Intestinal fungi contribute to development of alcoholic liver disease

Journal of Clinical Investigation

Volumn 127, Issue 7, 2017, Pages 2829-2841

  Yang, An Ming ^a,b   Inamine, Tatsuo ^a,c   Hochrath, Katrin ^a   Chen, Peng ^a   Wang, Lirui ^a,d   Llorente, Cristina ^a,d   Bluemel, Sena ^a   Hartmann, Phillipp ^a   Xu, Jun ^e   Koyama, Yukinori ^e   Kisseleva, Tatiana ^e   Torralba, Manolito G ^f   Moncera, Kelvin ^f   Beeri, Karen ^f   Chen, Chien Sheng ^g   Freese, Kim ^h   Hellerbrand, Claus ^h   Lee, Serene M L ⁱ   Hoffman, Hal M ^a   Mehal, Wajahat Z ^j,k   Garcia Tsao, Guadalupe ^j,k   Mutlu, Ece A ^l   Keshavarzian, Ali ^l   Brown, Gordon D ^m   Ho, Samuel B ^a,d   Bataller, Ramon ⁿ   Stärkel, Peter ^o   Fouts, Derrick E ^f   Schnabl, Bernd ^a,d   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EN CHU KONG HOSPITAL   (Taiwan)

^c NAGASAKI UNIVERSITY   (Japan)

^d VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f J CRAIG VENTER INSTITUTE   (United States)

^g NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^h UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

ⁱ LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^j YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^k VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^l RUSH UNIVERSITY MEDICAL CENTER   (United States)

^m UNIVERSITY OF ABERDEEN   (United Kingdom)

ⁿ UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^o CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

more..

Author keywords

[No Author keywords available]

Indexed keywords

1,3 BETA DEXTRO GLUCAN; ALANINE AMINOTRANSFERASE; ALCOHOL; AMPHOTERICIN B; BETA GLUCAN; DECTIN 1; INTERLEUKIN 1BETA; MESSENGER RNA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CLEC7A PROTEIN, HUMAN; LECTIN;

ALCOHOL CONSUMPTION; ALCOHOL LIVER CIRRHOSIS; ALCOHOL LIVER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS; BONE MARROW CELL; CANDIDA; CANDIDA ALBICANS; CANDIDA PARAPSILOSIS; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; DUODENUM BIOPSY; DYSBIOSIS; FEMALE; FUNGUS; FUNGUS GROWTH; FUSARIUM; HUMAN; HUMAN CELL; HUMICOLA; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INTESTINE; KUPFFER CELL; LIVER BIOPSY; LIVER CELL DAMAGE; LIVER CIRRHOSIS; MORTALITY; MOUSE; MYCOBIOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE FLORA; KNOCKOUT MOUSE; LIVER CELL; METABOLISM; MICROBIOLOGY; PATHOLOGY;

ANIMALS; CANDIDA; GASTROINTESTINAL MICROBIOME; HEPATOCYTES; HUMANS; INTESTINES; KUPFFER CELLS; LECTINS, C-TYPE; LIVER DISEASES, ALCOHOLIC; MICE; MICE, KNOCKOUT;

EID: 85021330462     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI90562     Document Type: Article

References (62)

