ZIC2-dependent OCT4 activation drives self-renewal of human liver cancer stem cells

Journal of Clinical Investigation

Volumn 125, Issue 10, 2015, Pages 3795-3808

  Zhu, Pingping ^a   Wang, Yanying ^a   He, Lei ^b   Huang, Guanling ^a,c   Du, Ying ^a   Zhang, Geng ^a   Yan, Xinlong ^a   Xia, Pengyan ^a   Ye, Buqing ^a   Wang, Shuo ^a   Hao, Lu ^a,c   Wu, Jiayi ^a,c   Fan, Zusen ^a,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR FACTOR; NUCLEAR REMODELING FACTOR; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZIC2; TRANSCRIPTOME; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; FETAL ALZHEIMER ANTIGEN; MULTIENZYME COMPLEX; NERVE PROTEIN; NUCLEAR PROTEIN; POU5F1 PROTEIN, HUMAN; RBBP4 PROTEIN, HUMAN; RETINOBLASTOMA BINDING PROTEIN 4; TUMOR PROTEIN; ZIC2 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER STEM CELL; CELL RENEWAL; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CANCER CELL LINE; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CELL SELF-RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CRISPR CAS SYSTEM; CYTOLOGY; DEFICIENCY; GENE EXPRESSION REGULATION; GENE INACTIVATION; LIVER TUMOR; METABOLISM; MULTICELLULAR SPHEROID; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIGENS, NUCLEAR; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL SELF RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CRISPR-CAS SYSTEMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKOUT TECHNIQUES; HETEROGRAFTS; HUMANS; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; MULTIENZYME COMPLEXES; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; PROTEIN INTERACTION MAPPING; RETINOBLASTOMA-BINDING PROTEIN 4; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; TRANSCRIPTION FACTORS;

EID: 84943327838     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81979     Document Type: Article

References (55)

