Overexpression of miR-122 promotes the hepatic differentiation and maturation of mouse ESCs through a miR-122/FoxA1/HNF4a-positive feedback loop

Liver International

Volumn 34, Issue 2, 2014, Pages 281-295

  Deng, Xiao Geng ^a   Qiu, Rong Lin ^a   Wu, Yao Hao ^a   Li, Zhi Xi ^a   Xie, Ping ^a   Zhang, Jie ^a   Zhou, Jia Jia ^a   Zeng, Le Xiang ^a   Tang, Jing ^a   Maharjan, Anu ^a   Deng, Jie Min ^b  

^a SUN YAT SEN MEMORIAL HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Differentiation; Embryonic stem cells; Hepatocytes; Mesenchymal to epithelial transition; MiR 122

Indexed keywords

ACTIVIN A; ADENOVIRUS VECTOR; BUTYRIC ACID; FIBROBLAST GROWTH FACTOR 4; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MICRORNA 122; UVOMORULIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; FEEDBACK SYSTEM; GENE OVEREXPRESSION; GENETIC TRANSFECTION; LIVER CELL; LIVER DEVELOPMENT; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; UPREGULATION;

DIFFERENTIATION; EMBRYONIC STEM CELLS; HEPATOCYTES; MESENCHYMAL-TO-EPITHELIAL TRANSITION; MIR-122;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FEEDBACK, PHYSIOLOGICAL; FLOW CYTOMETRY; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTES; MICE; MICROARRAY ANALYSIS; MICRORNAS; MICROSCOPY, FLUORESCENCE; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84891829963     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12239     Document Type: Article

References (47)

