Toll-Like Receptor 8 Agonist and Bacteria Trigger Potent Activation of Innate Immune Cells in Human Liver

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Jo, Juandy ^a,h   Tan, Anthony T ^b   Ussher, James E ^c,i   Sandalova, Elena ^a,h   Tang, Xin Zi ^a   Tan Garcia, Alfonso ^b   To, Natalie ^d   Hong, Michelle ^a   Chia, Adeline ^b   Gill, Upkar S ^d   Kennedy, Patrick T ^d   Tan, Kai Chah ^e   Lee, Kang Hoe ^e   De Libero, Gennaro ^f   Gehring, Adam J ^a,j   Willberg, Christian B ^c   Klenerman, Paul ^c   Bertoletti, Antonio ^a,b,g  

^a AGENCY FOR SCIENCE   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e Asian American Liver Centre   (Singapore)

^f UNIVERSITY HOSPITAL BASEL   (Switzerland)

^g UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^h Danone Research Centre for Specialised Nutrition   (Singapore)

ⁱ UNIVERSITY OF OTAGO   (New Zealand)

^j SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTERFERON; CD161 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; IONOMYCIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PHORBOL 13 ACETATE 12 MYRISTATE; RIBOFLAVIN; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 8 AGONIST; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; IMMUNOLOGICAL ADJUVANT; OLIGORIBONUCLEOTIDE; TLR8 PROTEIN, HUMAN;

ARTICLE; BACTERIAL INFECTION; CELL ACTIVATION; CELL STIMULATION; CELLULAR IMMUNITY; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; DEPLETION; ENTEROCOCCUS FAECALIS; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HEPATITIS B; HEPATITIS C; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LIVER BIOPSY; LIVER CELL; MONOCYTE; MONONUCLEAR CELL; NATURAL KILLER CELL; NONHUMAN; PSEUDOMONAS AERUGINOSA; AGONISTS; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; DRUG EFFECTS; HEPACIVIRUS; HEPATITIS B VIRUS; IMMUNOLOGY; INTERFERON GAMMA RELEASE ASSAY; LIVER; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; VIROLOGY;

ADJUVANTS, IMMUNOLOGIC; CELLS, CULTURED; COCULTURE TECHNIQUES; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HEPACIVIRUS; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HUMANS; IMMUNITY, INNATE; INTERFERON-GAMMA RELEASE TESTS; KILLER CELLS, NATURAL; LEUKOCYTES, MONONUCLEAR; LIVER; MONOCYTES; OLIGORIBONUCLEOTIDES; PSEUDOMONAS AERUGINOSA; RIBOFLAVIN; T-LYMPHOCYTE SUBSETS; TOLL-LIKE RECEPTOR 8; UP-REGULATION;

EID: 84903482908     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004210     Document Type: Article

References (37)

