TLR3/4 signaling is mediated via the NFκB-CXCR4/7 pathway in human alcoholic hepatitis and non-alcoholic steatohepatitis which formed Mallory-Denk bodies

Experimental and Molecular Pathology

Volumn 97, Issue 2, 2014, Pages 234-240

  Liu, Hui ^a   Li, Jun ^a   Tillman, Brittany ^a   Morgan, Timothy R ^b   French, Barbara A ^a   French, Samuel W ^a  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b VA LONG BEACH HEALTHCARE SYSTEM   (United States)

Author keywords

Chemokine receptor 4 and 7 (CXCR4 7); Liver disease development; Mallory Denk bodies (MDBs); MyD88 dependent pathway; Toll like receptor (TLR) signaling

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ALCOHOL LIVER DISEASE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; LIVER BIOPSY; MALLORY BODY; NONALCOHOLIC FATTY LIVER; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

CHEMOKINE RECEPTOR 4 AND 7 (CXCR4/7); LIVER DISEASE DEVELOPMENT; MALLORY-DENK BODIES (MDBS); MYD88-DEPENDENT PATHWAY; TOLL-LIKE RECEPTOR (TLR) SIGNALING;

CASE-CONTROL STUDIES; FATTY LIVER; HEPATITIS, ALCOHOLIC; HEPATOCYTES; HUMANS; INTERFERON REGULATORY FACTOR-7; MALLORY BODIES; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; RECEPTORS, CXCR; RECEPTORS, CXCR4; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 84905859549     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2014.07.001     Document Type: Article

References (56)

1. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511.
2. Bardag-Gorce F., Oliva J., Lin A., Li J., French B.A., French S.W. SAMe prevents the up regulation of toll-like receptor signaling in Mallory-Denk body forming hepatocytes. Exp. Mol. Pathol. 2010, 88:376-379.
3. Basaranoglu M., Turhan N., Sonsuz A., Basaranoglu G. Mallory-Denk bodies in chronic hepatitis. World J. Gastroenterol. 2011, 17:2172-2177.
4. Brechot C., Nalpas B., Feitelson M.A. Interactions between alcohol and hepatitis viruses in the liver. Clin. Lab. Med. 1996, 16:273-287.
5. Burger J.A., Peled A. CXCR4 antagonists: targeting the microenvironment in leukemia and other cancers. Leukemia 2009, 23:43-52.
6. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., Penfold M.E., Sunshine M.J., Littman D.R., Kuo C.J., Wei K., McMaster B.E., Wright K., Howard M.C., Schall T.J. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 2006, 203:2201-2213.
7. Burroughs A., McNamara D. Liver disease in Europe. Aliment. Pharmacol. Ther. 2003, 18(Suppl. 3):54-59.
8. Caldwell S., Ikura Y., Dias D., Isomoto K., Yabu A., Moskaluk C., Pramoonjago P., Simmons W., Scruggs H., Rosenbaum N., Wilkinson T., Toms P., Argo C.K., Al-Osaimi A.M., Redick J.A. Hepatocellular ballooning in NASH. J. Hepatol. 2010, 53:719-723.
9. Chen C.L., Tsukamoto H., Liu J.C., Kashiwabara C., Feldman D., Sher L., Dooley S., French S.W., Mishra L., Petrovic L., Jeong J.H., Machida K. Reciprocal regulation by TLR4 and TGF-beta in tumor-initiating stem-like cells. J. Clin. Invest. 2013, 123:2832-2849.
10. Csak T., Dolganiuc A., Kodys K., Nath B., Petrasek J., Bala S., Lippai D., Szabo G. Mitochondrial antiviral signaling protein defect links impaired antiviral response and liver injury in steatohepatitis in mice. Hepatology 2011, 53:1917-1931.
11. Csak T., Ganz M., Pespisa J., Kodys K., Dolganiuc A., Szabo G. Fatty acid and endotoxin activate inflammasomes in mouse hepatocytes that release danger signals to stimulate immune cells. Hepatology 2011, 54:133-144.
12. French S.W., Bardag-Gorce F., Li J., French B.A., Oliva J. Mallory-Denk body pathogenesis revisited. World J. Hepatol. 2010, 2:295-301.
13. French S.W., Bardag-Gorce F., French B.A., Li J., Oliva J. The role of innate immunity in the pathogenesis of preneoplasia in drug-induced chronic hepatitis based on a mouse model. Exp. Mol. Pathol. 2011, 91:653-659.
14. French S.W., Lee J., Zhong J., Morgan T.R., Buslon V., Lungo W., French B.A. Alcoholic liver disease - hepatocellular carcinoma transformation. J. Gastrointest. Oncol. 2012, 3:174-181.
15. Ganz M., Szabo G. Immune and inflammatory pathways in NASH. Hepatol. Int. 2013, 7:771-781.
16. Gao Y., Theng S.S., Zhuo J., Teo W.B., Ren J., Lee C.G. FAT10, an ubiquitin-like protein, confers malignant properties in non-tumorigenic and tumorigenic cells. Carcinogenesis 2014, 35:923-934.
17. Hattermann K., Held-Feindt J., Lucius R., Muerkoster S.S., Penfold M.E., Schall T.J., Mentlein R. The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res. 2010, 70:3299-3308.
18. Haybaeck J., Stumptner C., Thueringer A., Kolbe T., Magin T.M., Hesse M., Fickert P., Tsybrovskyy O., Muller H., Trauner M., Zatloukal K., Denk H. Genetic background effects of keratin 8 and 18 in a DDC-induced hepatotoxicity and Mallory-Denk body formation mouse model. Lab. Invest. 2012, 92:857-867.
19. Heintges T., Wands J.R. Hepatitis C virus: epidemiology and transmission. Hepatology 1997, 26:521-526.
20. Hritz I., Mandrekar P., Velayudham A., Catalano D., Dolganiuc A., Kodys K., Kurt-Jones E., Szabo G. The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 2008, 48:1224-1231.
21. Huang C.Y., Lee C.Y., Chen M.Y., Yang W.H., Chen Y.H., Chang C.H., Hsu H.C., Fong Y.C., Tang C.H. Stromal cell-derived factor-1/CXCR4 enhanced motility of human osteosarcoma cells involves MEK1/2, ERK and NF-kappaB-dependent pathways. J. Cell. Physiol. 2009, 221:204-212.
22. Isogawa M., Robek M.D., Furuichi Y., Chisari F.V. Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J. Virol. 2005, 79:7269-7272.
23. Kaifi J.T., Yekebas E.F., Schurr P., Obonyo D., Wachowiak R., Busch P., Heinecke A., Pantel K., Izbicki J.R. Tumor-cell homing to lymph nodes and bone marrow and CXCR4 expression in esophageal cancer. J. Natl. Cancer Inst. 2005, 97:1840-1847.
24. Khachatoorian R., Dawson D., Maloney E.M., Wang J., French B.A., French S.W. SAMe treatment prevents the ethanol-induced epigenetic alterations of genes in the Toll-like receptor pathway. Exp. Mol. Pathol. 2013, 94:243-246.
25. Lee C.G., Ren J., Cheong I.S., Ban K.H., Ooi L.L., Yong Tan S., Kan A., Nuchprayoon I., Jin R., Lee K.H., Choti M., Lee L.A. Expression of the FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene 2003, 22:2592-2603.
26. Lee J., French B., Morgan T., French S.W. The liver is populated by a broad spectrum of markers for macrophages. In alcoholic hepatitis the macrophages are M1 and M2. Exp. Mol. Pathol. 2014, 96:118-125.
27. Liu H., Li J., Tillman B., French B.A., French S.W. Ufmylation and FATylation pathways are downregulated in human alcoholic and nonalcoholic steatohepatitis, and mice fed DDC, where Mallory-Denk bodies (MDBs) form. Exp. Mol. Pathol. 2014, 97:81-88.
28. Lukasiak S., Schiller C., Oehlschlaeger P., Schmidtke G., Krause P., Legler D.F., Autschbach F., Schirmacher P., Breuhahn K., Groettrup M. Proinflammatory cytokines cause FAT10 upregulation in cancers of liver and colon. Oncogene 2008, 27:6068-6074.
