Effect of Korea red ginseng on nonalcoholic fatty liver disease: an association of gut microbiota with liver function |
Hong, Ji Taek
(Institute for Liver and Digestive Diseases, Hallym University)
Lee, Min-Jung (Department of Life Science, Multidisciplinary Genome Institute, Hallym University) Yoon, Sang Jun (Institute for Liver and Digestive Diseases, Hallym University) Shin, Seok Pyo (Institute for Liver and Digestive Diseases, Hallym University) Bang, Chang Seok (Institute for Liver and Digestive Diseases, Hallym University) Baik, Gwang Ho (Institute for Liver and Digestive Diseases, Hallym University) Kim, Dong Joon (Institute for Liver and Digestive Diseases, Hallym University) Youn, Gi Soo (Institute for Liver and Digestive Diseases, Hallym University) Shin, Min Jea (Institute for Liver and Digestive Diseases, Hallym University) Ham, Young Lim (Department of Nursing, Daewon University College) Suk, Ki Tae (Institute for Liver and Digestive Diseases, Hallym University) Kim, Bong-Soo (Department of Life Science, Multidisciplinary Genome Institute, Hallym University) |
1 | Kim H-G, Cho J-H, Yoo S-R, Lee J-S, Han J-M, Lee N-H, Ahn Y-C, Son C-G. Antifatigue effects of Panax ginseng CA Meyer: a randomised, double-blind, placebo-controlled trial. PloS One 2013;8:e61271. DOI |
2 | Hu J, Ma L, Nie Y, Chen J, Zheng W, Wang X, Xie C, Zheng Z, Wang Z, Yang T, et al. A microbiota-derived bacteriocin targets the host to confer diarrhea resistance in early-weaned piglets. Cell Host Microbe 2018;24:817-832 e8. DOI |
3 | Helenius TO, Antman CA, Asghar MN, Nystrom JH, Toivola DM. Keratins are altered in intestinal disease-related stress responses. Cells 2016;5. |
4 | Cho YJ, Son HJ, Kim KS. A 14-week randomized, placebo-controlled, double-blind clinical trial to evaluate the efficacy and safety of ginseng polysaccharide (Y-75). J Transl Med 2014;12:283. DOI |
5 | Yeo CR, Yang C, Wong TY, Popovich DG. A quantified ginseng (Panax ginseng C.A. Meyer) extract influences lipid acquisition and increases adiponectin expression in 3T3-L1 cells. Molecules 2011;16:477-92. DOI |
6 | Janssen AW, Houben T, Katiraei S, Dijk W, Boutens L, Van Der Bolt N, Wang Z, Brown JM, Hazen SL, Mandard S. Modulation of the gut microbiota impacts nonalcoholic fatty liver disease: a potential role for bile acids. J Lipid Res 2017;58:1399-416. DOI |
7 | Mouzaki M, Comelli EM, Arendt BM, Bonengel J, Fung SK, Fischer SE, McGilvray ID, Allard JP. Intestinal microbiota in patients with nonalcoholic fatty liver disease. Hepatology 2013;58:120-7. DOI |
8 | Mao J, Qi S, Cui Y, Dou X, Luo XM, Liu J, Zhu T, Ma Y, Wang H. Lactobacillus rhamnosus GG attenuates lipopolysaccharide-induced inflammation and barrier dysfunction by regulating MAPK/NF-kappaB signaling and modulating metabolome in the piglet intestine. J Nutr 2020. |
9 | Schuppan D, Schattenberg JM. Non-alcoholic steatohepatitis: pathogenesis and novel therapeutic approaches. J Gastroenterol Hepatol 2013;28:68-76. DOI |
10 | Brunt EM, Wong VW-S, Nobili V, Day CP, Sookoian S, Maher JJ, Bugianesi E, Sirlin CB, Neuschwander-Tetri BA, Rinella ME. Nonalcoholic fatty liver disease. Nat Rev Dis Primers 2015;1:15080. DOI |
11 | Chen CC, Lai CC, Huang HL, Su YT, Chiu YH, Toh HS, Chiang SR, Chuang YC, Lu YC, Tang HJ. Antimicrobial ability and mechanism analysis of Lactobacillus species against carbapenemase-producing Enterobacteriaceae. J Microbiol Immunol Infect 2020. |
