MicroRNA-19b Reduces Hepatic Stellate Cell Proliferation by Targeting GRB2 in Hepatic Fibrosis Models in Vivo and in Vitro as Part of the Inhibitory Effect of Estradiol

Journal of Cellular Biochemistry

Volumn 116, Issue 11, 2015, Pages 2455-2464

  Ge, Shanfei ^a   Xie, Jianping ^a   Liu, Fei ^a   He, Jinni ^b   He, Jinwen ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Central South University   (China)

Author keywords

ESTRADIOL; GRB2; miR 19b; PROLIFERATION

Indexed keywords

COLLAGEN TYPE 1; ESTRADIOL; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; MESSENGER RNA; MICRORNA; MICRORNA 19B; UNCLASSIFIED DRUG; COLLAGEN TYPE I, ALPHA 1 CHAIN; ESTROGEN; GRB2 PROTEIN, RAT; MIRN19 MICRORNA, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ESTROGEN ACTIVITY; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LIVER FIBROSIS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; SEX DIFFERENCE; STELLATE CELL; UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EXPERIMENTAL LIVER CIRRHOSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; GRB2 ADAPTOR PROTEIN; HEPATIC STELLATE CELLS; IN VITRO TECHNIQUES; LIVER CIRRHOSIS, EXPERIMENTAL; MALE; MICRORNAS; PROMOTER REGIONS, GENETIC; RATS;

EID: 84941027392     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25116     Document Type: Article

References (43)

