Natural killer cell-dependent anti-fibrotic pathway in liver injury via toll-like receptor-9

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Abu Tair, Lina ^a   Axelrod, Jonathan H ^a   Doron, Sarit ^a   Ovadya, Yossi ^b   Krizhanovsky, Valery ^b   Galun, Eithan ^a   Amer, Johnny ^a   Safadi, Rifaat ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; CPG OLIGODEOXYNUCLEOTIDE; TOLL LIKE RECEPTOR 9;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG MECHANISM; IN VITRO STUDY; IN VIVO STUDY; LIVER FIBROSIS; LIVER INJURY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; SENESCENCE; STELLATE CELL; WILD TYPE;

ADJUVANTS, IMMUNOLOGIC; ADOPTIVE TRANSFER; ANIMALS; CARBON TETRACHLORIDE POISONING; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; HEPATIC STELLATE CELLS; KILLER CELLS, NATURAL; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; OLIGODEOXYRIBONUCLEOTIDES; TOLL-LIKE RECEPTOR 9;

EID: 84892394789     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082571     Document Type: Article

References (38)

1. Rosenstiel P (2013) Stories of love and hate: innate immunity and hostmicrobe crosstalk in the intestine. Curr Opin Gastroenterol 29(2): 125-132. doi:10.1097/MOG.0b013e32835da2c7. PubMed: 23337934.
2. Aoyama T, Paik YH, Seki E (2010) Toll-like receptor signaling and liver fibrosis. Gastroenterol. Res Pract 1: 1-8.
3. Paik YH, Schwabe RF, Bataller R, Russo MP, Jobin C et al. (2003) Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 37: 1043-1055. doi:10.1053/jhep.2003.50182. PubMed: 12717385.
4. Lichtenegger FS, Mueller K, Otte B, Beck B, Hiddemann W et al. (2012) CD86 and IL-12p70 Are Key Players for T Helper 1 Polarization and Natural Killer Cell Activation by Toll-Like Receptor-Induced Dendritic Cells. PLOS ONE 9: e44266.
5. Latz E, Schoenemeyer A, Visintin A, Fitzgerald KA, Monks BG et al. (2004) TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol 5(2): 190-198. doi:10.1038/ni1028. PubMed: 14716310.
6. Takeda K, Akira S (2005) Toll-like receptors in innate immunity. Int Immunol 17 (1): 1-14. PubMed: 15585605.
7. Guicciardi ME, Gores GJ (2010) Apoptosis as a mechanism for liver disease progression. Semin Liver Dis 30(4): 402-410. doi:10.1055/s-0030-1267540. PubMed: 20960379.
8. Watanabe A, Hashmi A, Gomes DA, Town T, Badou A et al. (2007) Apoptotic hepatocyte DNA inhibits hepatic stellate cell chemotaxis via toll-like receptor 9. Hepatology 46(5): 1509-1518. doi:10.1002/hep.21867. PubMed: 17705260.
9. Gäbele E, Mühlbauer M, Dorn C, Weiss TS, Froh M et al. (2008) Role of TLR9 in hepatic stellate cells and experimental liver fibrosis. Biochem Biophys Res Commun 376(2): 271-276. doi:10.1016/j.bbrc.2008.08.096. PubMed: 18760996.
10. Merlo A, Calcaterra C, Mènard S, Balsari A (2007) Cross-talk between toll-like receptors 5 and 9 on activation of human immune responses. J Leukoc Biol 82: 509-518. doi:10.1189/jlb.0207100. PubMed: 17586660.
11. Girart MV, Fuertes MB, Domaica CI, Rossi LE, Zwirner NW (2007) Engagement of TLR3, TLR7, and NKG2D regulate IFN-gamma secretion but not NKG2D-mediated cytotoxicity by human NK cells stimulated with suboptimal doses of IL-12. J Immunol 179: 3472-3479. PubMed: 17804388.
12. Ballas ZK (2007) Modulation of NK cell activity by CpG oligodeoxynucleotides. Immunol Res 39: 15-21. doi:10.1007/s12026-007-0066-3. PubMed: 17917052.
13. Krieg AM (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5(6): 471-784. doi:10.1038/nrd2059. PubMed: 16763660.
14. Melhem A, Muhanna N, Bishara A, Alvarez CE, Ilan Y et al. (2006) Anti-fibrotic activity of NK cells in experimental liver injury through killing of activated HSC. J Hepatol 45(1): 60-71. doi:10.1016/j.jhep.2005.12.025. PubMed: 16515819.
15. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J et al. (2008) Senescence of activated stellate cells limits liver fibrosis. Cell 134(4): 657-667. doi:10.1016/j.cell.2008.06.049. PubMed: 18724938.
16. Muhanna N, Abu Tair L, Doron S, Amer J, Azzeh M et al. (2011) Amelioration of hepatic fibrosis by NK cell activation. Gut 60: 90-98. doi:10.1136/gut.2011.239301.186. PubMed: 20660699.
17. Takeda K, Akira S (2004) TLR signaling pathways. Semin Immunol 16: 3-9. doi:10.1016/j.smim.2003.10.003. PubMed: 14751757.
18. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21: 335-376. doi:10.1146/annurev.immunol. 21.120601.141126. PubMed: 12524386.
