H19 promotes cholestatic liver fibrosis by preventing ZEB1-mediated inhibition of epithelial cell adhesion molecule

Hepatology

Volumn 66, Issue 4, 2017, Pages 1183-1196

  Song, Yongfeng ^a,b   Liu, Chune ^a   Liu, Xia ^c   Trottier, Jocelyn ^d   Beaudoin, Michele ^a   Zhang, Li ^a   Pope, Chad ^a   Peng, Guangyong ^c   Barbier, Olivier ^d   Zhong, Xiaobo ^a   Li, Linheng ^e   Wang, Li ^a,f,g,h  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

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

^d UNIVERSITÉ LAVAL   (Canada)

^e STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^h WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA SMOOTH MUSCLE ACTIN; ASPARTATE AMINOTRANSFERASE; BILE ACID; BILIRUBIN; BILIRUBIN GLUCURONIDE; CHEMOKINE RECEPTOR CCR2; CHOLESTEROL 7ALPHA MONOOXYGENASE; CHOLIC ACID; COLLAGEN TYPE I ALPHA 1; COLLAGEN TYPE I ALPHA 2; CYP7B1 PROTEIN; CYP8B1 PROTEIN; CYTOKERATIN 19; CYTOKERATIN 7; EPITHELIAL CELL ADHESION MOLECULE; FARNESOID X RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 4; GLYCOCHENODEOXYCHOLIC ACID; GLYCOURSODEOXYCHOLIC ACID; INTERLEUKIN 17; INTERLEUKIN 4; PROTEIN FOS; PROTEIN TYROSINE PHOSPHATASE SHP; RNA H19; TAURODEOXYCHOLIC ACID; TAUROURSODEOXYCHOLIC ACID; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR ZEB1; UNCLASSIFIED DRUG; H19 LONG NON-CODING RNA; LONG UNTRANSLATED RNA;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILE ACID BLOOD LEVEL; BILE ACID SYNTHESIS; BILE DUCT LIGATION; BILIRUBIN BLOOD LEVEL; BINDING AFFINITY; CC-LP-1 CELL LINE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHOLANGIOCARCINOMA CELL LINE; CHOLANGIOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; FIBROGENESIS; GAMMA DELTA T LYMPHOCYTE; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HEK293T CELL LINE; HEP 3B2.1-7 CELL LINE; HEP-G2 CELL LINE; HEPATITIS; HUCC-T1 CELL LINE; HUH-7 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; INTRAHEPATIC CHOLESTASIS; LIVER FIBROSIS; LIVER HYPERPLASIA; LIVER TISSUE; MOUSE; MZ-CHA-1 CELL LINE; NONHUMAN; PRIMARY BILIARY CIRRHOSIS; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; SG231 CELL LINE; SIGNAL TRANSDUCTION; SPLEEN TISSUE; UPREGULATION; ADULT; AGED; ANIMAL; C57BL MOUSE; CHOLESTASIS; COMPLICATION; FEMALE; HEK293 CELL LINE; LIVER CIRRHOSIS; MALE; METABOLISM; MIDDLE AGED; YOUNG ADULT;

ADULT; AGED; ANIMALS; BILE ACIDS AND SALTS; CHOLESTASIS; EPITHELIAL CELL ADHESION MOLECULE; FEMALE; HEK293 CELLS; HEP G2 CELLS; HUMANS; LIVER CIRRHOSIS; MALE; MICE, INBRED C57BL; MIDDLE AGED; RNA, LONG NONCODING; UP-REGULATION; YOUNG ADULT; ZINC FINGER E-BOX-BINDING HOMEOBOX 1;

EID: 85028329477     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.29209     Document Type: Article

References (39)

