Oral Ampicillin Inhibits Liver Regeneration by Breaking Hepatic Innate Immune Tolerance Normally Maintained by Gut Commensal Bacteria

Hepatology

Volumn 62, Issue 1, 2015, Pages 253-264

  Wu, Xunyao ^a   Sun, Rui ^a,b   Chen, Yongyan ^a   Zheng, Xiaodong ^a   Bai, Li ^a,b   Lian, Zhexiong ^a,b   Wei, Haiming ^a,b   Tian, Zhigang ^a,b,c  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; AMPICILLIN; ASPARTATE AMINOTRANSFERASE; CD1D ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 12 ANTIBODY; INTERLEUKIN 12P40; METRONIDAZOLE; NEOMYCIN; VANCOMYCIN; ANTIINFECTIVE AGENT;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BACTERIAL LOAD; CELL ACTIVATION; CELL PROLIFERATION; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; INTESTINE FLORA; KUPFFER CELL; LIVER CELL; LIVER FUNCTION; LIVER REGENERATION; LIVER RESECTION; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GASTROINTESTINAL TRACT; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; SYMBIOSIS;

AMPICILLIN; ANIMALS; ANTI-BACTERIAL AGENTS; GASTROINTESTINAL TRACT; IMMUNE TOLERANCE; IMMUNITY, INNATE; KUPFFER CELLS; LIVER REGENERATION; MALE; MICE, INBRED C57BL; MICROBIOTA; NATURAL KILLER T-CELLS; SYMBIOSIS;

EID: 84933182697     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27791     Document Type: Article

References (45)

1. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313-323.
2. Ganal SC, Sanos SL, Kallfass C, Oberle K, Johner C, Kirschning C, et al. Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 2012; 37: 171-186.
3. + T-cell responses to intestinal commensal bacteria. Nature 2013; 498: 113-117.
4. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA 2011; 108: 5354-5359.
5. Olszak T, An DD, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012; 336: 489-493.
6. Dong ZJ, Wei HM, Sun R, Tian ZG. The roles of innate immune cells in liver injury and regeneration. Cell Mol Immunol 2007; 4: 241-252.
7. Jenne CN, Kubes P. Immune surveillance by the liver. Nat Immunol 2013; 14: 996-1006.
8. Zhang JH, Dong ZJ, Zhou RB, Luo DM, Wei HM, Tian ZG. Isolation of lymphocytes and their innate immune characterizations from liver, intestine, lung and uterus. Cell Mol Immunol 2005; 2: 271-280.
9. Bi JC, Zhang Q, Liang D, Xiong L, Wei HM, Sun R, et al. T-cell Ig and ITIM domain regulates natural killer cell activation in murine acute viral hepatitis. HEPATOLOGY 2014; 59: 1715-1725.
10. Hou X, Zhou RB, Wei HM, Sun R, Tian ZG. NKG2D-retinoic acid early inducible-1 recognition between natural killer cells and kupffer cells in a novel murine natural killer cell-dependent fulminant hepatitis. HEPATOLOGY 2009; 49: 940-949.
11. Jin ZX, Sun R, Wei HM, Gao XA, Chen YY, Tian ZG. Accelerated liver fibrosis in hepatitis B virus transgenic mice: involvement of natural killer T cells. HEPATOLOGY 2011; 53: 219-229.
12. Xu L, Yin WW, Sun R, Wei HM, Tian ZG. Kupffer cell-derived IL-10 plays a key role in maintaining humoral immune tolerance in hepatitis B virus-persistent mice. HEPATOLOGY 2014; 59: 443-452.
13. Bi J, Zheng X, Chen Y, Wei H, Sun R, Tian Z. TIGIT safeguards liver regeneration through regulating natural killer cell-hepatocyte crosstalk. HEPATOLOGY 2014; 60: 1389-1398.
14. Sun R, Gao B. Negative regulation of liver regeneration by innate immunity (natural killer cells/interferon-gamma). Gastroenterology 2004; 127: 1525-1539.
15. Dong ZJ, Zhang JH, Sun R, Wei HM, Tian ZG. Impairment of liver regeneration correlates with activated hepatic NKT cells in HBV transgenic mice. HEPATOLOGY 2007; 45: 1400-1412.
16. Nakashima H, Inui T, Habu Y, Kinoshita M, Nagao S, Kawaguchi A, et al. Activation of mouse natural killer T cells accelerates liver regeneration after partial hepatectomy. Gastroenterology 2006; 131: 1573-1583.
17. Cornell RP. Restriction of gut-derived endotoxin impairs DNA-synthesis for liver regeneration. Am J Physiol 1985; 249: R563-R569.
18. Cornell RP, Liljequist BL, Bartizal KF. Depressed liver-regeneration after partial-hepatectomy of germ-free, athymic and lipopolysaccharide-resistance mice. HEPATOLOGY 1990; 11: 916-922.
19. Mitchell C, Willenbring H. A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat Protoc 2008; 3: 1167-1170.
20. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric salmonella infection. Infect Immun 2009; 77: 2741-2753.
21. Tumanov AV, Koroleva EP, Christiansen PA, Khan MA, Ruddy MJ, Burnette B, et al. T cell-derived lymphotoxin regulates liver regeneration. Gastroenterology 2009; 136: 694-704.
22. Duwaerts CC, Sun EP, Cheng CW, van Rooijen N, Gregory SH. Cross-activating invariant NKT cells and Kupffer cells suppress cholestatic liver injury in a mouse model of biliary obstruction. PLoS One 2013; 8.
23. Kremer M, Thomas E, Milton RJ, Perry AW, van Rooijen N, Wheeler MD, et al. Kupffer cell and interleukin-12-dependent loss of natural killer T cells in hepatosteatosis. HEPATOLOGY 2010; 51: 130-141.
24. Akita K, Okuno M, Enya M, Imai S, Moriwaki H, Kawada N, et al. Impaired liver regeneration in mice by lipopolysaccharide via tumor necrosis factor-alpha/kallikrein-mediated activation of latent TGF-beta. Gastroenterology 2002; 123: 352-364.
25. Cornell RP. Gut-derived endotoxin elicts hepatotrophic factor secretion for liver-regeneration. Am J Physiol 1985; 249: R551-R562.
26. Muhamad M. The role of lipopolysaccharide/Toll-like receptor 4 signalling pathway during liver regeneration after partial hepatectomy in mice [dissertation]. Dunedin, NZ: University of Otago; 2011.
27. Campbell JS, Riehle KJ, Brooling JT, Bauer RL, Mitchell C, Fausto N. Proinflammatory cytokine production in liver regeneration is Myd88-dependent, but independent of Cd14, Tlr2, and Tlr4. J Immunol 2006; 176: 2522-2528.
28. Godfrey DI, Hammond KJL, Poulton LD, Smyth MJ, Baxter AG. NKT cells: facts, functions and fallacies. Immunol Today 2000; 21: 573-583.
29. Godfrey DI, MacDonald HR, Kronenberg M, Smyth MJ, Van Kaer L. NKT cells: what's in a name? Nat Rev Immunol 2004; 4: 231-237.
30. Kronenberg M, Gapin L. The unconventional lifestyle of NKT cells. Nat Rev Immunol 2002; 2: 557-568.
31. Kinjo Y, Wu D, Kim GS, Xing GW, Poles MA, Ho DD, et al. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 2005; 434: 520-525.
32. Mattner J, DeBord KL, Ismail N, Goff RD, Cantu C, Zhou DP, et al. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 2005; 434: 525-529.
33. Zhou DP, Mattner J, Cantu C, Schrantz N, Yin N, Gao Y, et al. Lysosomal glycosphingolipid recognition by NKT cells. Science 2004; 306: 1786-1789.
34. + NKT cells in germ-free mice. Eur J Immunol 2000; 30: 620-625.
35. Wingender G, Stepniak D, Krebs P, Lin L, McBride S, Wei B, et al. Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice. Gastroenterology 2012; 143: 418-428.
36. + T cells shape the formation of invariant NKT cells. J Immunol 2010; 184: 1218-1226.
37. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, et al. Cutting edge: Endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface Toll-like receptor 4 expression. J Immunol 2000; 164: 3476-3479.
38. Uhrig A, Banafsche R, Kremer M, Hegenbarth S, Hamann A, Neurath M, et al. Development and functional consequences of LIPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 2005; 77: 626-633.
39. Zieglerheitbrock HWL. Molecular mechanism in tolerance to lipopolysaccharide. J Inflamm 1995; 45: 13-26.
40. Gkouskou KK, Deligianni C, Tsatsanis C, Eliopoulos AG. The gut microbiota in mouse models of inflammatory bowel disease. Front Cell Infect Microbiol 2014; 4: 28.
41. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8: 958-969.
42. 2. Cell Host Microbe 2014; 15: 95-102.
43. Lynch L, Nowak M, Varghese B, Clark J, Hogan AE, Toxavidis V, et al. Adipose tissue invariant NKT cells protect against diet-induced obesity and metabolic disorder through regulatory cytokine production. Immunity 2012; 37: 574-587.
44. Wang J, Li FQ, Sun R, Gao X, Wei HM, Li LJ, et al. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat Commun 2013; 4: 2106.
45. Corbitt N, Kimura S, Isse K, Specht S, Chedwick L, Rosborough BR, et al. 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 2013; 182: 180-191.