Nanog regulates molecules involved in stemness and cell cycle-signaling pathway for maintenance of pluripotency of P19 embryonal carcinoma stem cells

Journal of Cellular Physiology

Volumn 227, Issue 11, 2012, Pages 3678-3692

  Choi, Seung Cheol ^a   Choi, Ji Hyun ^a   Park, Chi Yeon ^a   Ahn, Chul Min ^a   Hong, Soon Jun ^a   Lim, Do Sun ^a  

^a Korea University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; COMPLEMENTARY DNA; CYCLIN D1; CYCLIN D2; FIBROBLAST GROWTH FACTOR 4; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 2; LEUKEMIA INHIBITORY FACTOR; NUCLEAR RECEPTOR NR6A1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; PROTEIN BCL 6; PROTEIN CRIPTO; PROTEIN CUL3; PROTEIN JDP2; PROTEIN KINASE LYN; PROTEIN KINASE YES; PROTEIN P53; PROTEIN REX1; PROTEIN SMARCC1; PROTEIN TOB1; PROTEIN ZFP143; PROTEIN ZFP57; SMALL INTERFERING RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; CELL CYCLE; EMBRYONAL CARCINOMA STEM CELL; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

CELL CYCLE PROTEINS; CELL DIFFERENTIATION; EMBRYONAL CARCINOMA STEM CELLS; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLURIPOTENT STEM CELLS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84864077183     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24076     Document Type: Article

References (68)

