Gut microbiota modulate the immune effect against hepatitis B virus infection

European Journal of Clinical Microbiology and Infectious Diseases

Volumn 34, Issue 11, 2015, Pages 2139-2147

  Xu, D ^a   Huang, Y ^a   Wang, J ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE;

ADAPTIVE IMMUNITY; BACTERIAL COLONIZATION; DISEASE SEVERITY; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; INTESTINE FLORA; LIVER INJURY; NATURAL KILLER T CELL; PASSIVE IMMUNIZATION; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; VERTICAL TRANSMISSION; VIRUS IMMUNITY; VIRUS REPLICATION; IMMUNOLOGY;

GASTROINTESTINAL MICROBIOME; HEPATITIS B; HEPATITIS B VIRUS; HUMANS;

EID: 84944355196     PISSN: 09349723     EISSN: 14354373     Source Type: Journal    
DOI: 10.1007/s10096-015-2464-0     Document Type: Review

References (90)

1. Revill P, Yuan Z (2013) New insights into how HBV manipulates the innate immune response to establish acute and persistent infection. Antivir Ther 18(1):1–15
2. Trépo C, Chan HL, Lok A (2014) Hepatitis B virus infection. Lancet 384(9959):2053–2063
3. Kato LM, Kawamoto S, Maruya M, Fagarasan S (2014) The role of the adaptive immune system in regulation of gut microbiota. Immunol Rev 260(1):67–75
4. Festi D, Schiumerini R, Eusebi LH, Marasco G, Taddia M, Colecchia A (2014) Gut microbiota and metabolic syndrome. World J Gastroenterol 20(43):16079–16094
5. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, Iwasaki A (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108(13):5354–5359
6. Edelman SM, Kasper DL (2008) Symbiotic commensal bacteria direct maturation of the host immune system. Curr Opin Gastroenterol 24(6):720–724
7. Xue X, Feng T, Yao S, Wolf KJ, Liu CG, Liu X, Elson CO, Cong Y (2011) Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J Immunol 187(11):5879–5886
8. Cesaro C, Tiso A, Del Prete A, Cariello R, Tuccillo C, Cotticelli G, Del Vecchio Blanco C, Loguercio C (2011) Gut microbiota and probiotics in chronic liver diseases. Dig Liver Dis 43(6):431–438
9. Chen C, Yu X, Lu H, Xiao D, Mao W, Li L (2013) Antioxidant protective effects of lactitol against endotoxemia in patients with chronic viral hepatitis. Mol Med Rep 7(2):401–405
10. Chen C, Li L, Wu Z, Chen H, Fu S (2007) Effects of lactitol on intestinal microflora and plasma endotoxin in patients with chronic viral hepatitis. J Infect 54(1):98–102
11. Prendergast AJ, Klenerman P, Goulder PJ (2012) The impact of differential antiviral immunity in children and adults. Nat Rev Immunol 12(9):636–648
12. Custer B, Sullivan SD, Hazlet TK, Iloeje U, Veenstra DL, Kowdley KV (2004) Global epidemiology of hepatitis B virus. J Clin Gastroenterol 38(10 Suppl 3):S158–S168
13. Nebbia G, Peppa D, Maini MK (2012) Hepatitis B infection: current concepts and future challenges. QJM 105(2):109–113
14. Xu DZ, Yan YP, Zou S, Choi BC, Wang S, Liu P, Bai G, Wang X, Shi M, Wang X (2001) Role of placental tissues in the intrauterine transmission of hepatitis B virus. Am J Obstet Gynecol 185(4):981–987
15. Han GR, Cao MK, Zhao W, Jiang HX, Wang CM, Bai SF, Yue X, Wang GJ, Tang X, Fang ZX (2011) A prospective and open-label study for the efficacy and safety of telbivudine in pregnancy for the prevention of perinatal transmission of hepatitis B virus infection. J Hepatol 55(6):1215–1221
16. Wong F, Pai R, Van Schalkwyk J, Yoshida EM (2014) Hepatitis B in pregnancy: a concise review of neonatal vertical transmission and antiviral prophylaxis. Ann Hepatol 13(2):187–195