1. Ambros V,. 2004. The functions of animal microRNAs. Nature 431: 350-355.
2. Baltensperger K, Kozma LM, Cherniack AD, Klarlund JK, Chawla A, Banerjee U, Czech MP,. 1993. Binding of the Ras activator son of sevenless to insulin receptor substrate-1 signaling complexes. Science 260: 1950-1952.
3. Bissell DM,. 1999. Sex and hepatic fibrosis. Hepatology 29: 988-989.
4. Bogatkevich GS, Ludwicka-Bradley A, Highland KB, Hant F, Nietert PJ, Singleton CB, Silver RM,. 2007. Down-regulation of collagen and connective tissue growth factor expression with hepatocyte growth factor in lung fibroblasts from white scleroderma patients via two signaling pathways. Arthritis Rheum 56: 3468-3477.
5. Castellano L, Giamas G, Jacob J, Coombes RC, Lucchesi W, Thiruchelvam P, Barton G, Jiao LR, Wait R, Waxman J, Hannon GJ, Stebbing J,. 2009. The estrogen receptor-alpha-induced microRNA signature regulates itself and its transcriptional response. Proc Natl Acad Sci U S A 106: 15732-15737.
6. Chen XM,. 2009. MicroRNA signatures in liver diseases. World J Gastroenterol 15: 1665-1672.
7. Dance M, Montagner A, Salles J-P, Yart A, Raynal P,. 2008. The molecular functions of Shp2 in the Ras/Mitogen-activated protein kinase (ERK1/2) pathway. Cellular Signal 20: 453-459.
8. Dolganiuc A, Petrasek J, Kodys K, Catalano D, Mandrekar P, Velayudham A, Szabo G,. 2009. MicroRNA expression profile in Lieber-DeCarli diet-induced alcoholic and methionine choline deficient diet-induced nonalcoholic steatohepatitis models in mice. Alcohol Clin Exp Res 33: 1704-1710.
9. Friedman SL,. 2008. Hepatic fibrosis-overview. Toxicology 254: 120-129.
10. Hardie WD, Glasser SW, Hagood JS,. 2009. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 175: 3-16.
11. Iwaki J, Kikuchi K, Mizuguchi Y, Kawahigashi Y, Yoshida H, Uchida E, Takizawa T,. 2013. MiR-376c down-regulation accelerates EGF-dependent migration by targeting GRB2 in the HuCCT1 human intrahepatic cholangiocarcinoma cell line. PLOS ONE 8: e69496.
12. Jin X, Ye YF, Chen SH, Yu CH, Liu J, Li YM,. 2009. MicroRNA expression pattern in different stages of nonalcoholic fatty liver disease. Dig Liver Dis 41: 289-297.
13. Kim VN,. 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
14. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M,. 2005. Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
15. Lakner AM, Steuerwald NM, Walling TL, Ghosh S, Li T, McKillop IH, Russo MW, Bonkovsky HL, Schrum LW,. 2012. Inhibitory effects of microRNA 19b in hepatic stellate cell-mediated fibrogenesis. Hepatology 56: 300-310.
16. Liu Y, Liu Q, Jia W, Chen J, Wang J, Ye D, Guo X, Chen W, Li G, Wang G,. 2013. MicroRNA-200a regulates Grb2 and suppresses differentiation of mouse embryonic stem cells into endoderm and mesoderm. PLOS ONE 8: e68990.
17. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J,. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431-442.
18. Luo H, Zhang H, Zhang Z, Zhang X, Ning B, Guo J, Nie N, Liu B, Wu X,. 2009. Down-regulated miR-9 and miR-433 in human gastric carcinoma. J Exp Clin Cancer Res 28: 1-9.
19. Martino VD, Lebray P, Myers RP, Pannier E, Paradis V, Charlotte F, Moussalli J, Thabut D, Buffet C, Poynard T,. 2004. Progression of liver fibrosis in women infected with hepatitis C: long-term benefit of estrogen exposure. Hepatology 40: 1426-1433.
20. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A,. 2007. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773: 1263-1284.
21. Murakami Y, Toyoda H, Tanaka M, Kuroda M, Harada Y, Matsuda F, Tajima A, Kosaka N, Ochiya T, Shimotohno K,. 2011. The progression of liver fibrosis is related with overexpression of the miR-199 and 200 families. PLoS One 6: e16081.
22. Noetel A, Kwiecinski M, Elfimova N, Huang J, Odenthal M,. 2012. microRNA are central players in anti-and profibrotic gene regulation during liver fibrosis. Front Physiol 3.
23. Osuna-Martínez U, Reyes-Esparza JA, Petricevich VL, Hernández-Pando R, Rodríguez-Fragoso L,. 2011a. Protective effect of thymic humoral factor on porcine serum-induced hepatic fibrosis and liver damage in Wistar rats. Ann Hepatol 10: 540.
24. Osuna-Martínez U, Reyes-Esparza JA, Petricevich VL, Hernández-Pando R, Rodríguez-Fragoso L,. 2011b. Protective effect of thymic humoral factor on porcine serum induced hepatic fibrosis and liver dam age in Wistar rats. Ann Hepatol 10: 540-551.
25. Priya S, Sudhakaran PR,. 2008. Cell survival, activation and apoptosis of hepatic stellate cells: modulation by extracellular matrix proteins. Hepatol Res 38: 1221-1232.
26. Rescan C, Coutant A, Talarmin H, Theret N, Glaise D, Guguen-Guillouzo C, Baffet G,. 2001. Mechanism in the sequential control of cell morphology and S phase entry by epidermal growth factor involves distinct MEK/ERK activations. Mol Biol Cell 12: 725-738.
27. Roderburg C, Urban GW, Bettermann K, Vucur M, Zimmermann H, Schmidt S, Janssen J, Koppe C, Knolle P, Castoldi M, Tacke F, Trautwein C, Luedde T,. 2011. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 53: 209-218.
28. Rosenfeld MG, Lunyak VV, Glass CK,. 2006. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20: 1405-1428.
29. Scaltriti M, Baselga J,. 2006. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res 12: 5268-5272.
30. Shan X, Miao Y, Fan R, Song C, Wu G, Wan Z, Zhu J, Sun G, Zha W, Mu X,. 2013. Suppression of Grb2 expression improved hepatic steatosis, oxidative stress, and apoptosis induced by palmitic acid in vitro partly through insulin signaling alteration. In Vitro Cell Dev Biol Anim 49: 576-582.
31. Shanfei G, Xiaowei W, Jianping X, Xin Y, Fei L,. 2014. Deep sequencing analysis of microRNA expression in porcine serum-induced hepatic fibrosis rats. Ann Hepatol 13: 439-449.
32. Shimizu I,. 2003. Impact of oestrogens on the progression of liver disease. Liver Int 23: 63-69.
33. Shimizu I, Ito S,. 2007. Protection of estrogens against the progression of chronic liver disease. Hepatol Res 37: 239-247.
34. Shimizu I, Mizobuchi Y, Yasuda M, Shiba M, Ma Y, Horie T, Liu F, Ito S,. 1999. Inhibitory effect of oestradiol on activation of rat hepatic stellate cells in vivo and in vitro. Gut 44: 127-136.
35. Talarmin H, Rescan C, Cariou S, Glaise D, Zanninelli G, Bilodeau M, Loyer P, Guguen-Guillouzo C, Baffet G,. 1999. The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G1 phase progression in proliferating hepatocytes. Mol Cell Biol 19: 6003-6011.
36. van Almen GC, Verhesen W, van Leeuwen RE, van de Vrie M, Eurlings C, Schellings MW, Swinnen M, Cleutjens JP, van Zandvoort MA, Heymans S, Schroen B,. 2011. MicroRNA-18 and microRNA-19 regulate CTGF and TSP-1 expression in age-related heart failure. Aging Cell 10: 769-779.
37. Venugopal SK, Jiang J, Kim TH, Li Y, Wang SS, Torok NJ, Wu J, Zern MA,. 2010. Liver fibrosis causes downregulation of miRNA-150 and miRNA-194 in hepatic stellate cells, and their overexpression causes decreased stellate cell activation. Am J Physiol Gastrointest Liver Physiol 298: G101-G106.
38. Vogel S, Piantedosi R, Frank J, Lalazar A, Rockey DC, Friedman SL, Blaner WS,. 2000. An immortalized rat liver stellate cell line (HSC-T6): a new cell model for the study of retinoid metabolism in vitro. J Lipid Res 41: 882-893.
39. Wang P, Liu T, Cong M, Wu X, Bai Y, Yin C, An W, Wang B, Jia J, You H,. 2009. Expression of extracellular matrix genes in cultured hepatic oval cells: an origin of hepatic stellate cells through transforming growth factor beta ? Liver Int 29: 575-584.
40. Xu JW, Gong J, Chang XM, Luo JY, Dong L, Hao ZM, Jia A, Xu GP,. 2002. Estrogen reduces CCL4- induced liver fibrosis in rats. World J Gastroenterol 8: 883-887.
41. Yasuda M, Shimizu I, Shiba M, Ito S,. 1999. Suppressive effects of estradiol on dimethylnitrosamine-induced fibrosis of the liver in rats. Hepatology 29: 719-727.
42. Zhang S, Weinheimer C, Courtois M, Kovacs A, Zhang CE, Cheng AM, Wang Y, Muslin AJ,. 2003. The role of the Grb2-p38 MAPK signaling pathway in cardiac hypertrophy and fibrosis. J Clin Invest 111: 833-841.
43. Zhang Y, Wu L, Wang Y, Zhang M, Li L, Zhu D, Li X, Gu H, Zhang C-Y, Zen K,. 2012. Protective role of estrogen-induced miRNA-29 expression in carbon tetrachloride-induced mouse liver injury. J Biol Chem 287: 14851-14862.