Age-related immune clearance of hepatitis B virus infection requires the establishment of gut microbiota

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 7, 2015, Pages 2175-2180

  Chou, Han Hsuan ^a   Chien, Wei Hung ^a,b   Wu, Li Ling ^a   Cheng, Chi Hung ^a   Chung, Chen Han ^a   Horng, Jau Haw ^a   Ni, Yen Hsuan ^c   Tseng, Hong Tai ^a   Wu, Dafei ^d   Lu, Xuemei ^d   Wang, Hurng Yi ^a,e   Chen, Pei Jer ^a   Chen, Ding Shinn ^a,f  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f GENOMICS RESEARCH CENTER   (Taiwan)

Author keywords

Chronic hepatitis B; Kupffer cells; Liver tolerance; Temporal temperature gel electrophoresis; Toll like 4 receptor

Indexed keywords

AMPICILLIN; HEPATITIS B SURFACE ANTIGEN; METRONIDAZOLE; NEOMYCIN; TOLL LIKE RECEPTOR; VANCOMYCIN;

ADAPTIVE IMMUNITY; ADULT; AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ANTIBODY PRODUCTION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; HAPLOTYPE; HEPATITIS B; HEPATITIS B VIRUS; HUMORAL IMMUNITY; HYDRODYNAMICS BASED TRANSFECTION; INNATE IMMUNITY; INTESTINE FLORA; MOUSE; NONHUMAN; NORTHERN BLOTTING; PORTAL VEIN BLOOD FLOW; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; VIRAL CLEARANCE; VIRUS IMMUNITY; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; HUMAN; IMMUNOLOGY; INTESTINE; MICROBIOLOGY; MICROFLORA; NONOBESE DIABETIC MOUSE;

HEPATITIS B VIRUS; MUS;

ANIMALS; HEPATITIS B; HUMANS; INTESTINES; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICROBIOTA;

EID: 84983722767     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1424775112     Document Type: Article

References (34)

1. Cowie BC, Carville KS, MacLachlan JH (2013) Mortality due to viral hepatitis in the Global Burden of Disease Study 2010: New evidence of an urgent global public health priority demanding action. Antivir Ther 18(8):953-954.
2. Chen DS (1993) From hepatitis to hepatoma: Lessons from type B viral hepatitis. Science 262(5132):369-370.
3. Lin TM, et al. (1989) Hepatitis B virus markers in Chinese twins. Anticancer Res 9(3): 737-741.
4. Thursz M (2001) Genetic susceptibility in chronic viral hepatitis. Antiviral Res 52(2): 113-116.
5. Ben-Ari Z, et al. (2003) Cytokine gene polymorphisms in patients infected with hepatitis B virus. Am J Gastroenterol 98(1):144-150.
6. Thio CL, et al. (2004) Cytotoxic T-lymphocyte antigen 4 gene and recovery from hepatitis B virus infection. J Virol 78(20):11258-11262.
7. Godkin A, Davenport M, Hill AV (2005) Molecular analysis of HLA class II associations with hepatitis B virus clearance and vaccine nonresponsiveness. Hepatology 41(6): 1383-1390.
8. Thursz MR, et al. (1995) Association between an MHC class II allele and clearance of hepatitis B virus in the Gambia. N Engl J Med 332(16):1065-1069.
9. Kamatani Y, et al. (2009) A genome-wide association study identifies variants in the HLA-DP locus associated with chronic hepatitis B in Asians. Nat Genet 41(5):591-595.
10. Mbarek H, et al. (2011) A genome-wide association study of chronic hepatitis B identified novel risk locus in a Japanese population. Hum Mol Genet 20(19):3884-3892.
11. Ganem D, Prince AM (2004) Hepatitis B virus infection: Natural history and clinical consequences. N Engl J Med 350(11):1118-1129.
12. Liang TJ (2009) Hepatitis B: The virus and disease. Hepatology 49(5 Suppl):S13-S21.
13. Milich DR, et al. (1990) Is a function of the secreted hepatitis B e antigen to induce immunologic tolerance in utero? Proc Natl Acad Sci USA 87(17):6599-6603.
14. Milich DR, Jones J, Hughes J, Maruyama T (1993) Role of T-cell tolerance in the persistence of hepatitis B virus infection. J Immunother Emphasis Tumor Immunol 14(3): 226-233.
15. Molloy MJ, Bouladoux N, Belkaid Y (2012) Intestinal microbiota: Shaping local and systemic immune responses. Semin Immunol 24(1):58-66.
16. Belkaid Y, Naik S (2013) Compartmentalized and systemic control of tissue immunity by commensals. Nat Immunol 14(7):646-653.
17. Knolle PA, et al. (1998) IL-10 down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells through decreased antigen uptake via the mannose receptor and lowered surface expression of accessory molecules. Clin Exp Immunol 114(3):427-433.
18. Limmer A, et al. (2000) Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 6(12): 1348-1354.
19. Knolle P, et al. (1995) Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. J Hepatol 22(2):226-229.
20. Bissell DM, Wang SS, Jarnagin WR, Roll FJ (1995) Cell-specific expression of transforming growth factor-beta in rat liver. Evidence for autocrine regulation of hepatocyte proliferation. J Clin Invest 96(1):447-455.
21. Schuchmann M, et al. (2004) HSP60 and CpG-DNA-oligonucleotides differentially regulate LPS-tolerance of hepatic Kupffer cells. Immunol Lett 93(2-3):199-204.
22. Huang LR, et al. (2013) Intrahepatic myeloid-cell aggregates enable local proliferation of CD8(+) T cells and successful immunotherapy against chronic viral liver infection. Nat Immunol 14(6):574-583.
23. Wiegard C, et al. (2005) Murine liver antigen presenting cells control suppressor activity of CD4+CD25+ regulatory T cells. Hepatology 42(1):193-199.
24. Huang LR, Wu HL, Chen PJ, Chen DS (2006) An immunocompetent mouse model for the tolerance of human chronic hepatitis B virus infection. Proc Natl Acad Sci USA 103(47):17862-17867.
25. Yoshimoto S, et al. (2013) Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499(7456):97-101.
26. Ivanov II, et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139(3):485-498.
27. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH (2009) Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun 77(7):2741-2753.
28. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118(2):229-241.
29. Xu L, Yin W, Sun R, Wei H, Tian Z (2014) Kupffer cell-derived IL-10 plays a key role in maintaining humoral immune tolerance in hepatitis B virus-persistent mice. Hepatology 59(2):443-452.
30. Corbitt N, et al. (2013) Gut bacteria drive Kupffer cell expansion via MAMP-mediated ICAM-1 induction on sinusoidal endothelium and influence preservation-reperfusion injury after orthotopic liver transplantation. Am J Pathol 182(1):180-191.
31. Publicover J, et al. (2013) Age-dependent hepatic lymphoid organization directs successful immunity to hepatitis B. J Clin Invest 123(9):3728-3739.
32. Ayres JS, Schneider DS (2012) Tolerance of infections. Annu Rev Immunol 30:271-294.
33. Watanabe K, Kodama Y, Harayama S (2001) Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting. J Microbiol Methods 44(3):253-262.
34. Larsen N, et al. (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5(2):e9085.