17. Tan AT, Koh S, Goh W, Zhe HY, Gehring AJ, Lim SG, Bertoletti A (2010) A longitudinal analysis of innate and adaptive immune profile during hepatic flares in chronic hepatitis B. J Hepatol 52(3):330–339
18. Li X, Liu X, Tian L, Chen Y (2014) Cytokine-mediated immunopathogenesis of hepatitis B virus infections. Clin Rev Allergy Immunol (in press)
19. Zhang Z, Zhang JY, Wang LF, Wang FS (2012) Immunopathogenesis and prognostic immune markers of chronic hepatitis B virus infection. J Gastroenterol Hepatol 27(2):223–230
20. Wang FS, Zhang Z (2009) Host immunity influences disease progression and antiviral efficacy in humans infected with hepatitis B virus. Expert Rev Gastroenterol Hepatol 3(5):499–512
21. Szabo G, Mandrekar P, Dolganiuc A (2007) Innate immune response and hepatic inflammation. Semin Liver Dis 27(4):339–350
22. Bertoletti A, Ferrari C (2012) Innate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection. Gut 61(12):1754–1764
23. Wu Z, Han M, Chen T, Yan W, Ning Q (2010) Acute liver failure: mechanisms of immune-mediated liver injury. Liver Int 30(6):782–794
24. Busca A, Kumar A (2014) Innate immune responses in hepatitis B virus (HBV) infection. Virol J 11:22
25. Dienstag JL (2008) Hepatitis B virus infection. N Engl J Med 359(14):1486–1500
26. Zhang E, Lu M (2015) Toll-like receptor (TLR)-mediated innate immune responses in the control of hepatitis B virus (HBV) infection. Med Microbiol Immunol 204(1):11–20
27. He D, Tao S, Guo S, Li M, Wu J, Huang H, Guo X, Yan G, Zhu P, Wang Y (2014) Interaction of TLR-IFN and HLA polymorphisms on susceptibility of chronic HBV infection in Southwest Han Chinese. Liver Int. doi:10.1111/liv.12756
28. Ma Z, Zhang E, Yang D, Lu M (2015) Contribution of Toll-like receptors to the control of hepatitis B virus infection by initiating antiviral innate responses and promoting specific adaptive immune responses. Cell Mol Immunol 12(3):273–282
29. Visvanathan K, Skinner NA, Thompson AJ, Riordan SM, Sozzi V, Edwards R, Rodgers S, Kurtovic J, Chang J, Lewin S, Desmond P, Locarnini S (2007) Regulation of Toll-like receptor-2 expression in chronic hepatitis B by the precore protein. Hepatology 45(1):102–110
30. Wang S, Chen Z, Hu C, Qian F, Cheng Y, Wu M, Shi B, Chen J, Hu Y, Yuan Z (2013) Hepatitis B virus surface antigen selectively inhibits TLR2 ligand-induced IL-12 production in monocytes/macrophages by interfering with JNK activation. J Immunol 190(10):5142–5151
31. Levy O (2007) Innate immunity of the newborn: basic mechanisms and clinical correlates. Nat Rev Immunol 7(5):379–390
32. Strunk T, Doherty D, Richmond P, Simmer K, Charles A, Levy O, Liyanage K, Smith T, Currie A, Burgner D (2009) Reduced levels of antimicrobial proteins and peptides in human cord blood plasma. Arch Dis Child Fetal Neonatal Ed 94(3):F230–F231
33. Nguyen M, Leuridan E, Zhang T, De Wit D, Willems F, Van Damme P, Goldman M, Goriely S (2010) Acquisition of adult-like TLR4 and TLR9 responses during the first year of life. PLoS One 5(4):e10407
34. Corbett NP, Blimkie D, Ho KC, Cai B, Sutherland DP, Kallos A, Crabtree J, Rein-Weston A, Lavoie PM, Turvey SE, Hawkins NR, Self SG, Wilson CB, Hajjar AM, Fortuno ES 3rd, Kollmann TR (2010) Ontogeny of Toll-like receptor mediated cytokine responses of human blood mononuclear cells. PLoS One 5(11):e15041