1. Wang L, Lee YK, Bundman D, Han Y, Thevananther S, Kim CS, et al. Redundant pathways for negative feedback regulation of bile acid production. Dev Cell 2002;2:721-731.
2. Chiang JY. Bile acids: regulation of synthesis. J Lipid Res 2009;50:1955-1966.
3. Zhang Y, Xu N, Xu J, Kong B, Copple B, Guo GL, et al. E2F1 is a novel fibrogenic gene that regulates cholestatic liver fibrosis through the Egr-1/SHP/EID1 network. Hepatology 2014;60:919-930.
4. Ratajczak MZ. Igf2-H19, an imprinted tandem gene, is an important regulator of embryonic development, a guardian of proliferation of adult pluripotent stem cells, a regulator of longevity, and a “passkey” to cancerogenesis. Folia Histochem Cytobiol 2012;50:171-179.
5. Zhang Y, Liu C, Barbier O, Smalling R, Tsuchiya H, Lee S, et al. Bcl2 is a critical regulator of bile acid homeostasis by dictating Shp and lncRNA H19 function. Sci Rep 2016;6:20559.
6. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008;10:593-601.
7. Larsen JE, Nathan V, Osborne JK, Farrow RK, Deb D, Sullivan JP, et al. ZEB1 drives epithelial-to-mesenchymal transition in lung cancer. J Clin Invest 2016;126:3219-3235.
8. Zhang Y, Yang Z, Whitby R, Wang L. Regulation of miR-200c by nuclear receptors PPARalpha, LRH-1 and SHP. Biochem Biophys Res Commun 2011;416:135-139.
9. Zhang Y, Hagedorn CH, Wang L. Role of nuclear receptor SHP in metabolism and cancer. Biochim Biophys Acta 2011;1812:893-908.
10. Rudraiah S, Zhang X, Wang L. nuclear receptors as therapeutic targets in liver disease: are we there yet? Annu Rev Pharmacol Toxicol 2016;56:605-626.
11. Matouk IJ, Halle D, Raveh E, Gilon M, Sorin V, Hochberg A. The role of the oncofetal H19 lncRNA in tumor metastasis: orchestrating the EMT-MET decision. Oncotarget 2016;7:3748-3765.
12. Dolle L, Theise ND, Schmelzer E, Boulter L, Gires O, van Grunsven LA. EpCAM and the biology of hepatic stem/progenitor cells. Am J Physiol Gastrointest Liver Physiol 2015;308:G233-G250.
13. Mani SK, Zhang H, Diab A, Pascuzzi PE, Lefrancois L, Fares N, et al. EpCAM-regulated intramembrane proteolysis induces a cancer stem cell-like gene signature in hepatitis B virus-infected hepatocytes. J Hepatol 2016;65:888-898.
14. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, et al. Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 2009;11:162-171.
15. Uehara T, Ainslie GR, Kutanzi K, Pogribny IP, Muskhelishvili L, Izawa T, et al. Molecular mechanisms of fibrosis-associated promotion of liver carcinogenesis. Toxicol Sci 2013;132:53-63.
16. Venkatraman A, He XC, Thorvaldsen JL, Sugimura R, Perry JM, Tao F, et al. Maternal imprinting at the H19-Igf2 locus maintains adult haematopoietic stem cell quiescence. Nature 2013;500:345-349.
17. Lee SM, Zhang Y, Tsuchiya H, Smalling R, Jetten AM, Wang L. Small heterodimer partner/neuronal PAS domain protein 2 axis regulates the oscillation of liver lipid metabolism. Hepatology 2015;61:497-505.
18. Yang Z, Tsuchiya H, Zhang Y, Lee S, Liu C, Huang Y, et al. REV-ERBalpha activates C/EBP homologous protein to control small heterodimer partner-mediated oscillation of alcoholic fatty liver. Am J Pathol 2016;186:2909-2920.
19. Tabbi-Anneni I, Cooksey R, Gunda V, Liu S, Mueller A, Song G, et al. Overexpression of nuclear receptor SHP in adipose tissues affects diet-induced obesity and adaptive thermogenesis. Am J Physiol Endocrinol Metab 2010;298:E961-E970.
20. Zhang L, Yang Z, Trottier J, Barbier O, Wang L. Long noncoding RNA MEG3 induces cholestatic liver injury by interaction with PTBP1 to facilitate shp mRNA decay. Hepatology 2017;65:604-615.