12 | Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002;346:1221-31. DOI |
13 | Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, Almeida M, Arumugam M, Batto J-M, Kennedy S. Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541. DOI |
14 | Tsutsui M, Tanaka N, Kawakubo M, Sheena Y, Horiuchi A, Komatsu M, Nagaya T, Joshita S, Umemura T, T Ichijo. Serum fragmented cytokeratin 18 levels reflect the histologic activity score of nonalcoholic fatty liver disease more accurately than serum alanine aminotransferase levels. J Clin Gastroenter 2010;44:440-7. DOI |
15 | Ren Q, Yang B, Zhu G, Wang S, Fu C, Zhang H, Ross RP, Stanton C, Chen H, Chen W. Antiproliferation Activity and Mechanism of c9, t11, c15-CLNA and t9, t11, c15-CLNA from Lactobacillus plantarum ZS2058 on Colon Cancer Cells. Molecules 2020;25. |
16 | Heo SB, Lim SW, Jhun JY, La Cho M, Chung BH, Yang CW. Immunological benefits by ginseng through reciprocal regulation of Th17 and Treg cells during cyclosporine-induced immunosuppression. J Ginseng Res 2016;40:18-27. DOI |
17 | Kargulewicz A, Stankowiak-Kulpa H, Grzymislawski MJ. Dietary recommendations for patients with nonalcoholic fatty liver disease. Prz Gastroenterol 2014;9:18. |
18 | Nassir F, Ibdah J. Role of mitochondria in nonalcoholic fatty liver disease. Int J Mol Sci 2014;15:8713-42. DOI |
19 | Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J. Introducing EzBio-Cloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613. DOI |
20 | Kolodziejczyk AA, Zheng D, Shibolet O, Elinav EJ. The role of the microbiome in NAFLD and NASH. EMBO Mol Med 2019;11. |
21 | Murthy HN, Dandin VS, Paek KY. Hepatoprotective activity of ginsenosides from Panax ginseng adventitious roots against carbon tetrachloride treated hepatic injury in rats. J Ethnopharmacol 2014;158:442-6. DOI |
22 | Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537-41. DOI |
23 | Zakrzewski M, Proietti C, Ellis JJ, Hasan S, Brion M-J, Berger B, Krause L. Calypso: a user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics 2016;33:782-3. DOI |
24 | Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower CJ. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60. DOI |
25 | Gui QF, Xu ZR, Xu KY, Yang YM. The efficacy of ginseng-related therapies in type 2 diabetes mellitus: an updated systematic review and meta-analysis. Medicine (Baltimore) 2016;95:e2584. DOI |
26 | Hong SH, Suk KT, Choi SH, Lee JW, Sung HT, Kim CH, Kim EJ, Kim MJ, Han SH, Kim MY. Anti-oxidant and natural killer cell activity of Korean red ginseng (Panax ginseng) and urushiol (Rhus vernicifera Stokes) on non-alcoholic fatty liver disease of rat. Food Chem Toxicol 2013;55:586-91. DOI |
27 | Adolph TE, Grander C, Moschen AR, Tilg HJT. Liver-microbiome axis in health and disease. Trends Immunol 2018;39:712-23. DOI |
28 | Stanislawski MA, Lozupone CA, Wagner BD, Eggesbo M, Sontag MK, Nusbacher NM, Martinez M, Dabelea DJ. Gut microbiota in adolescents and the association with fatty liver: the EPOCH study. Pediatr Res 2018. |
29 | Sharpton SR, Ajmera V, Loomba RJCG. Emerging role of the gut microbiome in nonalcoholic fatty liver disease: from composition to function. Clin Gastroenterol Hepatol 2019;17:296-306. DOI |
30 | Shen L, Xiong Y, Wang DQ, Howles P, Basford JE, Wang J, Xiong YQ, Hui DY, Woods SC, Liu M. Ginsenoside Rb1 reduces fatty liver by activating AMP-activated protein kinase in obese rats. J Lipid Res 2013;54:1430-8. DOI |