29. Machida K., Tsukamoto H., Mkrtchyan H., Duan L., Dynnyk A., Liu H.M., Asahina K., Govindarajan S., Ray R., Ou J.H., Seki E., Deshaies R., Miyake K., Lai M.M. Toll-like receptor 4 mediates synergism between alcohol and HCV in hepatic oncogenesis involving stem cell marker Nanog. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1548-1553.
30. Machida K., Chen C.L., Liu J.C., Kashiwabara C., Feldman D., French S.W., Sher L., Hyeongnam J.J., Tsukamoto H. Cancer stem cells generated by alcohol, diabetes, and hepatitis C virus. J. Gastroenterol. Hepatol. 2012, 27(Suppl. 2):19-22.
31. Mandal P., Roychowdhury S., Park P.H., Pratt B.T., Roger T., Nagy L.E. Adiponectin and heme oxygenase-1 suppress TLR4/MyD88-independent signaling in rat Kupffer cells and in mice after chronic ethanol exposure. J. Immunol. 2010, 185:4928-4937.
32. Marechal R., Demetter P., Nagy N., Berton A., Decaestecker C., Polus M., Closset J., Deviere J., Salmon I., Van Laethem J.L. High expression of CXCR4 may predict poor survival in resected pancreatic adenocarcinoma. Br. J. Cancer 2009, 100:1444-1451.
33. Miao Z., Luker K.E., Summers B.C., Berahovich R., Bhojani M.S., Rehemtulla A., Kleer C.G., Essner J.J., Nasevicius A., Luker G.D., Howard M.C., Schall T.J. CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:15735-15740.
34. Minino A.M., Heron M.P., Murphy S.L., Kochanek K.D. Deaths: final data for 2004. Natl. Vital Stat. Rep. 2007, 55:1-119.
35. Nan L., Wu Y., Bardag-Gorce F., Li J., French B.A., Wilson L.T., French S.W. The p105/50 NF-kappaB pathway is essential for Mallory body formation. Exp. Mol. Pathol. 2005, 78:198-206.
36. Nan L., Dedes J., French B.A., Bardag-Gorce F., Li J., Wu Y., French S.W. Mallory body (cytokeratin aggresomes) formation is prevented in vitro by p38 inhibitor. Exp. Mol. Pathol. 2006, 80:228-240.
37. Oliva J., Bardag-Gorce F., French B.A., Li J., McPhaul L., Amidi F., Dedes J., Habibi A., Nguyen S., French S.W. Fat10 is an epigenetic marker for liver preneoplasia in a drug-primed mouse model of tumorigenesis. Exp. Mol. Pathol. 2008, 84:102-112.
38. Oliva J., Bardag-Gorce F., Lin A., French B.A., French S.W. The role of cytokines in UbD promoter regulation and Mallory-Denk body-like aggresomes. Exp. Mol. Pathol. 2010, 89:1-8.
39. Petrasek J., Csak T., Ganz M., Szabo G. Differences in innate immune signaling between alcoholic and non-alcoholic steatohepatitis. J. Gastroenterol. Hepatol. 2013, 28(Suppl. 1):93-98.
40. Petrasek J., Iracheta-Vellve A., Csak T., Satishchandran A., Kodys K., Kurt-Jones E.A., Fitzgerald K.A., Szabo G. STING-IRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:16544-16549.
41. Qing X., French B.A., Oliva J., French S.W. Increased expression of FAT10 in colon benign, premalignant and malignant epithelial neoplasms. Exp. Mol. Pathol. 2011, 90:51-54.
42. Ren J., Wang Y., Gao Y., Mehta S.B., Lee C.G. FAT10 mediates the effect of TNF-alpha in inducing chromosomal instability. J. Cell Sci. 2011, 124:3665-3675.
43. Roh Y.S., Seki E. Toll-like receptors in alcoholic liver disease, non-alcoholic steatohepatitis and carcinogenesis. J. Gastroenterol. Hepatol. 2013, 28(Suppl. 1):38-42.
44. Schimanski C.C., Schwald S., Simiantonaki N., Jayasinghe C., Gonner U., Wilsberg V., Junginger T., Berger M.R., Galle P.R., Moehler M. Effect of chemokine receptors CXCR4 and CCR7 on the metastatic behavior of human colorectal cancer. Clin. Cancer Res. 2005, 11:1743-1750.
45. Seki E., Brenner D.A. Toll-like receptors and adaptor molecules in liver disease: update. Hepatology 2008, 48:322-335.
46. Seki E., Park E., Fujimoto J. Toll-like receptor signaling in liver regeneration, fibrosis and carcinogenesis. Hepatol. Res. 2011, 41:597-610.
47. Sierro F., Biben C., Martinez-Munoz L., Mellado M., Ransohoff R.M., Li M., Woehl B., Leung H., Groom J., Batten M., Harvey R.P., Martinez A.C., Mackay C.R., Mackay F. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14759-14764.
48. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
49. Tarnowski M., Grymula K., Reca R., Jankowski K., Maksym R., Tarnowska J., Przybylski G., Barr F.G., Kucia M., Ratajczak M.Z. Regulation of expression of stromal-derived factor-1 receptors: CXCR4 and CXCR7 in human rhabdomyosarcomas. Mol. Cancer Res. 2010, 8:1-14.
50. Vandercappellen J., Van Damme J., Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett. 2008, 267:226-244.
51. Wang J., Shiozawa Y., Wang Y., Jung Y., Pienta K.J., Mehra R., Loberg R., Taichman R.S. The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J. Biol. Chem. 2008, 283:4283-4294.
52. Wang B., Trippler M., Pei R., Lu M., Broering R., Gerken G., Schlaak J.F. Toll-like receptor activated human and murine hepatic stellate cells are potent regulators of hepatitis C virus replication. J. Hepatol. 2009, 51:1037-1045.
53. Yuan Q.X., Nagao Y., French B.A., Wan Y.J., French S.W. Dexamethasone enhances Mallory body formation in drug-primed mouse liver. Exp. Mol. Pathol. 2000, 69:202-210.
54. Zatloukal K., French S.W., Stumptner C., Strnad P., Harada M., Toivola D.M., Cadrin M., Omary M.B. From Mallory to Mallory-Denk bodies: what, how and why?. Exp. Cell Res. 2007, 313:2033-2049.
55. Zhang D.W., Jeang K.T., Lee C.G. p53 negatively regulates the expression of FAT10, a gene upregulated in various cancers. Oncogene 2006, 25:2318-2327.
56. Zhao X.J., Dong Q., Bindas J., Piganelli J.D., Magill A., Reiser J., Kolls J.K. TRIF and IRF-3 binding to the TNF promoter results in macrophage TNF dysregulation and steatosis induced by chronic ethanol. J. Immunol. 2008, 181:3049-3056.