1. Protzer U, Maini MK, Knolle PA, (2012) Living in the liver: hepatic infections. Nat Rev Immunol 12: 201-213.
2. Raz E, (2007) Organ-specific regulation of innate immunity. Nat Immunol 8: 3-4.
3. Crispe IN, (2009) The liver as a lymphoid organ. Annu Rev Immunol 27: 147-163.
4. Chisari FV, Nakamura M, Milich DR, Han K, Molden D, et al. (1985) Production of two distinct and independent hepatic immunoregulatory molecules by the perfused rat liver. Hepatology 5: 735-743.
5. Lee WY, Moriarty TJ, Wong CH, Zhou H, Strieter RM, et al. (2010) An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol 11: 295-302.
6. Tu Z, Bozorgzadeh A, Pierce RH, Kurtis J, Crispe IN, et al. (2008) TLR-dependent cross talk between human Kupffer cells and NK cells. J Exp Med 205: 233-244.
7. Treiner E, Lantz O, (2006) CD1d- and MR1-restricted invariant T cells: of mice and men. Curr Opin Immunol 18: 519-526.
8. Tang XZ, Jo J, Tan AT, Sandalova E, Chia A, et al. (2013) IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J Immunol 190: 3142-3152.
9. Blasius AL, Beutler B, (2010) Intracellular toll-like receptors. Immunity 32: 305-315.
10. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
11. Kjer-Nielsen L, Patel O, Corbett AJ, Le Nours J, Meehan B, et al. (2012) MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491: 717-723.
12. Chua WJ, Truscott SM, Eickhoff CS, Blazevic A, Hoft DF, et al. (2012) Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect Immun 80: 3256-3267.
13. Ussher JE, Bilton M, Attwod E, Shadwell J, Richardson R, et al. (2014) CD161(++) CD8(+) T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur J Immunol 44: 195-203.
14. Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, et al. (2010) Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33: 375-386.
15. Cavanaugh VJ, Guidotti LG, Chisari FV, (1997) Interleukin-12 inhibits hepatitis B virus replication in transgenic mice. J Virol 71: 3236-3243.
16. Kimura K, Kakimi K, Wieland S, Guidotti LG, Chisari FV, (2002) Interleukin-18 inhibits hepatitis B virus replication in the livers of transgenic mice. J Virol 76: 10702-10707.
17. Lau DT, Negash A, Chen J, Crochet N, Sinha M, et al. (2013) Innate immune tolerance and the role of kupffer cells in differential responses to interferon therapy among patients with HCV genotype 1 infection. Gastroenterology 144: 402-e412, 402-413, e412.
18. Lanford RE, Guerra B, Chavez D, Giavedoni L, Hodara VL, et al. (2013) GS-9620, an Oral Agonist of Toll-Like Receptor-7, Induces Prolonged Suppression of Hepatitis B Virus in Chronically Infected Chimpanzees. Gastroenterology 144: 1508-e1510, 1508-1517, e1510.
19. Liaskou E, Zimmermann HW, Li KK, Oo YH, Suresh S, et al. (2013) Monocyte subsets in human liver disease show distinct phenotypic and functional characteristics. Hepatology 57: 385-398.
20. Peppa D, Micco L, Javaid A, Kennedy PT, Schurich A, et al. (2010) Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog 6: e1001227.
21. Cervantes JL, Dunham-Ems SM, La Vake CJ, Petzke MM, Sahay B, et al. (2011) Phagosomal signaling by Borrelia burgdorferi in human monocytes involves Toll-like receptor (TLR) 2 and TLR8 cooperativity and TLR8-mediated induction of IFN-beta. Proc Natl Acad Sci U S A 108: 3683-3688.
22. Gantier MP, Irving AT, Kaparakis-Liaskos M, Xu D, Evans VA, et al. (2010) Genetic modulation of TLR8 response following bacterial phagocytosis. Hum Mutat 31: 1069-1079.
23. Kariko K, Buckstein M, Ni H, Weissman D, (2005) Suppression of RNA recognition by Toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA. Immunity 23: 165-175.
24. Sander LE, Davis MJ, Boekschoten MV, Amsen D, Dascher CC, et al. (2011) Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474: 385-389.
25. Le Bourhis L, Martin E, Peguillet I, Guihot A, Froux N, et al. (2010) Antimicrobial activity of mucosal-associated invariant T cells. Nat Immunol 11: 701-708.
26. Horsmans Y, Berg T, Desager JP, Mueller T, Schott E, et al. (2005) Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection. Hepatology 42: 724-731.
27. Lee J, Wu CC, Lee KJ, Chuang TH, Katakura K, et al. (2006) Activation of anti-hepatitis C virus responses via Toll-like receptor 7. Proc Natl Acad Sci U S A 103: 1828-1833.
28. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C, (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
29. Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R, et al. (1999) Viral clearance without destruction of infected cells during acute HBV infection. Science 284: 825-829.
30. Guidotti LG, Ishikawa T, Hobbs MV, Matzke B, Schreiber R, et al. (1996) Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4: 25-36.
31. Fosdick A, Zheng J, Pflanz S, Frey CR, Hesselgesser J, et al. (2014) Pharmacokinetic and Pharmacodynamic Properties of GS-9620, a Novel Toll-Like Receptor 7 Agonist, Demonstrate Interferon-Stimulated Gene Induction without Detectable Serum Interferon at Low Oral Doses. J Pharmacol Exp Ther 348: 96-105.
32. Schurich A, Pallett LJ, Lubowiecki M, Singh HD, Gill US, et al. (2013) The third signal cytokine IL-12 rescues the anti-viral function of exhausted HBV-specific CD8 T cells. PLoS Pathog 9: e1003208.
33. Lan P, Zhang C, Han Q, Zhang J, Tian Z, (2013) Therapeutic recovery of hepatitis B virus (HBV)-induced hepatocyte-intrinsic immune defect reverses systemic adaptive immune tolerance. Hepatology 58: 73-85.
34. Tan AT, Koh S, Goh W, Zhe HY, Gehring AJ, et al. (2010) A longitudinal analysis of innate and adaptive immune profile during hepatic flares in chronic hepatitis B. J Hepatol 52: 330-339.
35. Schenkel JM, Fraser KA, Vezys V, Masopust D, (2013) Sensing and alarm function of resident memory CD8(+) T cells. Nat Immunol 14: 509-513.
36. Kakimi K, Lane TE, Wieland S, Asensio VC, Campbell IL, et al. (2001) Blocking chemokine responsive to gamma-2/interferon (IFN)-gamma inducible protein and monokine induced by IFN-gamma activity in vivo reduces the pathogenetic but not the antiviral potential of hepatitis B virus-specific cytotoxic T lymphocytes. J Exp Med 194: 1755-1766.
37. Tumas DB, Zheng X, Rhodes G, Duatschek P, Hesselgesser J, et al. (2011) Preclinical characterization of GS-9620, a potent and selective oral TLR7 agonist. J Hepatol 56: S180.