31 | Jiang C, Xie C, Li F, Zhang L, Nichols RG, Krausz KW, Cai J, Qi Y, Fang Z-Z, Takahashi SJT. Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J Clin Invest 2015;125:386-402. DOI |
32 | Korean Association for the Study of the L. KASL clinical practice guidelines: management of nonalcoholic fatty liver disease. Clin Mol Hepatol 2013;19:325-48. DOI |
33 | Bang CS, Hong SH, Suk KT, Kim JB, Han SH, Sung H, Kim EJ, Kim MJ, Kim MY, Baik SK. 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. J Ginseng Res 2014;38:167-72. DOI |
34 | Jeong H, Kim J-W, Yang M-S, Park C, Kim JH, Lim CW, Kim BJT. Beneficial effects of Korean red ginseng in the progression of non-alcoholic steatohepatitis via FABP4 modulation. Am J Chinese Med 2018;46:1581-607. DOI |
35 | Hong M, Lee YH, Kim S, Suk KT, Bang CS, Yoon JH, Baik GH, Kim DJ, Kim MJJ. Anti-inflammatory and antifatigue effect of Korean Red Ginseng in patients with nonalcoholic fatty liver disease. J Ginseng Res 2016;40:203-10. DOI |
36 | George ES, Forsyth A, Itsiopoulos C, Nicoll AJ, Ryan M, Sood S, Roberts SK, Tierney ACJ. Practical dietary recommendations for the prevention and management of nonalcoholic fatty liver disease in adults. Adv Nutr 2018;9:30-40. DOI |
37 | Jeong TC, Kim HJ, Park JI, Ha CS, Park JD, Kim SI, Roh JK. Protective effects of red ginseng saponins against carbon tetrachloride-induced hepatotoxicity in Sprague Dawley rats. Planta Med 1997;63:136-40. DOI |
38 | Papatheodoridis GV, Hadziyannis E, Tsochatzis E, Georgiou A, Kafiri G, Tiniakos DG, Margariti K, Manolakopoulos S, Manesis EK, Archimandritis AJJ. Serum apoptotic caspase activity in chronic hepatitis C and nonalcoholic Fatty liver disease. J Clin Gastroenter 2010;44:e87-95. DOI |
39 | Morris G, Berk M, Walder K, Maes M. Central pathways causing fatigue in neuro-inflammatory and autoimmune illnesses. BMC Med 2015;13:28. DOI |
40 | Mehta M, Duseja A, Mitra S, Das A, Taneja S, Dhiman R, Chawla YJ. Cytokeratin-18 (CK-18) is A useful biomarker in differentiating between NASH and No-NASH amongst patients with nonalcoholic fatty liver disease (NAFLD). J Clin Exp Hepatol 2017;7:S44. |
41 | Schweizer J, Bowden PE, Coulombe PA, Langbein L, Lane EB, Magin TM, Maltais L, Omary MB, Parry DA, Rogers MA. New consensus nomenclature for mammalian keratins. J Cell Biol 2006;174:169-74. DOI |
42 | Jang HR, Park HJ, Kang D, Chung H, Nam MH, Lee Y, Park JH, Lee HY. A protective mechanism of probiotic Lactobacillus against hepatic steatosis via reducing host intestinal fatty acid absorption. Exp Mol Med 2019;51:1-14. |
43 | Brunt EM. Nonalcoholic fatty liver disease: what the pathologist can tell the clinician. Digest Dis 2012;30:61-8. DOI |
44 | Seo S-J, Cho JY, Jeong YH, Choi Y-S. Effect of Korean red ginseng extract on liver damage induced by short-term and long-term ethanol treatment in rats. J Ginseng Res 2013;37:194. DOI |
45 | Pei R-J, Danbara N, Tsujita-Kyutoku M, Yuri T, Tsubura A. Immunohistochemical profiles of Mallory body by a panel of anti-cytokeratin antibodies. Med Electron Microsc 2004;37:114-8. |
46 | Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, Guy CD, Seed PC, Rawls JF, David LA. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 2016;63:764-75. DOI |
47 | Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005;41:1313-21. DOI |
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