Dectin-1 Regulates Hepatic Fibrosis and Hepatocarcinogenesis by Suppressing TLR4 Signaling Pathways

Cell Reports

Volumn 13, Issue 9, 2015, Pages 1909-1921

  Seifert, Lena ^a   Deutsch, Michael ^a   Alothman, Sara ^a   Alqunaibit, Dalia ^a   Werba, Gregor ^a   Pansari, Mridul ^a   Pergamo, Matthew ^a   Ochi, Atsuo ^a   Torres Hernandez, Alejandro ^a   Levie, Elliot ^a   Tippens, Daniel ^a   Greco, Stephanie H ^a   Tiwari, Shaun ^a   Ly, Nancy Ngoc Giao ^a   Eisenthal, Andrew ^a   van Heerden, Eliza ^a   Avanzi, Antonina ^a   Barilla, Rocky ^a   Zambirinis, Constantinos P ^a   Rendon, Mauricio ^a   Daley, Donnele ^a   Pachter, H Leon ^a   Hajdu, Cristina ^a   Miller, George ^a   more..

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C type lectin receptors; Hepatocellular cancer; Liver fibrosis

Indexed keywords

CD14 ANTIGEN; COLONY STIMULATING FACTOR 1; DECTIN 1; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4; CCL2 PROTEIN, MOUSE; CYTOKINE; DIETHYLNITROSAMINE; LECTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; RECOMBINANT PROTEIN; THIOACETAMIDE; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC LIVER DISEASE; CONTROLLED STUDY; ENDOTOXEMIA; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; INNATE IMMUNITY; LIPOPOLYSACCHARIDE-INDUCED SEPSIS; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER FIBROSIS; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STELLATE CELL; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BLOOD; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; CHEMICALLY INDUCED; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENETICS; INFLAMMATION; ISOLATION AND PURIFICATION; KNOCKOUT MOUSE; LIVER; LIVER CELL; LIVER CIRRHOSIS; LIVER TUMOR; METABOLISM; PATHOLOGY; SEPSIS;

ANIMALS; ANTIGENS, CD14; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHEMOKINE CCL2; CYTOKINES; DIETHYLNITROSAMINE; HEPATOCYTES; HUMANS; INFLAMMATION; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; LIVER; LIVER CIRRHOSIS; LIVER NEOPLASMS; MACROPHAGE COLONY-STIMULATING FACTOR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT PROTEINS; SEPSIS; SIGNAL TRANSDUCTION; THIOACETAMIDE; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 84947557486     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.10.058     Document Type: Article

References (49)