35. Liao SL, Yeh KW, Lai SH, Lee WI, Huang JL (2013) Maturation of Toll-like receptor 1–4 responsiveness during early life. Early Hum Dev 89(7):473–478
36. Dasari P, Zola H, Nicholson IC (2011) Expression of Toll-like receptors by neonatal leukocytes. Pediatr Allergy Immunol 22(2):221–228
37. Koumbi LJ, Papadopoulos NG, Anastassiadou V, Machaira M, Kafetzis DA, Papaevangelou V (2010) Dendritic cells in uninfected infants born to hepatitis B virus-positive mothers. Clin Vaccine Immunol 17(7):1079–1085
38. Belderbos ME, Levy O, Stalpers F, Kimpen JL, Meyaard L, Bont L (2012) Neonatal plasma polarizes TLR4-mediated cytokine responses towards low IL-12p70 and high IL-10 production via distinct factors. PLoS One 7(3):e33419
39. Ye Y, Xie X, Yu J, Zhou L, Xie H, Jiang G, Yu X, Zhang W, Wu J, Zheng S (2010) Involvement of Th17 and Th1 effector responses in patients with Hepatitis B. J Clin Immunol 30(4):546–555
40. Wu W, Li J, Chen F, Zhu H, Peng G, Chen Z (2010) Circulating Th17 cells frequency is associated with the disease progression in HBV infected patients. J Gastroenterol Hepatol 25(4):750–757
41. Chou HH, Chien WH, Wu LL, Cheng CH, Chung CH, Horng JH, Ni YH, Tseng HT, Wu D, Lu X, Wang HY, Chen PJ, Chen DS (2015) Age-related immune clearance of hepatitis B virus infection requires the establishment of gut microbiota. Proc Natl Acad Sci U S A 112(7):2175–2180
42. Wang B, Li L (2015) Who determines the outcomes of HBV exposure? Trends Microbiol 23(6):328–329
43. Spengler U, Nischalke HD, Nattermann J, Strassburg CP (2013) Between Scylla and Charybdis: the role of the human immune system in the pathogenesis of hepatitis C. World J Gastroenterol 19(44):7852–7866
44. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410(6832):1099–1103
45. Park MR, Seo JK, Kim KH (2013) Viral and nonviral elements in potexvirus replication and movement and in antiviral responses. Adv Virus Res 87:75–112
46. Isogawa M, Tanaka Y (2015) Immunobiology of hepatitis B virus infection. Hepatol Res 45(2):179–189
47. Urbani S, Boni C, Amadei B, Fisicaro P, Cerioni S, Valli MA, Missale G, Ferrari C (2005) Acute phase HBV-specific T cell responses associated with HBV persistence after HBV/HCV coinfection. Hepatology 41(4):826–831
48. Das A, Maini MK (2010) Innate and adaptive immune responses in hepatitis B virus infection. Dig Dis 28(1):126–132
49. Fisicaro P, Valdatta C, Boni C, Massari M, Mori C, Zerbini A, Orlandini A, Sacchelli L, Missale G, Ferrari C (2009) Early kinetics of innate and adaptive immune responses during hepatitis B virus infection. Gut 58(7):974–982
50. Liberal R, Grant CR, Longhi MS, Mieli-Vergani G, Vergani D (2014) Diagnostic criteria of autoimmune hepatitis. Autoimmun Rev 13(4–5):435–440
51. Georgiadou SP, Zachou K, Liaskos C, Gabeta S, Rigopoulou EI, Dalekos GN (2009) Occult hepatitis B virus infection in patients with autoimmune liver diseases. Liver Int 29(3):434–442
52. Szabo G, Bala S, Petrasek J, Gattu A (2010) Gut–liver axis and sensing microbes. Dig Dis 28(6):737–744
53. Ma HD, Wang YH, Chang C, Gershwin ME, Lian ZX (2015) The intestinal microbiota and microenvironment in liver. Autoimmun Rev 14(3):183–191
54. Miyake Y, Yamamoto K (2013) Role of gut microbiota in liver diseases. Hepatol Res 43(2):139–146
55. McGettrick AF, O’Neill LA (2010) Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr Opin Immunol 22(1):20–27
