Influence of gut bacteria on development and progression of non-alcoholic fatty liver disease

World Journal of Hepatology

Volumn 7, Issue 12, 2015, Pages 1679-1684

  Abdul Hai, Ali ^a   Abdallah, Ali ^a   Malnick, Stephen D H ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Metabolic syndrome; Microbiome; Non alcoholic fatty liver disease; Stool transplantation

Indexed keywords

EID: 84934293973     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v7.i12.1679     Document Type: Short Survey

References (49)

1. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40: 1387-1395 [PMID: 15565570 DOI: 10.1002/hep.20466].
2. Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, Landt CL, Harrison SA. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middleaged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 2011; 140: 124-131 [PMID: 20858492 DOI: 10.1053/j.gastro.2010.09.038].
3. Caldwell S, Argo C. The natural history of non-alcoholic fatty liver disease. Dig Dis 2010; 28: 162-168 [PMID: 20460906].
4. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science 2012; 336: 1262-1267 [PMID: 22674330 DOI: 10.1126/science.1223813].
5. Floch MH. The power of poop: probiotics and fecal microbial transplant. J Clin Gastroenterol 2012; 46: 625-626 [PMID: 22874805 DOI: 10.1097/MCG.0b013e3182667a93].
6. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008; 6: 776-788 [PMID: 18794915 DOI: 10.1038/nrmicro1978].
7. Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 1998; 64: 3854-3859 [PMID: 9758810].
8. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 2009; 1: 6ra14 [PMID: 20368178 DOI: 10.1126/scitranslmed.3000322].
9. Bowey E, Adlercreutz H, Rowland I. Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem Toxicol 2003; 41: 631-636 [PMID: 12659715].
10. Gérard P, Béguet F, Lepercq P, Rigottier-Gois L, Rochet V, Andrieux C, Juste C. Gnotobiotic rats harboring human intestinal microbiota as a model for studying cholesterol-to-coprostanol conversion. FEMS Microbiol Ecol 2004; 47: 337-343 [PMID: 19712322 DOI: 10.1016/S0168-6496(03)00285-X].
11. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013; 341: 1241214 [PMID: 24009397 DOI: 10.1126/science.1241214].
12. Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 2014; 146: 1513-1524 [PMID: 24440671 DOI: 10.1053/j.gastro.2014.01.020].
13. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-15723 [PMID: 15505215 DOI: 10.1073/pnas. 0407076101].
14. Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 2007; 104: 979-984 [PMID: 17210919 DOI: 10.1073/pnas.0605374104].
15. Rabot S, Membrez M, Bruneau A, Gérard P, Harach T, Moser M, Raymond F, Mansourian R, Chou CJ. Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. FASEB J 2010; 24: 4948-4959 [PMID: 20724524 DOI: 10.1096/fj.10-164921].
16. Jang I, Hwang D, Lee J, Chae K, Kim Y, Kang T, Kim C, Shin D, Hwang J, Huh Y, Cho J. Physiological difference between dietary obesity-susceptible and obesity-resistant Sprague Dawley rats in response to moderate high fat diet. Exp Anim 2003; 52: 99-107 [PMID: 12806884].
17. Li H, Xie Z, Lin J, Song H, Wang Q, Wang K, Su M, Qiu Y, Zhao T, Song K, Wang X, Zhou M, Liu P, Zhao G, Zhang Q, Jia W. Transcriptomic and metabonomic profiling of obesity-prone and obesity-resistant rats under high fat diet. J Proteome Res 2008; 7: 4775-4783 [PMID: 18828625].
18. Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A, Perlemuter G, Cassard-Doulcier AM, Gérard P. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 2013; 62: 1787-1794 [PMID: 23197411 DOI: 10.1136/gutjnl-2012-303816].
19. Caesar R, Reigstad CS, Bäckhed HK, Reinhardt C, Ketonen M, Lundén Gö, Cani PD, Bäckhed F. Gut-derived lipopolysaccharide augments adipose macrophage accumulation but is not essential for impaired glucose or insulin tolerance in mice. Gut 2012; 61: 1701-1707 [PMID: 22535377 DOI: 10.1136/gutjnl-2011-301689].
20. Membrez M, Blancher F, Jaquet M, Bibiloni R, Cani PD, Burcelin RG, Corthesy I, Macé K, Chou CJ. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J 2008; 22: 2416-2426 [PMID: 18326786 DOI: 10.1096/fj.07-102723].
21. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012; 143: 913-6.e7 [PMID: 22728514 DOI: 10.1053/j.gastro.2012.06.031].
22. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008; 3: 213-223 [PMID: 18407065 DOI: 10.1016/j.chom.2008.02.015].
23. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmée E, Cousin B, Sulpice T, Chamontin B, Ferrières J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-1772 [PMID: 17456850 DOI: 10.2337/db06-1491].
24. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007; 50: 2374-2383 [PMID: 17823788 DOI: 10.1007/s00125-007-0791-0].
25. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031 [PMID: 17183312 DOI: 10.1038/nature05414].