1. Aoyama T., Paik Y.H., Seki E. Toll-like receptor signaling and liver fibrosis. Gastroenterol. Res. Pract. 2010, 2010:2010.
2. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
3. Bianchi M.E. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 2007, 81:1-5.
4. Connolly M.K., Bedrosian A.S., Mallen-St Clair J., Mitchell A.P., Ibrahim J., Stroud A., Pachter H.L., Bar-Sagi D., Frey A.B., Miller G. In liver fibrosis, dendritic cells govern hepatic inflammation in mice via TNF-alpha. J. Clin. Invest. 2009, 119:3213-3225.
5. Dapito D.H., Mencin A., Gwak G.Y., Pradere J.P., Jang M.K., Mederacke I., Caviglia J.M., Khiabanian H., Adeyemi A., Bataller R., et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 2012, 21:504-516.
6. De Creus A., Abe M., Lau A.H., Hackstein H., Raimondi G., Thomson A.W. Low TLR4 expression by liver dendritic cells correlates with reduced capacity to activate allogeneic T cells in response to endotoxin. J. Immunol. 2005, 174:2037-2045.
7. Del Fresno C., Soulat D., Roth S., Blazek K., Udalova I., Sancho D., Ruland J., Ardavín C. Interferon-β production via Dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 2013, 38:1176-1186.
8. El-Serag H.B. Epidemiology of hepatocellular carcinoma in USA. Hepatol. Res. 2007, 37(Suppl 2):S88-S94.
9. Ferwerda B., Ferwerda G., Plantinga T.S., Willment J.A., van Spriel A.B., Venselaar H., Elbers C.C., Johnson M.D., Cambi A., Huysamen C., et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 2009, 361:1760-1767.
10. Franceschi S., Raza S.A. Epidemiology and prevention of hepatocellular carcinoma. Cancer Lett. 2009, 286:5-8.
11. Fujimoto M., Naka T. SOCS1, a negative regulator of cytokine signals and TLR Responses, in human liver diseases. Gastroenterol. Res. Pract. 2010, 2010:2010.
12. Fujisawa K., Maesawa C., Sato R., Wada K., Ogasawara S., Akiyama Y., Takeda M., Fujita T., Otsuka K., Higuchi T., et al. Epigenetic status and aberrant expression of the maspin gene in human hepato-biliary tract carcinomas. Lab. Invest. 2005, 85:214-224.
13. Gross O., Gewies A., Finger K., Schäfer M., Sparwasser T., Peschel C., Förster I., Ruland J. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 2006, 442:651-656.
14. Hamerman J.A., Tchao N.K., Lowell C.A., Lanier L.L. Enhanced Toll-like receptor responses in the absence of signaling adaptor DAP12. Nat. Immunol. 2005, 6:579-586.
15. Hammerich L., Bangen J.M., Govaere O., Zimmermann H.W., Gassler N., Huss S., Liedtke C., Prinz I., Lira S.A., Luedde T., et al. Chemokine receptor CCR6-dependent accumulation of γδ T cells in injured liver restricts hepatic inflammation and fibrosis. Hepatology 2014, 59:630-642.
16. Han C., Jin J., Xu S., Liu H., Li N., Cao X. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 2010, 11:734-742.
17. Hsu H.C., Tseng H.J., Lai P.L., Lee P.H., Peng S.Y. Expression of p53 gene in 184 unifocal hepatocellular carcinomas: association with tumor growth and invasiveness. Cancer Res. 1993, 53:4691-4694.
18. Hu H., Li Z., Chen J., Wang D., Ma J., Wang W., Li J., Wu H., Li L., Wu M., et al. P16 reactivation induces anoikis and exhibits antitumour potency by downregulating Akt/survivin signalling in hepatocellular carcinoma cells. Gut 2011, 60:710-721.
19. Hui L., Zatloukal K., Scheuch H., Stepniak E., Wagner E.F. Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J. Clin. Invest. 2008, 118:3943-3953.
20. Ibrahim J., Nguyen A.H., Rehman A., Ochi A., Jamal M., Graffeo C.S., Henning J.R., Zambirinis C.P., Fallon N.C., Barilla R., et al. Dendritic cell populations with different concentrations of lipid regulate tolerance and immunity in mouse and human liver. Gastroenterology 2012, 143:1061-1072.
21. Kawagoe T., Takeuchi O., Takabatake Y., Kato H., Isaka Y., Tsujimura T., Akira S. TANK is a negative regulator of Toll-like receptor signaling and is critical for the prevention of autoimmune nephritis. Nat. Immunol. 2009, 10:965-972.
22. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
23. Klein I., Cornejo J.C., Polakos N.K., John B., Wuensch S.A., Topham D.J., Pierce R.H., Crispe I.N. Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages. Blood 2007, 110:4077-4085.
24. Kuramitsu K., Sverdlov D.Y., Liu S.B., Csizmadia E., Burkly L., Schuppan D., Hanto D.W., Otterbein L.E., Popov Y. Failure of fibrotic liver regeneration in mice is linked to a severe fibrogenic response driven by hepatic progenitor cell activation. Am. J. Pathol. 2013, 183:182-194.
25. Kwan W.H., Boix C., Gougelet N., Fridman W.H., Mueller C.G. LPS induces rapid IL-10 release by M-CSF-conditioned tolerogenic dendritic cell precursors. J. Leukoc. Biol. 2007, 82:133-141.
26. Li W., Liang X., Kellendonk C., Poli V., Taub R. STAT3 contributes to the mitogenic response of hepatocytes during liver regeneration. J. Biol. Chem. 2002, 277:28411-28417.