1. Lozano R, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859):2095-2128.
2. WHO. Global Status Report On Alcohol And Health 2014. World Health Organization website. http://www.who.int/substance-abuse/publications/global-alcohol-report/en/. Accessed April 10, 2017.
3. Bode JC, Bode C, Heidelbach R, Dürr HK, Martini GA. Jejunal microflora in patients with chronic alcohol abuse. Hepatogastroenterology. 1984;31(1):30-34.
4. Yan AW, et al. Enteric dysbiosis associated with a mouse model of alcoholic liver disease. Hepatology. 2011;53(1):96-105.
5. Hartmann P, et al. Deficiency of intestinal mucin-2 ameliorates experimental alcoholic liver disease in mice. Hepatology. 2013;58(1):108-119.
6. Keshavarzian A, et al. Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J Hepatol. 2009;50(3):538-547.
7. Mutlu EA, et al. Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol. 2012;302(9):G966-G978.
8. Iliev ID, et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science. 2012;336(6086):1314-1317.
9. Wang ZK, Yang YS, Stefka AT, Sun G, Peng LH. Review article: fungal microbiota and digestive diseases. Aliment Pharmacol Ther. 2014;39(8):751-766.
10. Iliev ID, Underhill DM. Striking a balance: fungal commensalism versus pathogenesis. Curr Opin Microbiol. 2013;16(3):366-373.
11. Miranda LN, et al. Candida colonisation as a source for candidaemia. J Hosp Infect. 2009;72(1):9-16.
12. Papp M, et al. Presence of anti-microbial antibodies in liver cirrhosis - a tell-tale sign of compromised immunity? PLoS One. 2010;5(9):e12957.
13. Park WB, et al. Spontaneous cryptococcal peritonitis in patients with liver cirrhosis. Am J Med. 2006;119(2):169-171.
14. Bartoletti M, et al. Epidemiology and outcomes of bloodstream infection in patients with cirrhosis. J Hepatol. 2014;61(1):51-58.
15. Gustot T, et al. Invasive aspergillosis in patients with severe alcoholic hepatitis. J Hepatol. 2014;60(2):267-274.
16. Hwang SY, et al. Spontaneous fungal peritonitis: a severe complication in patients with advanced liver cirrhosis. Eur J Clin Microbiol Infect Dis. 2014;33(2):259-264.
17. Theel ES, Doern CD. β-D-glucan testing is important for diagnosis of invasive fungal infections. J Clin Microbiol. 2013;51(11):3478-3483.
18. Dambuza IM, Brown GD. C-type lectins in immunity: recent developments. Curr Opin Immunol. 2015;32:21-27.
19. Kankkunen P, Teirilä L, Rintahaka J, Alenius H, Wolff H, Matikainen S. (1,3)-β-glucans activate both dectin-1 and NLRP3 inflammasome in human macrophages. J Immunol. 2010;184(11):6335-6342.
20. Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology. 2014;146(6):1513-1524.
21. Chen P, et al. Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology. 2015;148(1):203-214.e16.
22. Wang L, et al. Intestinal REG3 lectins protect against alcoholic steatohepatitis by reducing mucosa-associated microbiota and preventing bacterial translocation. Cell Host Microbe. 2016;19(2):227-239.
23. Chen P, Stärkel P, Turner JR, Ho SB, Schnabl B. Dysbiosis-induced intestinal inflammation activates tumor necrosis factor receptor I and mediates alcoholic liver disease in mice. Hepatology. 2015;61(3):883-894.
24. Kobayashi K, Hernandez LD, Galán JE, Janeway CA, Medzhitov R, Flavell RA. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell. 2002;110(2):191-202.
25. Taylor PR, et al. The β-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol. 2002;169(7):3876-3882.
26. Seki E, et al. TLR4 enhances TGF-β signaling and hepatic fibrosis. Nat Med. 2007;13(11):1324-1332.
27. Petrasek J, et al. IL-1 receptor antagonist ameliorates inflammasome-dependent alcoholic steatohepatitis in mice. J Clin Invest. 2012;122(10):3476-3489.
28. Niemelä O, Parkkila S, Bradford B, Iimuro Y, Pasanen M, Thurman RG. Effect of Kupffer cell inactivation on ethanol-induced protein adducts in the liver. Free Radic Biol Med. 2002;33(3):350-355.
29. Ganesan S, et al. Caspase-8 modulates dectin-1 and complement receptor 3-driven IL-1β production in response to β-glucans and the fungal pathogen, Candida albicans. J Immunol. 2014;193(5):2519-2530.
30. Standaert-Vitse A, et al. Candida albicans is an immunogen for anti-Saccharomyces cerevisiae antibody markers of Crohn's disease. Gastroenterology. 2006;130(6):1764-1775.
31. Sokol H, et al. Fungal microbiota dysbiosis in IBD [published online ahead of print February 3, 2016]. Gut. https://doi.org/10.1136/gutjnl-2015-310746.