56. Xu D, Zhao M, Song Y, Song J, Huang Y, Wang J (2015) Novel insights in preventing Gram-negative bacterial infection in cirrhotic patients: review on the effects of GM-CSF in maintaining homeostasis of the immune system. Hepatol Int 9(1):28–34
57. Henao-Mejia J, Elinav E, Thaiss CA, Licona-Limon P, Flavell RA (2013) Role of the intestinal microbiome in liver disease. J Autoimmun 46:66–73
58. Schnabl B, Brenner DA (2014) Interactions between the intestinal microbiome and liver diseases. Gastroenterology 146(6):1513–1524
59. Nardone G, Compare D, Liguori E, Di Mauro V, Rocco A, Barone M, Napoli A, Lapi D, Iovene MR, Colantuoni A (2010) Protective effects of Lactobacillus paracasei F19 in a rat model of oxidative and metabolic hepatic injury. Am J Physiol Gastrointest Liver Physiol 299(3):G669–G676
60. Mazagova M, Wang L, Anfora AT, Wissmueller M, Lesley SA, Miyamoto Y, Eckmann L, Dhungana S, Pathmasiri W, Sumner S, Westwater C, Brenner DA, Schnabl B (2015) Commensal microbiota is hepatoprotective and prevents liver fibrosis in mice. FASEB J 29(3):1043–1055
61. Quigley EM, Stanton C, Murphy EF (2013) The gut microbiota and the liver. Pathophysiological and clinical implications. J Hepatol 58(5):1020–1027
62. Quigley EM, Monsour HP (2013) The gut microbiota and the liver: implications for clinical practice. Expert Rev Gastroenterol Hepatol 7(8):723–732
63. Chassaing B, Etienne-Mesmin L, Gewirtz AT (2014) Microbiota–liver axis in hepatic disease. Hepatology 59(1):328–339
64. Chen Y, Qin N, Guo J, Qian G, Fang D, Shi D, Xu M, Yang F, He Z, Van Nostrand JD, Yuan T, Deng Y, Zhou J, Li L (2014) Functional gene arrays-based analysis of fecal microbiomes in patients with liver cirrhosis. BMC Genomics 15:753
65. Sjögren YM, Jenmalm MC, Böttcher MF, Björkstén B, Sverremark-Ekström E (2009) Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy 39(4):518–526
66. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J; MetaHIT Consortium, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65
67. Rougé C, Goldenberg O, Ferraris L, Berger B, Rochat F, Legrand A, Göbel UB, Vodovar M, Voyer M, Rozé JC, Darmaun D, Piloquet H, Butel MJ, de La Cochetière MF (2010) Investigation of the intestinal microbiota in preterm infants using different methods. Anaerobe 16(4):362–370
68. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI (2011) Human nutrition, the gut microbiome and the immune system. Nature 474(7351):327–336
69. Van den Abbeele P, Grootaert C, Marzorati M, Possemiers S, Verstraete W, Gérard P, Rabot S, Bruneau A, El Aidy S, Derrien M, Zoetendal E, Kleerebezem M, Smidt H, Van de Wiele T (2010) Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. Appl Environ Microbiol 76(15):5237–5246
70. Park BS, Lee JO (2013) Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp Mol Med 45:e66
71. Zhang SY, Jouanguy E, Ugolini S, Smahi A, Elain G, Romero P, Segal D, Sancho-Shimizu V, Lorenzo L, Puel A, Picard C, Chapgier A, Plancoulaine S, Titeux M, Cognet C, von Bernuth H, Ku CL, Casrouge A, Zhang XX, Barreiro L, Leonard J, Hamilton C, Lebon P, Héron B, Vallée L, Quintana-Murci L, Hovnanian A, Rozenberg F, Vivier E, Geissmann F, Tardieu M, Abel L, Casanova JL (2007) TLR3 deficiency in patients with herpes simplex encephalitis. Science 317(5844):1522–1527