26. Dumas ME, Barton RH, Toye A, Cloarec O, Blancher C, Rothwell A, Fearnside J, Tatoud R, Blanc V, Lindon JC, Mitchell SC, Holmes E, McCarthy MI, Scott J, Gauguier D, Nicholson JK. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci USA 2006; 103: 12511-12516 [PMID: 16895997 DOI: 10.1073/pnas.0601056103].
27. Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, Bailey J, Myers RP, Rioux KP. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2013; 11: 868-875.e1-3 [PMID: 23454028].
28. 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: 120-127 [PMID: 23401313].
29. Zhu L, Baker SS, Gill C, Liu W, Alkhouri R, Baker RD, Gill SR. Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology 2013; 57: 601-609 [PMID: 23055155 DOI: 10.1002/hep.26093].
30. Wong VW, Tse CH, Lam TT, Wong GL, Chim AM, Chu WC, Yeung DK, Law PT, Kwan HS, Yu J, Sung JJ, Chan HL. Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis-a longitudinal study. PLoS One 2013; 8: e62885 [PMID: 23638162 DOI: 10.1371/journal.pone.0062885].
31. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, Mascianà R, Forgione A, Gabrieli ML, Perotti G, Vecchio FM, Rapaccini G, Gasbarrini G, Day CP, Grieco A. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1877-1887 [PMID: 19291785 DOI: 10.1002/hep.22848].
32. Sabaté JM, Jouët P, Harnois F, Mechler C, Msika S, Grossin M, Coffin B. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes Surg 2008; 18: 371-377 [PMID: 18286348 DOI: 10.1007/s11695-007-9398-2].
33. Wigg AJ, Roberts-Thomson IC, Dymock RB, McCarthy PJ, Grose RH, Cummins AG. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut 2001; 48: 206-211 [PMID: 11156641].
34. Cope K, Risby T, Diehl AM. Increased gastrointestinal ethanol production in obese mice: implications for fatty liver disease pathogenesis. Gastroenterology 2000; 119: 1340-1347 [PMID: 11054393].
35. Hartmann P, Chen WC, Schnabl B. The intestinal microbiome and the leaky gut as therapeutic targets in alcoholic liver disease. Front Physiol 2012; 3: 402 [PMID: 23087650 DOI: 10.3389/fphys.2012.00402].
36. Day CP. Pathogenesis of steatohepatitis. Best Pract Res Clin Gastroenterol 2002; 16: 663-678 [PMID: 12406438].
37. Blumberg H, McCollum EV. The prevention by choline of liver cirrhosis in rats on high fat, low protein diets. Science 1941; 93: 598-599 [PMID: 17795968 DOI: 10.1126/science.93.2425.598].
38. Jiang XC, Li Z, Liu R, Yang XP, Pan M, Lagrost L, Fisher EA, Williams KJ. Phospholipid transfer protein deficiency impairs apolipoprotein-B secretion from hepatocytes by stimulating a proteolytic pathway through a relative deficiency of vitamin E and an increase in intracellular oxidants. J Biol Chem 2005; 280: 18336-18340 [PMID: 15734742 DOI: 10.1074/jbc.M500007200].
39. Farhadi A, Gundlapalli S, Shaikh M, Frantzides C, Harrell L, Kwasny MM, Keshavarzian A. Susceptibility to gut leakiness: a possible mechanism for endotoxaemia in non-alcoholic steatohepatitis. Liver Int 2008; 28: 1026-1033 [PMID: 18397235 DOI: 10.1111/j.1478-3231.2008.01723.x].
40. Saberi M, Woods NB, de Luca C, Schenk S, Lu JC, Bandyopadhyay G, Verma IM, Olefsky JM. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 2009; 10: 419-429 [PMID: 19883619 DOI: 10.1016/j.cmet.2009.09.006].
41. Miura K, Kodama Y, Inokuchi S, Schnabl B, Aoyama T, Ohnishi H, Olefsky JM, Brenner DA, Seki E. Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1beta in mice. Gastroenterology 2010; 139: 323-34.e7 [PMID: 20347818 DOI: 10.1053/j.gastro.2010.03.052].
42. Rivera CA, Adegboyega P, van Rooijen N, Tagalicud A, Allman M, Wallace M. Toll-like receptor-4 signaling and Kupffer cells play pivotal roles in the pathogenesis of non-alcoholic steatohepatitis. J Hepatol 2007; 47: 571-579 [PMID: 17644211 DOI: 10.1016/j.jhep.2007.04.019].
43. Yang SQ, Lin HZ, Lane MD, Clemens M, Diehl AM. Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc Natl Acad Sci USA 1997; 94: 2557-2562 [PMID: 9122234].
44. Ma YY, Li L, Yu CH, Shen Z, Chen LH, Li YM. Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis. World J Gastroenterol 2013; 19: 6911-6918 [PMID: 24187469].
45. Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NM, Magness S, Jobin C, Lund PK. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One 2010; 5: e12191 [PMID: 20808947 DOI: 10.3748/wjg.v19.i40.6911].
46. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, Thaiss CA, Kau AL, Eisenbarth SC, Jurczak MJ, Camporez JP, Shulman GI, Gordon JI, Hoffman HM, Flavell RA. Inflammasomemediated dysbiosis regulates progression of NAFLD and obesity. Nature 2012; 482: 179-185 [PMID: 22297845 DOI: 10.1038/nature10809].
47. Zhang F, Luo W, Shi Y, Fan Z, Ji G. Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol 2012; 107: 1755; author reply p.1755-p.1756 [PMID: 23160295 DOI: 10.1038/ajg.2012.251].
48. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 1958; 44: 854-859 [PMID: 13592638].
49. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, Speelman P, Dijkgraaf MG, Keller JJ. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 2013; 368: 407-415 [PMID: 23323867 DOI: 10.1056/NEJMoa1205037].