32. Lilly LM, et al. The β-glucan receptor dectin-1 promotes lung immunopathology during fungal allergy via IL-22. J Immunol. 2012;189(7):3653-3660.
33. Szabo G. Gut-liver axis in alcoholic liver disease. Gastroenterology. 2015;148(1):30-36.
34. Kirpich IA, et al. Saturated and unsaturated dietary fats differentially modulate ethanol-induced changes in gut microbiome and metabolome in a mouse model of alcoholic liver disease. Am J Pathol. 2016;186(4):765-776.
35. Du Plessis J, et al. Activated intestinal macrophages in patients with cirrhosis release NO and IL-6 that may disrupt intestinal barrier function. J Hepatol. 2013;58(6):1125-1132.
36. Wang Y, et al. Lactobacillus rhamnosus GG treatment potentiates intestinal hypoxia-inducible factor, promotes intestinal integrity and ameliorates alcohol-induced liver injury. Am J Pathol. 2011;179(6):2866-2875.
37. Yamahiro A, Lau KH, Peaper DR, Villanueva M. Meningitis caused by Candida Dubliniensis in a patient with cirrhosis: a case report and review of the literature. Mycopathologia. 2016;181(7-8):589-593.
38. Chen SC, et al. Candidaemia with uncommon Candida species: predisposing factors, outcome, antifungal susceptibility, and implications for management. Clin Microbiol Infect. 2009;15(7):662-669.
39. Wang Y, et al. Role of IRAK-M in alcohol induced liver injury. PLoS One. 2013;8(2):e57085.
40. Taylor PR, et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol. 2007;8(1):31-38.
41. Wagner M, Srivastava KK. Decontamination of gnotobiotic mice experimentally monoassociated with Candida albicans. Infect Immun. 1975;12(6):1401-1404.
42. Fouts DE, Torralba M, Nelson KE, Brenner DA, Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J Hepatol. 2012;56(6):1283-1292.
43. Maeda H, et al. Quantitative real-time PCR using TaqMan and SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol Med Microbiol. 2003;39(1):81-86.
44. Liu CM, et al. FungiQuant: a broad-coverage fungal quantitative real-time PCR assay. BMC Microbiol. 2012;12:255.
45. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112-5120.
46. Fouts DE, et al. Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS One. 2012;7(11):e48289.
47. Bokulich NA, Mills DA. Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol. 2013;79(8):2519-2526.
48. Bokulich NA, Thorngate JH, Richardson PM, Mills DA. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc Natl Acad Sci U S A. 2014;111(1):E139-E148.
49. Schloss PD, et al. Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537-7541.
50. Fouts DE, et al. Integrated next-generation sequencing of 16S rDNA and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J Transl Med. 2012;10:174.
51. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150-3152.
52. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22(13):1658-1659.
53. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261-5267.
54. Tang J, Iliev ID, Brown J, Underhill DM, Funari VA. Mycobiome: Approaches to analysis of intestinal fungi. J Immunol Methods. 2015;421:112-121.
55. Fettweis JM, et al. Species-level classification of the vaginal microbiome. BMC Genomics. 2012;13(suppl 8):S17.
56. Iwaisako K, et al. Protection from liver fibrosis by a peroxisome proliferator-activated receptor δ agonist. Proc Natl Acad Sci U S A. 2012;109(21):E1369-E1376.
57. Kisseleva T, et al. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc Natl Acad Sci U S A. 2012;109(24):9448-9453.
58. Brydges SD, Broderick L, McGeough MD, Pena CA, Mueller JL, Hoffman HM. Divergence of IL-1, IL-18, and cell death in NLRP3 inflammasomopathies. J Clin Invest. 2013;123(11):4695-4705.
59. Lee SM, Schelcher C, Demmel M, Hauner M, Thasler WE. Isolation of human hepatocytes by a two-step collagenase perfusion procedure. J Vis Exp. 2013;(79):50615.
60. Steiling H, Mühlbauer M, Bataille F, Schölmerich J, Werner S, Hellerbrand C. Activated hepatic stellate cells express keratinocyte growth factor in chronic liver disease. Am J Pathol. 2004;165(4):1233-1241.
61. Thasler WE, Weiss TS, Schillhorn K, Stoll PT, Irrgang B, Jauch KW. Charitable state-controlled foundation human tissue and cell research: ethic and legal aspects in the supply of surgically removed human tissue for research in the academic and commercial sector in Germany. Cell Tissue Bank. 2003;4(1):49-56.
62. Yang AM, Wen LL, Yang CS, Wang SC, Chen CS, Bair MJ. Interleukin 10 promoter haplotype is associated with alcoholic liver cirrhosis in Taiwanese patients. Kaohsiung J Med Sci. 2014;30(6):291-298.