27. Lim Y.S., Kim W.R. The global impact of hepatic fibrosis and end-stage liver disease. Clin. Liver Dis. 2008, 12:733-746. vii.
28. Lu Y.C., Yeh W.C., Ohashi P.S. LPS/TLR4 signal transduction pathway. Cytokine 2008, 42:145-151.
29. Nishida N., Fukuda Y., Komeda T., Kita R., Sando T., Furukawa M., Amenomori M., Shibagaki I., Nakao K., Ikenaga M., et al. Amplification and overexpression of the cyclin D1 gene in aggressive human hepatocellular carcinoma. Cancer Res. 1994, 54:3107-3110.
30. Ochi A., Graffeo C.S., Zambirinis C.P., Rehman A., Hackman M., Fallon N., Barilla R.M., Henning J.R., Jamal M., Rao R., et al. Toll-like receptor 7 regulates pancreatic carcinogenesis in mice and humans. J. Clin. Invest. 2012, 122:4118-4129.
31. Ochi A., Nguyen A.H., Bedrosian A.S., Mushlin H.M., Zarbakhsh S., Barilla R., Zambirinis C.P., Fallon N.C., Rehman A., Pylayeva-Gupta Y., et al. MyD88 inhibition amplifies dendritic cell capacity to promote pancreatic carcinogenesis via Th2 cells. J. Exp. Med. 2012, 209:1671-1687.
32. Paik Y.H., Schwabe R.F., Bataller R., Russo M.P., Jobin C., Brenner D.A. Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology 2003, 37:1043-1055.
33. Peri F., Piazza M. Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol. Adv. 2012, 30:251-260.
34. Preisser L., Miot C., Le Guillou-Guillemette H., Beaumont E., Foucher E.D., Garo E., Blanchard S., Fremaux I., Croue A., Fouchard I., et al. IL-34 and M-CSF are overexpressed in HCV fibrosis and induce pro-fibrotic macrophages which promote collagen synthesis by hepatic stellate cells. Hepatology 2014, 60:1879-1890.
35. Rao R., Graffeo C.S., Gulati R., Jamal M., Narayan S., Zambirinis C.P., Barilla R., Deutsch M., Greco S.H., Ochi A., et al. Interleukin 17-producing gammadeltaT cells promote hepatic regeneration in mice. Gastroenterology 2014, 147:473-484.
36. Rehman A., Hemmert K.C., Ochi A., Jamal M., Henning J.R., Barilla R., Quesada J.P., Zambirinis C.P., Tang K., Ego-Osuala M., et al. Role of fatty-acid synthesis in dendritic cell generation and function. J. Immunol. 2013, 190:4640-4649.
37. Ren X., Hu B., Colletti L.M. IL-22 is involved in liver regeneration after hepatectomy. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G74-G80.
38. Saijo S., Fujikado N., Furuta T., Chung S.H., Kotaki H., Seki K., Sudo K., Akira S., Adachi Y., Ohno N., et al. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat. Immunol. 2007, 8:39-46.
39. Seki E., De Minicis S., Osterreicher C.H., Kluwe J., Osawa Y., Brenner D.A., Schwabe R.F. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat. Med. 2007, 13:1324-1332.
40. Strasser D., Neumann K., Bergmann H., Marakalala M.J., Guler R., Rojowska A., Hopfner K.P., Brombacher F., Urlaub H., Baier G., et al. Syk kinase-coupled C-type lectin receptors engage protein kinase C-σ to elicit Card9 adaptor-mediated innate immunity. Immunity 2012, 36:32-42.
41. Tsung A., Sahai R., Tanaka H., Nakao A., Fink M.P., Lotze M.T., Yang H., Li J., Tracey K.J., Geller D.A., Billiar T.R. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 2005, 201:1135-1143.
42. Vasel M., Rutz R., Bersch C., Feick P., Singer M.V., Kirschfink M., Nakchbandi I.A. Complement activation correlates with liver necrosis and fibrosis in chronic hepatitis C. Clin. Immunol. 2014, 150:149-156.
43. Vautier S., MacCallum D.M., Brown G.D. C-type lectin receptors and cytokines in fungal immunity. Cytokine 2012, 58:89-99.
44. Wang L., Gordon R.A., Huynh L., Su X., Park Min K.H., Han J., Arthur J.S., Kalliolias G.D., Ivashkiv L.B. Indirect inhibition of Toll-like receptor and type I interferon responses by ITAM-coupled receptors and integrins. Immunity 2010, 32:518-530.
45. Whetton A.D., Heyworth C.M., Nicholls S.E., Evans C.A., Lord J.M., Dexter T.M., Owen-Lynch P.J. Cytokine-mediated protein kinase C activation is a signal for lineage determination in bipotential granulocyte macrophage colony-forming cells. J. Cell Biol. 1994, 125:651-659.
46. Yee N.K., Hamerman J.A. β(2) integrins inhibit TLR responses by regulating NF-κB pathway and p38 MAPK activation. Eur. J. Immunol. 2013, 43:779-792.
47. Yoshimura A., Ohishi H.M., Aki D., Hanada T. Regulation of TLR signaling and inflammation by SOCS family proteins. J. Leukoc. Biol. 2004, 75:422-427.
48. Yuk J.M., Shin D.M., Lee H.M., Kim J.J., Kim S.W., Jin H.S., Yang C.S., Park K.A., Chanda D., Kim D.K., et al. The orphan nuclear receptor SHP acts as a negative regulator in inflammatory signaling triggered by Toll-like receptors. Nat. Immunol. 2011, 12:742-751.
49. Zanoni I., Ostuni R., Capuano G., Collini M., Caccia M., Ronchi A.E., Rocchetti M., Mingozzi F., Foti M., Chirico G., et al. CD14 regulates the dendritic cell life cycle after LPS exposure through NFAT activation. Nature 2009, 460:264-268.