21. Zhang Y, Wang L. Nuclear receptor SHP inhibition of Dnmt1 expression via ERRgamma. FEBS Lett 2011;585:1269-1275.
22. Yang Z, Koehler AN, Wang L. A novel small molecule activator of nuclear receptor SHP inhibits HCC cell migration via suppressing Ccl2. Mol Cancer Ther 2016;15:2294-2301.
23. Zhou T, Zhang Y, Macchiarulo A, Yang Z, Cellanetti M, Coto E, et al. Novel polymorphisms of nuclear receptor SHP associated with functional and structural changes. J Biol Chem 2010;285:24871-24881.
24. Yang Z, Wang L. An autoregulatory feedback loop between Mdm2 and SHP that fine tunes Mdm2 and SHP stability. FEBS Lett 2012;586:1135-1140.
25. Woo K, Sathe M, Kresge C, Esser V, Ueno Y, Venter J, et al. Adenosine triphosphate release and purinergic (P2) receptor-mediated secretion in small and large mouse cholangiocytes. Hepatology 2010;52:1819-1828.
26. Han Y, Meng F, Venter J, Wu N, Wan Y, Standeford H, et al. miR-34a-dependent overexpression of Per1 decreases cholangiocarcinoma growth. J Hepatol 2016;64:1295-1304.
27. Huang Y, Ma C, Zhang Q, Ye J, Wang F, Zhang Y, et al. CD4+ and CD8+ T cells have opposing roles in breast cancer progression and outcome. Oncotarget 2015;6:17462-17478.
28. Yang Z, Zhang Y, Wang L. A feedback inhibition between miRNA-127 and TGFbeta/c-Jun cascade in HCC cell migration via MMP13. PLoS One 2013;8:e65256.
29. Tsuchiya H, da Costa KA, Lee S, Renga B, Jaeschke H, Yang Z, et al. Interactions between nuclear receptor SHP and FOXA1 maintain oscillatory homocysteine homeostasis in mice. Gastroenterology 2015;148:1012-1023.
30. Lua I, James D, Wang J, Wang KS, Asahina K. Mesodermal mesenchymal cells give rise to myofibroblasts, but not epithelial cells, in mouse liver injury. Hepatology 2014;60:311-322.
31. Yoon SM, Gerasimidou D, Kuwahara R, Hytiroglou P, Yoo JE, Park YN, et al. Epithelial cell adhesion molecule (EpCAM) marks hepatocytes newly derived from stem/progenitor cells in humans. Hepatology 2011;53:964-973.
32. Zhang Y, Andrews GK, Wang L. Zinc-induced Dnmt1 expression involves antagonism between MTF-1 and nuclear receptor SHP. Nucleic Acids Res 2012;40:4850-4860.
33. Yang Z, Tsuchiya H, Zhang Y, Hartnett ME, Wang L. MicroRNA-433 inhibits liver cancer cell migration by repressing the protein expression and function of cAMP response element-binding protein. J Biol Chem 2013;288:28893-28899.
34. Marchioni Beery RM, Vaziri H, Forouhar F. Primary biliary cirrhosis and primary sclerosing cholangitis: a review featuring a women's health perspective. J Clin Transl Hepatol 2014;2:266-284.
35. Williams MJ, Clouston AD, Forbes SJ. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 2014;146:349-356.
36. Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, Hochberg A, Galun E. The H19 non-coding RNA is essential for human tumor growth. PLoS One 2007;2:e845.
37. Zen Y, Vara R, Portmann B, Hadzic N. Childhood hepatocellular carcinoma: a clinicopathological study of 12 cases with special reference to EpCAM. Histopathology 2014;64:671-682.
38. Jagle S, Dertmann A, Schrempp M, Hecht A. ZEB1 is neither sufficient nor required for epithelial-mesenchymal transition in LS174T colorectal cancer cells. Biochem Biophys Res Commun 2017;482:1226-1232.
39. Michelotti GA, Tucker A, Swiderska-Syn M, Machado MV, Choi SS, Kruger L, Soderblom E, et al. Pleiotrophin regulates the ductular reaction by controlling the migration of cells in liver progenitor niches. Gut 2016;65:683-692.