1. Ahn J, Ko M, Lee C, Kim J, Yoon H, Seong RH. 2011. Srg3, a mouse homolog of BAF155, is a novel p53 target and acts as a tumor suppressor by modulating p21(WAF1/CIP1) expression. Oncogene 30: 445- 456.
2. Al-Mulla F, Al-Tamimi R, Bitar MS. 2004. Comparison of two probe preparation methods using long oligonucleotide microarrays. Biotechniques 37: 827- 833.
3. Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL, van Wijnen AJ, Stein GS. 2006. Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J Cell Physiol 209: 883- 893.
4. Becker KA, Ghule PN, Lian JB, Stein JL, van Wijnen AJ, Stein GS. 2010. Cyclin D2 and the CDK substrate p220(NPAT) are required for self-renewal of human embryonic stem cells. J Cell Physiol 222: 456- 464.
5. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947- 956.
6. Bryja V, Pacherník J, Vondrácek J, Soucek K, Cajánek L, Horvath V, Holubcová Z, Dvorák P, Hampl A. 2008. Lineage specific composition of cyclin D-CDK4/CDK6-p27 complexes reveals distinct functions of CDK4, CDK6 and individual D-type cyclins in differentiating cells of embryonic origin. Cell Prolif 41: 875- 893.
7. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643- 655.
8. Chang G, Miao YL, Zhang Y, Liu S, Kou Z, Ding J, Chen DY, Sun QY, Gao S. 2010. Linking incomplete reprogramming to the improved pluripotency of murine embryonal carcinoma cell-derived pluripotent stem cells. PLoS ONE 5: e10320.
9. Chen Y, Du Z, Yao Z. 2006. Roles of the Nanog protein in murine F9 embryonal carcinoma cells and their endoderm-differentiated counterparts. Cell Res 16: 641- 650.
10. Chen X, Fang F, Liou YC, Ng HH. 2008. Zfp143 regulates Nanog through modulation of Oct4 binding. Stem Cells 26: 2759- 2767.
11. Choi SC, Yoon J, Shim WJ, Ro YM, Lim DS. 2004. 5-Azacytidine induces cardiac differentiation of P19 embryonic stem cells. Exp Mol Med 36: 515- 523.
12. Choi SC, Choi JH, Shim WJ, Lim DS. 2008. P19 embryonal carcinoma cells: A new model for the study of endothelial cell differentiation. Biotechnol Lett 30: 1169- 1175.
13. Chong JL, Wenzel PL, Sáenz-Robles MT, Nair V, Ferrey A, Hagan JP, Gomez YM, Sharma N, Chen HZ, Ouseph M, Wang SH, Trikha P, Culp B, Mezache L, Winton DJ, Sansom OJ, Chen D, Bremner R, Cantalupo PG, Robinson ML, Pipas JM, Leone G. 2009. E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 462: 930- 934.
14. Clark AT, Rodriguez RT, Bodnar MS, Abeyta MJ, Cedars MI, Turek PJ, Firpo MT, Reijo Pera RA. 2004. Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22: 169- 179.
15. Darr H, Mayshar Y, Benvenisty N. 2006. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 133: 1193- 1201.
16. Faast R, White J, Cartwright P, Crocker L, Sarcevic B, Dalton S. 2004. Cdk6-cyclin D3 activity in murine ES cells is resistant to inhibition by p16(INK4a). Oncogene 23: 491- 502.
17. Glozak MA, Rogers MB. 2001. Retinoic acid- and BMP 4-induced apoptosis in P19 embryonal carcinoma cells requires p27. Exp Cell Res 268: 128- 138.
18. Hall J, Guo G, Wray J, Eyres I, Nichols J, Grotewold L, Morfopoulou S, Humphreys P, Mansfield W, Walker R, Tomlinson S, Smith A. 2009. Oct4 and LIF/Stat3 additively induce Krüppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell 5: 597- 609.
19. Hardiman G. 2004. Microarray platforms-Comparisons and contrasts. Pharmacogenomics 5: 487- 502.
20. He Z, Wu L, Fields MW, Zhou J. 2005. Use of microarrays with different probe sizes for monitoring gene expression. Appl Environ Microbiol 71: 5154- 5162.
21. Hessner MJ, Xiang B, Jia S, Geoffrey R, Holmes S, Meyer L, Muheisen S, Wang X. 2006. Three-color cDNA microarrays with prehybridization quality control yield gene expression data comparable to that of commercial platforms. Physiol Genomics 25: 166- 178.
22. Ho KJ, Do NL, Otu HH, Dib MJ, Ren X, Enjyoji K, Robson SC, Terwilliger EF, Karp SJ. 2010. Tob1 is a constitutively expressed repressor of liver regeneration. J Exp Med 207: 1197- 1208.
23. Hosler BA, LaRosa GJ, Grippo JF, Gudas LJ. 1989. Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol Cell Biol 9: 5623- 5629.
24. Hough SR, Clements I, Welch PJ, Wiederholt KA. 2006. Differentiation of mouse embryonic stem cells after RNA interference-mediated silencing of OCT4 and Nanog. Stem Cells 24: 1467- 1475.
25. Hyslop L, Stojkovic M, Armstrong L, Walter T, Stojkovic P, Przyborski S, Herbert M, Murdoch A, Strachan T, Lako M. 2005. Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells 23: 1035- 1043.