72. Chen J, Wei Y, He J, Cui G, Zhu Y, Lu C, Ding Y, Xue R, Bai L, Uede T, Li L, Diao H (2014) Natural killer T cells play a necessary role in modulating of immune-mediated liver injury by gut microbiota. Sci Rep 4:7259
73. Zou Y, Chen T, Han M, Wang H, Yan W, Song G, Wu Z, Wang X, Zhu C, Luo X, Ning Q (2010) Increased killing of liver NK cells by Fas/Fas ligand and NKG2D/NKG2D ligand contributes to hepatocyte necrosis in virus-induced liver failure. J Immunol 184(1):466–475
74. Schnabl B (2013) Linking intestinal homeostasis and liver disease. Curr Opin Gastroenterol 29(3):264–270
75. Szabo G, Petrasek J, Bala S (2012) Innate immunity and alcoholic liver disease. Dig Dis 30(Suppl 1):55–60
76. Knolle PA, Böttcher J, Huang LR (2015) The role of hepatic immune regulation in systemic immunity to viral infection. Med Microbiol Immunol 204(1):21–27
77. Maini MK, Peppa D (2013) NK cells: a double-edged sword in chronic hepatitis B virus infection. Front Immunol 4:57
78. Himanen JP, Pyhälä L, Olander RM, Merimskaya O, Kuzina T, Lysyuk O, Pronin A, Sanin A, Helander IM, Sarvas M (1993) Biological activities of lipoteichoic acid and peptidoglycan–teichoic acid of Bacillus subtilis 168 (Marburg). J Gen Microbiol 139(11):2659–2665
79. Deshmukh HS, Liu Y, Menkiti OR, Mei J, Dai N, O’Leary CE, Oliver PM, Kolls JK, Weiser JN, Worthen GS (2014) The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat Med 20(5):524–530
80. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillère R, Hannani D, Enot DP, Pfirschke C, Engblom C, Pittet MJ, Schlitzer A, Ginhoux F, Apetoh L, Chachaty E, Woerther PL, Eberl G, Bérard M, Ecobichon C, Clermont D, Bizet C, Gaboriau-Routhiau V, Cerf-Bensussan N, Opolon P, Yessaad N, Vivier E, Ryffel B, Elson CO, Doré J, Kroemer G, Lepage P, Boneca IG, Ghiringhelli F, Zitvogel L (2013) The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342(6161):971–976
81. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504(7480):446–450
82. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, Kim S, Fritz JV, Wilmes P, Ueha S, Matsushima K, Ohno H, Olle B, Sakaguchi S, Taniguchi T, Morita H, Hattori M, Honda K (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500(7461):232–236
83. Waggoner SN, Cornberg M, Selin LK, Welsh RM (2011) Natural killer cells act as rheostats modulating antiviral T cells. Nature 481(7381):394–398
84. Waggoner SN, Daniels KA, Welsh RM (2014) Therapeutic depletion of natural killer cells controls persistent infection. J Virol 88(4):1953–1960
85. Elahi S, Ertelt JM, Kinder JM, Jiang TT, Zhang X, Xin L, Chaturvedi V, Strong BS, Qualls JE, Steinbrecher KA, Kalfa TA, Shaaban AF, Way SS (2013) Immunosuppressive CD71+ erythroid cells compromise neonatal host defence against infection. Nature 504(7478):158–162
86. Yilmaz B, Portugal S, Tran TM, Gozzelino R, Ramos S, Gomes J, Regalado A, Cowan PJ, d’Apice AJ, Chong AS, Doumbo OK, Traore B, Crompton PD, Silveira H, Soares MP (2014) Gut microbiota elicits a protective immune response against malaria transmission. Cell 159(6):1277–1289
87. Ott JJ, Irving G, Wiersma ST (2012) Long-term protective effects of hepatitis A vaccines. A systematic review. Vaccine 31(1):3–11
88. Freshwater DA (2013) Hepatitis E: the forgotten virus. J R Army Med Corps 159(3):167–168
89. Chang JJ, Lewin SR (2007) Immunopathogenesis of hepatitis B virus infection. Immunol Cell Biol 85(1):16–23
90. Ubeda C, Pamer EG (2012) Antibiotics, microbiota, and immune defense. Trends Immunol 33(9):459–466