Epigenetic regulation of mir-302 by jmjd1c inhibits neural differentiation of human embryonic stem cells

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2384-2395

  Wang, Jianle ^a   Park, Jung W ^a   Drissi, Hicham ^a   Wang, Xiaofang ^a   Xu, Ren He ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEMETHYLASE; EMBRYONIC STEM CELLS; EPIGENETIC REGULATION; HISTONE METHYLATION; HUMAN EMBRYONIC STEM CELLS; NEURAL DIFFERENTIATIONS;

ALKYLATION;

CELL GROWTH;

BONE MORPHOGENETIC PROTEIN; HISTONE DEMETHYLASE; MICRORNA; MICRORNA 302; PROTEIN JMJD1C; SHORT HAIRPIN RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; ENZYME INHIBITION; EPIGENETIC REPRESSION; GENE SILENCING; HISTONE METHYLATION; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION;

EMBRYONIC STEM CELL; EPIGENETICS; HISTONE METHYLATION; MICRORNA; NEURODIFFERENTIATION;

BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINE; COUP TRANSCRIPTION FACTOR I; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FIBROBLAST GROWTH FACTOR 2; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MICRORNAS; NEURONS; OXIDOREDUCTASES, N-DEMETHYLATING; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84893109030     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.535799     Document Type: Article

References (38)