26. Irizarry RA, Warren D, Spencer F, Kim IF, Biswal S, Frank BC, Gabrielson E, Garcia JG, Geoghegan J, Germino G, Griffin C, Hilmer SC, Hoffman E, Jedlicka AE, Kawasaki E, Martínez-Murillo F, Morsberger L, Lee H, Petersen D, Quackenbush J, Scott A, Wilson M, Yang Y, Ye SQ, Yu W. 2005. Multiple-laboratory comparison of microarray platforms. Nat Methods 2: 345- 350.
27. Izumi H, Wakasugi T, Shimajiri S, Tanimoto A, Sasaguri Y, Kashiwagi E, Yasuniwa Y, Akiyama M, Han B, Wu Y, Uchiumi T, Arao T, Nishio K, Yamazaki R, Kohno K. 2010. Role of ZNF143 in tumor growth through transcriptional regulation of DNA replication and cell-cycle-associated genes. Cancer Sci 101: 2538- 2545.
28. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, Robson P, Zhong S, Ng HH. 2008. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 10: 353- 360.
29. Jin C, Li H, Murata T, Sun K, Horikoshi M, Chiu R, Yokoyama KK. 2002. JDP2, a repressor of AP-1, recruits a histone deacetylase 3 complex to inhibit the retinoic acid-induced differentiation of F9 cells. Mol Cell Biol 22: 4815- 4826.
30. Kawaida R, Ohtsuka T, Okutsu J, Takahashi T, Kadono Y, Oda H, Hikita A, Nakamura K, Tanaka S, Furukawa H. 2003. Jun dimerization protein 2 (JDP2), a member of the AP-1 family of transcription factor, mediates osteoclast differentiation induced by RANKL. J Exp Med 197: 1029- 1035.
31. Kim K, Choi J, Heo K, Kim H, Levens D, Kohno K, Johnson EM, Brock HW, An W. 2008. Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription. J Biol Chem 283: 9113- 9126.
32. Kossatz U, Breuhahn K, Wolf B, Hardtke-Wolenski M, Wilkens L, Steinemann D, Singer S, Brass F, Kubicka S, Schlegelberger B, Schirmacher P, Manns MP, Singer JD, Malek NP. 2010. The cyclin E regulator cullin 3 prevents mouse hepatic progenitor cells from becoming tumor-initiating cells. J Clin Invest 120: 3820- 3833.
33. Kuijk EW, van Mil A, Brinkhof B, Penning LC, Colenbrander B, Roelen BA. 2010. PTEN and TRP53 independently suppress Nanog expression in spermatogonial stem cells. Stem Cells Dev 19: 979- 988.
34. Kuo WP, Jenssen TK, Butte AJ, Ohno-Machado L, Kohane IS. 2002. Analysis of matched mRNA measurements from two different microarray technologies. Bioinformatics 18: 405- 412.
35. Li Y, Glozak MA, Smith SM, Rogers MB. 1999. The expression and activity of D-type cyclins in F9 embryonal carcinoma cells: Modulation of growth by RXR-selective retinoids. Exp Cell Res 253: 372- 384.
36. Liang J, Wan M, Zhang Y, Gu P, Xin H, Jung SY, Qin J, Wong J, Cooney AJ, Liu D, Songyang Z. 2008. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 10: 731- 739.
37. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, Xu Y. 2005. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 7: 165- 171.
38. Mah N, Thelin A, Lu T, Nikolaus S, Kühbacher T, Gurbuz Y, Eickhoff H, Klöppel G, Lehrach H, Mellgård B, Costello CM, Schreiber S. 2004. A comparison of oligonucleotide and cDNA-based microarray systems. Physiol Genomics 16: 361- 370.
39. Mallanna SK, Boer B, Desler M, Rizzino A. 2008. Differential regulation of the Oct-3/4 gene in cell culture model systems that parallel different stages of mammalian development. Mol Reprod Dev 75: 1247- 1257.
40. McBurney MW, Jones-Villeneuve EM, Edwards MK, Anderson PJ. 1982. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299: 165- 167.
41. Mecham BH, Klus GT, Strovel J, Augustus M, Byrne D, Bozso P, Wetmore DZ, Mariani TJ, Kohane IS, Szallasi Z. 2004. Sequence-matched probes produce increased cross-platform consistency and more reproducible biological results in microarray-based gene expression measurements. Nucleic Acids Res 32: e74.
42. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631- 642.
43. Mo P, Wang H, Lu H, Boyd DD, Yan C. 2010. MDM2 mediates ubiquitination and degradation of activating transcription factor 3. J Biol Chem 285: 26908- 26915.
44. Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R. 1998. A role for SOX1 in neural determination. Development 125: 1967- 1978.
45. Polager S, Ginsberg D. 2008. E2F-At the crossroads of life and death. Trends Cell Biol 18: 528- 535.
46. Polager S, Ginsberg D. 2009. p53 and E2f: Partners in life and death. Nat Rev Cancer 9: 738- 748.
47. Preclíková H, Bryja V, Pacherník J, Krejcí P, Dvorák P, Hampl A. 2002. Early cycling-independent changes to p27, cyclin D2, and cyclin D3 in differentiating mouse embryonal carcinoma cells. Cell Growth Differ 13: 421- 430.
48. Qin P, Haberbusch JM, Zhang Z, Soprano KJ, Soprano DR. 2004. Pre-B cell leukemia transcription factor (PBX) proteins are important mediators for retinoic acid-dependent endodermal and neuronal differentiation of mouse embryonal carcinoma P19 cells. J Biol Chem 279: 16263- 16271.
49. Relógio A, Schwager C, Richter A, Ansorge W, Valcárcel J. 2002. Optimization of oligonucleotide-based DNA microarrays. Nucleic Acids Res 30: e51.