19. Arad U, Zeira E, El-Latif MA, Mukherjee S, Mitchell L et al. (2005) Liver-targeted gene therapy by SV40-based vectors using the hydrodynamic injection method. Hum Gene Ther 16: 361-371. doi:10.1089/hum.2005.16.361. PubMed: 15812231.
20. Miranda SR, Erlich S, Visser JW, Gatt A, Dagan VL, et al. (1997) Bone marrow transplantation in acid sphingomyelinase-deficient mice: engraftment and cell migration into the brain as a function of radiation, age, and phenotype. Blood 90: 444-452.
21. Avraham Y, Amer J, Doron S, Abu-Tair L, Mahamid M, et al. (2012) The direct profibrotic and indirect immune antifibrotic balance of blocking the cannabinoid 2 receptor. Am J Physiol Gastrointest Liver Physiol 302 (12): G1364-G72.
22. Horani A, Muhanna N, Pappo O, Melhem A, Alvarez CE et al. (2007) Beneficial effect of glatiramer acetate (Copaxone) on immune modulation of experimental hepatic fibrosis. Am J Physiol Gastrointest Liver Physiol 292(2): G628-G638. PubMed: 17038628.
23. Muhanna N, Doron S, Wald O, Horani A, Eid A et al. (2008) Activation of hepatic stellate cells following phagocytosis of lymphocytes: a novel pathway of fibrogenesis. Hepatology 48: 963-977. doi:10.1002/hep.22413. PubMed: 18726940.
24. Sagiv A, Biran A, Yon M, Simon J, Lowe SW et al. (2013) Granule exocytosis mediates immune surveillance of senescent cells. Oncogene, 32: 1-7. PubMed: 22751116.
25. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602. doi:10.1016/ S0092-8674(00)81902-9. PubMed: 9054499.
26. Graubardt N, Fahrner R, Trochsler M, Keogh A, Breu K et al. (2012) Promotion of liver regeneration by natural killer cells in mice is dependent on extracellular ATP phosphohydrolysis. Hepatology 2: 1-11.
27. Li Q, Yan Z, Li F, Lu W, Wang J et al. (2012) The improving effects on hepatic fibrosis of interferon-γ liposomes targeted to hepatic stellate cells. Nanotechnology 23(26): 1-10. PubMed: 22700686.
28. Gao B (2010) Innate Immunity and Steatohepatitis: A Critical Role of another Toll (TLR-9). Gastroenterology 139(1): 27-30. doi:10.1053/j.gastro.2010. 05.018. PubMed: 20639084.
29. Seki E, Brenner DA (2008) Toll-like receptors and adaptor molecules in liver disease: update. Hepatology 48: 322-335. doi:10.1002/hep.22306. PubMed: 18506843.
30. Miura K, Kodama Y, Inokuchi S, Schnabl B, Aoyama T et al. (2010) Toll-like receptor 9 promotes steatohepatitis by induction of interleukin-1β in mice. Gastroenterology 139: 323-334. doi:10.1053/j. gastro.2010.03.052. PubMed: 20347818.
31. Bamboat ZM, Balachandran VP, Ocuin LM, Obaid H, Plitas G et al. (2010) Toll-like receptor 9 inhibition confers protection from liver ischemia-reperfusion injury. Hepatology 51: 621-632. doi:10.1002/hep.23365. PubMed: 19902481.
32. Marcenaro E, Carlomagno S, Pesce S, Moretta A, Sivori S (2011) Bridging innate NK cell functions with adaptive immunity. Adv Exp Med Biol 780: 45-55. PubMed: 21842364.
33. Jiang W, Sun R, Zhou R, Wei H, Tian Z (2009) TLR-9 activation aggravates concanavalin A-induced hepatitis via promoting accumulation and activation of liver CD4+ NKT cells. J Immunol 182: 3768-3774. doi:10.4049/jimmunol.0800973. PubMed: 19265155.
34. Krieg AM (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5(6): 471-484. doi:10.1038/nrd2059. PubMed: 16763660.
35. Sugauchi F, Wang RY, Qiu Q, Jin B, Alter HJ et al. (2006) Vigorous hepatitis C virus-specific CD4+ and CD8+ T cell responses induced by protein immunization in the presence of Montanide ISA720 plus synthetic oligodeoxynucleotides containing immunostimulatory cytosine-guanine dinucleotide motifs. J Infect Dis 193: 563-572. doi:10.1086/499823. PubMed: 16425136.
36. Kamar N, Rostaing L, Sandres-Saune K, Selves J, Barthe C et al. (2005) Intrahepatic cytokine profile in renal-transplant patients infected by hepatitis C virus. J Med Virol 76: 482-488. doi:10.1002/jmv.20387. PubMed: 15977245.
37. Gur C, Doron S, Kfir-Erenfeld S, Horwitz E, Abu-Tair L et al. (2012) NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut 61(6): 885-893. doi:10.1136/gutjnl-2011-301400. PubMed: 22198715.
38. Guillerey C, Mouriès J, Polo G, Doyen N, Law HK et al. (2012) Pivotal role of plasmacytoid dendritic cells in inflammation and NK-cell responses after TLR9 triggering in mice. Blood 120(1): 90-99. doi:10.1182/blood-2012-02-410936. PubMed: 22611152.