1. Greer, E. L., and Shi, Y. (2012) Histone methylation. A dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 13, 343-357
2. Black, J. C., Van Rechem, C., and Whetstine, J. R. (2012) Histone lysine methylation dynamics. Establishment, regulation, and biological impact. Mol. Cell 48, 491-507
3. Kooistra, S. M., and Helin, K. (2012) Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol. 13, 297-311
4. Loh, Y. H., Zhang, W., Chen, X., George, J., and Ng, H. H. (2007) Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev. 21, 2545-2557
5. Wang, J., Zhang, M., Zhang, Y., Kou, Z., Han, Z., Chen, D. Y., Sun, Q. Y., and Gao, S. (2010) The histone demethylase JMJD2C is stage-specifically expressed in preimplantation mouse embryos and is required for embryonic development. Biol. Reprod. 82, 105-111
6. Wang, T., Chen, K., Zeng, X., Yang, J., Wu, Y., Shi, X., Qin, B., Zeng, L., Esteban, M. A., Pan, G., and Pei, D. (2011) The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9, 575-587
7. Kim, S. M., Kim, J. Y., Choe, N. W., Cho, I. H., Kim, J. R., Kim, D. W., Seol, J. E., Lee, S. E., Kook, H., Nam, K. I., Kook, H., Bhak, Y. Y., and Seo, S. B. (2010) Regulation of mouse steroidogenesis by WHISTLE and JMJD1C through histone methylation balance. Nucleic Acids Res. 38, 6389-6403
8. Xu, R. H., Chen, X., Li, D. S., Li, R., Addicks, G. C., Glennon, C., Zwaka, T. P., and Thomson, J. A. (2002) BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 20, 1261-1264
9. Xu, R. H., Sampsell-Barron, T. L., Gu, F., Root, S., Peck, R. M., Pan, G., Yu, J., Antosiewicz-Bourget, J., Tian, S., Stewart, R., and Thomson, J. A. (2008) NANOG is a direct target of TGFβ/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3, 196-206
10. Katoh, M., and Katoh, M. (2007) Comparative integromics on JMJD1C gene encoding histone demethylase. Conserved POU5F1 binding site elucidating mechanism of JMJD1C expression in undifferentiated ES cells and diffuse-type gastric cancer. Int. J. Oncol. 31, 219-223
11. Greber, B., Coulon, P., Zhang, M., Moritz, S., Frank, S., Müller-Molina, A. J., Araüzo-Bravo, M. J., Han, D. W., Pape, H. C., and Schöler, H. R. (2011) FGF signalling inhibits neural induction in human embryonic stem cells. EMBO J. 30, 4874-4884
12. Rosa, A., and Brivanlou, A. H. (2011) A regulatory circuitry comprised of miR-302 and the transcription factors OCT4 and NR2F2 regulates human embryonic stem cell differentiation. EMBO J. 30, 237-248
13. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., and Jones, J. M. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147
14. Lin, G., Martins-Taylor, K., and Xu, R. H. (2010) Human embryonic stem cell derivation, maintenance, and differentiation to trophoblast. Methods Mol. Biol. 636, 1-24
15. Xu, C., Inokuma, M. S., Denham, J., Golds, K., Kundu, P., Gold, J. D., and Carpenter, M. K. (2001) Feeder-free growth of undifferentiated human embryonic stem cells. Nat. Biotechnol. 19, 971-974
16. Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., and Thomson, J. A. (2006) Feeder-independent culture of human embryonic stem cells. Nat. Methods 3, 637-646
17. Zhang, S. C., Wernig, M., Duncan, I. D., Brüstle, O., and Thomson, J. A. (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133
18. Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., and Studer, L. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280
19. Müller, F. J., Schuldt, B. M., Williams, R., Mason, D., Altun, G., Papapetrou, E. P., Danner, S., Goldmann, J. E., Herbst, A., Schmidt, N. O., Aldenhoff, J. B., Laurent, L. C., and Loring, J. F. (2011) A bioinformatic assay for pluripotency in human cells. Nat. Methods 8, 315-317
20. Kim, S. W., Li, Z., Moore, P. S., Monaghan, A. P., Chang, Y., Nichols, M., and John, B. (2010) A sensitive non-radioactive Northern blot method to detect small RNAs. Nucleic Acids Res. 38, e98
21. Lienert, F., Mohn, F., Tiwari, V. K., Baubec, T., Roloff, T. C., Gaidatzis, D., Stadler, M. B., and Schübeler, D. (2011) Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLoS Genet. 7, e1002090
22. Barroso-delJesus, A., Romero-López, C., Lucena-Aguilar, G., Melen, G. J., Sanchez, L., Ligero, G., Berzal-Herranz, A., and Menendez, P. (2008) Embryonic stem cell-specific miR302-367 cluster. Human gene structure and functional characterization of its core promoter. Mol. Cell Biol. 28, 6609-6619
23. Card, D. A., Hebbar, P. B., Li, L., Trotter, K. W., Komatsu, Y., Mishina, Y., and Archer, T. K. (2008) Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol. Cell Biol. 28, 6426-6438
24. Miyazono, K. (2000) Positive and negative regulation of TGF-β signaling. J. Cell Sci. 113, 1101-1109
25. Kawabata, M., Chytil, A., and Moses, H. L. (1995) Cloning of a novel type II serine/threonine kinase receptor through interaction with the type I transforming growth factor-β receptor. J. Biol. Chem. 270, 5625-5630
26. Katoh, M. (2006) CER1 is a common target of WNT and NODAL signaling pathways in human embryonic stem cells. Int. J. Mol. Med. 17, 795-799
27. Besser, D. (2004) Expression of nodal, lefty-a, and lefty-B in undifferentiated human embryonic stem cells requires activation of Smad2/3. J. Biol. Chem. 279, 45076-45084
28. Lipchina, I., Elkabetz, Y., Hafner, M., Sheridan, R., Mihailovic, A., Tuschl, T., Sander, C., Studer, L., and Betel, D. (2011) Genome-wide identification of microRNA targets in human ES cells reveals a role for miR-302 in modulating BMP response. Genes Dev. 25, 2173-2186
29. Anokye-Danso, F., Trivedi, C. M., Juhr, D., Gupta, M., Cui, Z., Tian, Y., Zhang, Y., Yang, W., Gruber, P. J., Epstein, J. A., and Morrisey, E. E. (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8, 376-388
30. Subramanyam, D., Lamouille, S., Judson, R. L., Liu, J. Y., Bucay, N., Derynck, R., and Blelloch, R. (2011) Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat. Biotechnol. 29, 443-448
31. Barroso-delJesus, A., Lucena-Aguilar, G., Sanchez, L., Ligero, G., Gutierrez-Aranda, I., and Menendez, P. (2011) The Nodal inhibitor Lefty is negatively modulated by the microRNA miR-302 in human embryonic stem cells. FASEB J. 25, 1497-1508
32. Wen, S., Li, H., and Liu, J. (2009) Epigenetic background of neuronal fate determination. Prog. Neurobiol. 87, 98-117
33. Coskun, V., Tsoa, R., and Sun, Y. E. (2012) Epigenetic regulation of stem cells differentiating along the neural lineage. Curr. Opin. Neurobiol. 22, 762-767
34. Xu, C., Rosler, E., Jiang, J., Lebkowski, J. S., Gold, J. D., O'Sullivan, C., Delavan-Boorsma, K., Mok, M., Bronstein, A., and Carpenter, M. K. (2005) Basic fibroblast growth factor supports undifferentiated human embryonic stem cell growth without conditioned medium. Stem Cells 23, 315-323
35. Wang, X., Lin, G., Martins-Taylor, K., Zeng, H., and Xu, R. H. (2009) Inhibition of caspase-mediated anoikis is critical for basic fibroblast growth factor-sustained culture of human pluripotent stem cells. J. Biol. Chem. 284, 34054-34064
36. Jaenisch, R., and Young, R. (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582
37. Castermans,D., Vermeesch, J. R., Fryns, J. P., Steyaert, J. G., Van de Ven, W. J., Creemers, J. W., and Devriendt, K. (2007) Identification and characterization of the TRIP8 and REEP3 genes on chromosome 10q21.3 as novel candidate genes for autism. Eur. J. Hum. Genet. 15, 422-431
38. Lipchina, I., Studer, L., and Betel, D. (2012) The expanding role of miR-302-367 in pluripotency and reprogramming. Cell Cycle 11, 1517-1523