50. Ren X, Cao C, Zhu L, Yoshida K, Kharbanda S, Weichselbaum R, Kufe D. 2002. Lyn tyrosine kinase inhibits nuclear export of the p53 tumor suppressor. Cancer Biol Ther 1: 703- 708.
51. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. 2000. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 18: 399- 404.
52. Rogers MB, Hosler BA, Gudas LJ. 1991. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 113: 815- 824.
53. Schaniel C, Ang YS, Ratnakumar K, Cormier C, James T, Bernstein E, Lemischka IR, Paddison PJ. 2009. Smarcc1/Baf155 couples self-renewal gene repression with changes in chromatin structure in mouse embryonic stem cells. Stem Cells 27: 2979- 2991.
54. Shi L, Reid LH, Jones WD, Shippy R, Warrington JA, Baker SC, Collins PJ, de Longueville F, Kawasaki ES, Lee KY, Luo Y, Sun YA, Willey JC, Setterquist RA, Fischer GM, Tong W, Dragan YP, Dix DJ, Frueh FW, Goodsaid FM, Herman D, Jensen RV, Johnson CD, Lobenhofer EK, Puri RK, Schrf U, Thierry-Mieg J, Wang C, Wilson M, Wolber PK, Zhang L, Amur S, Bao W, Barbacioru CC, Lucas AB, Bertholet V, Boysen C, Bromley B, Brown D, Brunner A, Canales R, Cao XM, Cebula TA, Chen JJ, Cheng J, Chu TM, Chudin E, Corson J, Corton JC, Croner LJ, Davies C, Davison TS, Delenstarr G, Deng X, Dorris D, Eklund AC, Fan XH, Fang H, Fulmer-Smentek S, Fuscoe JC, Gallagher K, Ge W, Guo L, Guo X, Hager J, Haje PK, Han J, Han T, Harbottle HC, Harris SC, Hatchwell E, Hauser CA, Hester S, Hong H, Hurban P, Jackson SA, Ji H, Knight CR, Kuo WP, LeClerc JE, Levy S, Li QZ, Liu C, Liu Y, Lombardi MJ, Ma Y, Magnuson SR, Maqsodi B, McDaniel T, Mei N, Myklebost O, Ning B, Novoradovskaya N, Orr MS, Osborn TW, Papallo A, Patterson TA, Perkins RG, Peters EH, Peterson R, Philips KL, Pine PS, Pusztai L, Qian F, Ren H, Rosen M, Rosenzweig BA, Samaha RR, Schena M, Schroth GP, Shchegrova S, Smith DD, Staedtler F, Su Z, Sun H, Szallasi Z, Tezak Z, Thierry-Mieg D, Thompson KL, Tikhonova I, Turpaz Y, Vallanat B, Van C, Walker SJ, Wang SJ, Wang Y, Wolfinger R, Wong A, Wu J, Xiao C, Xie Q, Xu J, Yang W, Zhang L, Zhong S, Zong Y, Slikker W, Jr. 2006a. The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat Biotechnol 24: 1151- 1161.
55. Shi W, Wang H, Pan G, Geng Y, Guo Y, Pei D. 2006b. Regulation of the pluripotency marker Rex-1 by Nanog and Sox2. J Biol Chem 281: 23319- 23325.
56. Shi G, Gao F, Jin Y. 2011. The regulatory role of histone deacetylase inhibitors in Fgf4 expression is dependent on the differentiation state of pluripotent stem cells. J Cell Physiol 226: 3190- 3196.
57. Shvarts A, Brummelkamp TR, Scheeren F, Koh E, Daley GQ, Spits H, Bernards R. 2002. A senescence rescue screen identifies BCL6 as an inhibitor of anti-proliferative p19(ARF)-p53 signaling. Genes Dev 16: 681- 686.
58. Singer JD, Gurian-West M, Clurman B, Roberts JM. 1999. Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev 13: 2375- 2387.
59. Singh AM, Hamazaki T, Hankowski KE, Terada N. 2007. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25: 2534- 2542.
60. Solozobova V, Blattner C. 2011. p53 in stem cells. World J Biol Chem 2: 202- 214.
61. Tamm C, Böwer N, Annerén C. 2011. Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. J Cell Sci 124: 1136- 1144.
62. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145- 1147.
63. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116- 5121.
64. Walker E, Chang WY, Hunkapiller J, Cagney G, Garcha K, Torchia J, Krogan NJ, Reiter JF, Stanford WL. 2010. Polycomb-like 2 associates with PRC2 and regulates transcriptional networks during mouse embryonic stem cell self-renewal and differentiation. Cell Stem Cell 6: 153- 166.
65. Wang H, Mo P, Ren S, Yan C. 2010. Activating transcription factor 3 activates p53 by preventing E6-associated protein from binding to E6. J Biol Chem 285: 13201- 13210.
66. Weidenfeld-Baranboim K, Hasin T, Darlyuk I, Heinrich R, Elhanani O, Pan J, Yokoyama KK, Aronheim A. 2009. The ubiquitously expressed bZIP inhibitor, JDP2, suppresses the transcription of its homologue immediate early gene counterpart, ATF3. Nucleic Acids Res 37: 2194- 2203.
67. Zhang X, Neganova I, Przyborski S, Yang C, Cooke M, Atkinson SP, Anyfantis G, Fenyk S, Keith WN, Hoare SF, Hughes O, Strachan T, Stojkovic M, Hinds PW, Armstrong L, Lako M. 2009. A role for NANOG in G1 to S transition in human embryonic stem cells through direct binding of CDK6 and CDC25A. J Cell Biol 184: 67- 82.
68. Zhang P, Andrianakos R, Yang Y, Liu C, Lu W. 2010. Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression. J Biol Chem 285: 9180- 9189.