1. Zhou M, Li P, Tan L, et al. Differentiation of mouse embryonic stem cells into hepatocytes induced by a combination of cytokines and sodium butyrate. J Cell Biochem 2010; 109: 606-14.
2. Rambhatla L, Chiu CP, Kundu P, et al. Generation of hepatocyte-like cells from human embryonic stem cells. Cell Transplant 2003; 12: 1-11.
3. Moore RN, Dasgupta A, Rajaei N, et al. Enhanced differentiation of embryonic stem cells using co-cultivation with hepatocytes. Biotechnol Bioeng 2008; 101: 1332-43.
4. Deng X, Qiu R, Li Z, et al. Selection of hepatocyte-like cells from mouse differentiated embryonic stem cells and application in therapeutic liver repopulation. Cell Physiol Biochem 2012; 30: 1271-86.
5. Ivey KN, Muth A, Arnold J, et al. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2008; 2: 219-29.
6. Zhao C, Sun G, Li S, et al. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 2009; 16: 365-71.
7. Esau C, Davis S, Murray SF, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006; 3: 87-98.
8. Chang J, Nicolas E, Marks D, et al. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol 2004; 2: 106-13.
9. Tzur G, Levy A, Meiri E, et al. MicroRNA expression patterns and function in endodermal differentiation of human embryonic stem cells. PLoS ONE 2008; 3: e3726.
10. Cifelli CJ, Ross AC. All-trans-retinoic acid distribution and metabolism in vitamin A-marginal rats. Am J Physiol Gastrointest Liver Physiol 2006; 291: 195-202.
11. Zaret KS. Regulatory phases of early liver development: paradigms of organogenesis. Nat Rev Genet 2002; 3: 499-512.
12. Ann D, Masato N, Karim ST, et al. HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells. Development 2011; 138: 4143-53.
13. Yang J, MacDougall ML, McDowell MT, et al. Polyomic profiling reveals significant hepatic metabolic alterations in glucagon-receptor (GCGR) knockout mice: implications on anti-glucagon therapies for diabetes. BMC Genomics 2011; 12: 281.
14. Ball HJ, Sanchez-Perez A, Weiser S, et al. Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene 2007; 396: 203-13.
15. Hirschhorn R, Huie ML, Kasper JS. Computer assisted cloning of human neutral alpha-glucosidase C (GANC): a new paralog in the glycosyl hydrolase gene family 31. Proc Natl Acad Sci USA 2002; 99: 13642-6.
16. Chefetz I, Kohno K, Izumi H, et al. GALNT3, a gene associated with hyperphosphatemic familial tumoral calcinosis, is transcriptionally regulated by extracellular phosphate and modulates matrix metalloproteinase activity. Biochim Biophys Acta 2009; 1792: 61-7.
17. Purcell R, Childs M, Maibach R, et al. HGF/c-Met related activation of β-catenin in hepatoblastoma. J Exp Clin Cancer Res 2011; 30: 96.
18. Hartmann W, Küchler J, Koch A, et al. Activation of phosphatidylinositol-3′-kinase/AKT signaling is essential in hepatoblastoma survival. Clin Cancer Res 2009; 15: 4538-45.
19. Yang ZF, Ho DW, Lam CT, et al. Identification of brain-derived neurotrophic factor as a novel functional protein in hepatocellular carcinoma. Cancer Res 2005; 65: 219-25.
20. Schimanski CC, Bahre R, Gockel I, et al. Dissemination of hepatocellular carcinoma is mediated via chemokine receptor CXCR4. Br J Cancer 2006; 95: 210-7.
21. Teng Xm, Deng Q, Han Zg, et al. Expression of PNM A5 in hepatocellular carcinoma tissues and its function. Tumor 2008; 28: 911-5.
22. Qu X, Zhang C, Zhai Y, et al. Characterization and tissue expression of a novel human gene npdc1. Gene 2001; 264: 37-44.
23. Li T, Li D, Cheng L, et al. Epithelial-mesenchymal transition induced by hepatitis C virus core protein in cholangiocarcinoma. Ann Surg Oncol 2010; 17: 1937-44.
24. Baek JY, Morris SM, Campbell J, et al. TGF-beta inactivation and TGF-alpha overexpression cooperate in an in vivo mouse model to induce hepatocellular carcinoma that recapitulates molecular features of human liver cancer. Int J Cancer 2010; 127: 1060-71.
25. VanArsdale TL, VanArsdale SL, Force WR, et al. Lymphotoxin-beta receptor signaling complex: role of tumor necrosis factor receptor-associated factor 3 recruitment in cell death and activation of nuclear factor kappaB. Proc Natl Acad Sci USA 1997; 94: 2460-5.
26. Vail ME, Chaisson ML, Thompson J, et al. Bcl-2 expression delays hepatocyte cell cycle progression during liver regeneration. Oncogene 2002; 21: 1548-55.
27. Zaltsman Y, Shachnai L, Yivgi-Ohana N, et al. MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat Cell Biol 2010; 12: 553-62.
28. Sano M, Aoyagi K, Takahashi H, et al. Forkhead box A1 transcriptional pathway in KRT7-expressing esophageal squamous cell carcinomas with extensive lymph node metastasis. Int J Oncol 2010; 36: 321-30.
29. Santangelo L, Marchetti A, Cicchini C, et al. The stable repression of mesenchymal program is required for hepatocyte identity: a novel role for hepatocyte nuclear factor 4α. Hepatology 2011; 53: 2063-74.
30. Katoh Y, Katoh M. Hedgehog signaling, epithelial-to-mesenchymal transition and miRNA. Int J Mol Med 2008; 22: 271-5.
31. Cai J, Zhao Y, Liu Y, et al. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 2007; 45: 1229-39.
32. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11.
33. Magli MC, Levantini E, Giorgetti A. Developmental potential of somatic stem cells in mammalian adults. J Hematother Stem Cell Res 2000; 9: 961-9.
34. Kaestner KH. The making of the liver: developmental competence in foregut endoderm and induction of the hepatogenic program. Cell Cycle 2005; 4: 1146-8.
35. Lee CS, Friedman JR, Fulmer JT, et al. The initiation of liver development is dependent on Foxa transcription factors. Nature 2005; 435: 944-7.
36. Duncan SA, Manova K, Chen WS, et al. Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst. Proc Natl Acad Sci USA 1994; 91: 7598-602.
37. Odom DT, Zizlsperger N, Gordon DB, et al. Control of pancreas and liver gene expression by HNF transcription factors. Science 2004; 303: 1378-81.
38. Li J, Ning G, Duncan SA. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev 2000; 14: 464-74.
39. Sekiya S, Suzuki A. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 2011; 475: 390-3.
40. Zamule SM, Coslo DM, Chen F, et al. Differentiation of human embryonic stem cells along a hepatic lineage. Chem Biol Interact 2011; 190: 62-72.
41. Tomaru Y, Nakanishi M, Miura H, et al. Identification of an inter-transcription factor regulatory network in human hepatoma cells by Matrix RNAi. Nucleic Acids Res 2009; 37: 1049-60.
42. Li ZY, Xi Y, Zhu WN, et al. Positive regulation of hepatic miR-122 expression by HNF4α. J Hepatol 2011; 55: 602-11.
43. Xu H, He JH, Xiao ZD, et al. Liver-enriched transcription factors regulate microRNA-122 that targets CUTL1 during liver development. Hepatology 2010; 52: 1431-42.
44. Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90.
45. Yue HY, Yin C, Hou JL, et al. Hepatocyte nuclear factor 4alpha attenuates hepatic fibrosis in rats. Gut 2010; 59: 236-46.
46. Cheng JC, Leung PC. Type I collagen down-regulates E-cadherin expression by increasing PI3KCA in cancer cells. Cancer Lett 2011; 304: 107-16.
47. Kupferman ME, Jiffar T, El-Naggar A, et al. TrkB induces EMT and has a key role in invasion of head and neck squamous cell carcinoma. Oncogene 2010; 29: 2047-59.