1. Han ZG. Functional genomic studies: insights into the pathogenesis of liver cancer. Annu Rev Genomics Hum Genet. 2012;13:171-205.
2. Visvader JE. Cells of origin in cancer. Nature. 2011;469(7330):314-322.
3. Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012;10(6):717-728.
4. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov. 2009;8(10):806-823.
5. Yang ZF, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell. 2008;13(2):153-166.
6. Haraguchi N, et al. CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest. 2010;120(9):3326-3339.
7. Sekiya S, Suzuki A. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature. 2011;475(7356):390-393.
8. Ladewig J, Koch P, Brüstle O. Leveling Waddington: the emergence of direct programming and the loss of cell fate hierarchies. Nat Rev Mol Cell Biol. 2013;14(4):225-236.
9. Yu J, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917-1920.
10. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663-676.
11. Nichols J, et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor OCT4. Cell. 1998;95(3):379-391.
12. Kim JB, et al. OCT4-induced pluripotency in adult neural stem cells. Cell. 2009;136(3):411-419.
13. Kim JB, et al. Direct reprogramming of human neural stem cells by OCT4. Nature. 2009;461(7264):649-653.
14. Wezel F, Pearson J, Kirkwood LA, Southgate J. Differential expression of OCT4 variants and pseudogenes in normal urothelium and urothelial cancer. Am J Pathol. 2013;183(4):1128-1136.
15. Zhang Z, et al. Follicle-stimulating hormone inhibits apoptosis in ovarian cancer cells by regulating the OCT4 stem cell signaling pathway. Int J Oncol. 2013;43(4):1194-1204.
16. Benedyk MJ, Mullen JR, DiNardo S. odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev. 1994;8(1):105-117.
17. Garcia-Frigola C, Carreres MI, Vegar C, Mason C, Herrera E. ZIC2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and-independent mechanisms. Development. 2008;135(10):1833-1841.
18. Chan DW, et al. ZIC2 synergistically enhances Hedgehog signalling through nuclear retention of Gli1 in cervical cancer cells. J Pathol. 2011;225(4):525-534.
19. Marchini S, et al. The zinc finger gene ZIC2 has features of an oncogene and its overexpression correlates strongly with the clinical course of epithelial ovarian cancer. Clin Cancer Res. 2012;18(16):4313-4324.
20. Narlikar GJ, Sundaramoorthy R, Owen-Hughes T. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell. 2013;154(3):490-503.
21. Wysocka J, et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature. 2006;442(7098):86-90.
22. Ruthenburg AJ, et al. Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell. 2011;145(5):692-706.
23. Hamiche A, Sandaltzopoulos R, Gdula DA, Wu C. ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell. 1999;97(7):833-842.
24. Landry J, et al. Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet. 2008;4(10):e1000241.
25. Cherry CM, Matunis EL. Epigenetic regulation of stem cell maintenance in the Drosophila testis via the nucleosome-remodeling factor NURF. Cell Stem Cell. 2010;6(6):557-567.
26. Song H, Spichiger-Haeusermann C, Basler K. The ISWI-containing NURF complex regulates the output of the canonical Wingless pathway. EMBO Rep. 2009;10(10):1140-1146.
27. Xia P, et al. WASH is required for the differentiation commitment of hematopoietic stem cells in a c-Myc-dependent manner. J Exp Med. 2014;211(10):2119-2134.
28. Ma S, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132(7):2542-2556.
29. Wang Y, et al. The long noncoding RNA lncTCF7 primes self-renewal of liver cancer stem cells through activation of Wnt signaling. Cell Stem Cell. 2015;16(4):413-425.
30. Wurmbach E, et al. Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma. Hepatology. 2007;45(4):938-947.
31. Barretina J, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603-607.
32. Hoshida Y, et al. Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma. Cancer Res. 2009;69(18):7385-7392.
33. Pan G, Qin B, Liu N, Scholer HR, Pei D. Identification of a nuclear localization signal in OCT4 and generation of a dominant negative mutant by its ablation. J Biol Chem. 2004;279(35):37013-37020.
34. Roessler S, et al. Integrative genomic identification of genes on 8p associated with hepatocellular carcinoma progression and patient survival. Gastroenterology. 2012;142(4):957-966 e912.
35. Boyault S, et al. Transcriptome classification of HCC is related to gene alterations and to new therapeutic targets. Hepatology. 2007;45(1):42-52.
36. Lapidot T, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367(6464):645-648.
37. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445(7123):106-110.
38. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med. 2009;15(9):1010-1012.
39. Ji J, Wang XW. Clinical implications of cancer stem cell biology in hepatocellular carcinoma. Semin Oncol. 2012;39(4):461-472.
40. Gidekel S, Pizov G, Bergman Y, Pikarsky E. Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell. 2003;4(5):361-370.
41. Hochedlinger K, Yamada Y, Beard C, Jaenisch R. Ectopic expression of Oct-4 blocks progenitorcell differentiation and causes dysplasia in epithelial tissues. Cell. 2005;121(3):465-477.
42. Chang CC, Shieh GS, Wu P, Lin CC, Shiau AL, Wu CL. Oct-3/4 expression reflects tumor progression and regulates motility of bladder cancer cells. Cancer Res. 2008;68(15):6281-6291.
43. Chen YC, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One. 2008;3(7):e2637.
44. Brown SA, et al. Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet. 1998;20(2):180-183.
45. Beck B, Blanpain C. Unravelling cancer stem cell potential. Nat Rev Cancer. 2013;13(10):727-738.
46. Greaves M, Maley CC. Clonal evolution in cancer. Nature. 2012;481(7381):306-313.
47. Krasteva V, Buscarlet M, Diaz-Tellez A, Bernard MA, Crabtree GR, Lessard JA. The BAF53a subunit of SWI/SNF-like BAF complexes is essential for hemopoietic stem cell function. Blood. 2012;120(24):4720-4732.
48. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273-304.
49. Alkhatib SG, Landry JW. The nucleosome remodeling factor. FEBS Lett. 2011;585(20):3197-3207.
50. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: the R Foundation for Statistical Computing; 2011.
51. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281-2308.
52. Xia P, et al. RNF2 is recruited by WASH to ubiquitinate AMBRA1 leading to downregulation of autophagy. Cell Res. 2014;24(8):943-958.
53. Ye B, et al. Pcid2 inactivates developmental genes in human and mouse embryonic stem cells to sustain their pluripotency by modulation of EID1 stability. Stem Cells. 2014;32(3):623-635.
54. Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347(1-2):70-78.
55. Zhu P, et al. C8orf4 negatively regulates selfrenewal of liver cancer stem cells via suppression of NOTCH2 signalling. Nat Commun. 2015;6:7122.