like Receptor 4 in Mice with Alcoholic Liver Disease vol.10, pp.2, 2014, https://doi.org/10.1371/journal.pone.0117451
  3. Protective Effects of Korean Red Ginseng against Alcohol-Induced Fatty Liver in Rats vol.20, pp.6, 2014, https://doi.org/10.3390/molecules200611604
  4. Hepatoprotective effects of dual-coated and uncoated mixture of probiotics in rats vol.29, pp.6, 2014, https://doi.org/10.1080/13102818.2015.1063452
  5. Compound K Production from Red Ginseng Extract by β-Glycosidase from Sulfolobus solfataricus Supplemented with α- L -Arabinofuranosidase from Caldicellulosiruptor saccharo vol.10, pp.12, 2015, https://doi.org/10.1371/journal.pone.0145876
  6. Microbiota-based treatments in alcoholic liver disease vol.22, pp.29, 2016, https://doi.org/10.3748/wjg.v22.i29.6673
  7. Bacterial Diversity and Community Structure in Korean Ginseng Field Soil Are Shifted by Cultivation Time vol.11, pp.5, 2014, https://doi.org/10.1371/journal.pone.0155055
  8. Precision medicine in alcoholic and nonalcoholic fatty liver disease via modulating the gut microbiota vol.311, pp.6, 2014, https://doi.org/10.1152/ajpgi.00245.2016
  9. 내분비교란물질 비스페놀 A를 처리한 마우스에서 홍삼 추출물의 간 섬유화 개선 vol.30, pp.2, 2014, https://doi.org/10.7732/kjpr.2017.30.2.125
  10. Protective effect of Korean Red Ginseng against FK506-induced damage in LLC-PK1 cells vol.41, pp.3, 2014, https://doi.org/10.1016/j.jgr.2016.05.002
  11. Alcohol extract of North American ginseng (Panax quinquefolius) reduces fatty liver, dyslipidemia, and other complications of metabolic syndrome in a mouse model vol.95, pp.9, 2014, https://doi.org/10.1139/cjpp-2016-0510
  12. Oleoresin urushiol: Can its immunogenicity be exploited for healthcare? vol.104, pp.None, 2014, https://doi.org/10.1016/j.biopha.2018.02.087
  13. Novel C15 Triene Triazole, D-A Derivatives Anti-HepG2, and as HDAC2 Inhibitors: A Synergy Study vol.19, pp.10, 2014, https://doi.org/10.3390/ijms19103184
  14. Ginseng ( Panax ginseng Meyer) Oligopeptides Protect Against Binge Drinking-Induced Liver Damage through Inhibiting Oxidative Stress and Inflammation in Rats vol.10, pp.11, 2014, https://doi.org/10.3390/nu10111665
  15. Are Probiotics Effective in Targeting Alcoholic Liver Diseases? vol.11, pp.2, 2014, https://doi.org/10.1007/s12602-018-9419-6
  16. Synergies of urushiol and its pechmann derivative compatible with paclitaxel anti-HepG2 activity vol.33, pp.16, 2014, https://doi.org/10.1080/14786419.2018.1446013
  17. Fermented‐ Rhus verniciflua extract ameliorate Helicobacter pylori eradication rate and gastritis vol.9, pp.2, 2021, https://doi.org/10.1002/fsn3.2055
  18. In vitro modulatory effects of ginsenoside compound K, 20(S)-protopanaxadiol and 20(S)-protopanaxatriol on uridine 5′-diphospho-glucuronosyltransferase activity and expression vol.51, pp.10, 2014, https://doi.org/10.1080/00498254.2021.1963503
  19. The Gut-Liver Axis in Chronic Liver Disease: A Macrophage Perspective vol.10, pp.11, 2014, https://doi.org/10.3390/cells10112959