Dna hypomethylation induces a dna replication-associated cell cycle arrest to block hepatic outgrowth in uhrf1 mutant zebrafish embryos

Development (Cambridge)

Volumn 142, Issue 3, 2015, Pages 510-521

  Jacob, Vinitha ^a   Chernyavskaya, Yelena ^a   Chen, Xintong ^a   Tan, Poh Seng ^a,b   Kent, Brandon ^a   Hoshida, Yujin ^a   Sadler, Kirsten C ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

Author keywords

DNA methylation; DNA replication; Hepatic outgrowth; Liver development; UHRF1; Zebrafish

Indexed keywords

BROXURIDINE; TRANSACTIVATOR PROTEIN; UHRF1 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRDU ASSAY; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA CONTENT; DNA DETERMINATION; DNA METHYLATION; DNA REPLICATION; DNMT1 GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; GENE MUTATION; LIVER CELL; LIVER DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; UHRF1 GENE; ZEBRA FISH; ANIMAL; CELL CYCLE CHECKPOINT; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; LIVER; NONMAMMALIAN EMBRYO; NONPARAMETRIC TEST; PHYSIOLOGY; TUNEL ASSAY;

DANIO RERIO;

ANIMALS; APOPTOSIS; BROMODEOXYURIDINE; CELL CYCLE CHECKPOINTS; DNA METHYLATION; DNA REPLICATION; EMBRYO, NONMAMMALIAN; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; IN SITU NICK-END LABELING; LIVER; STATISTICS, NONPARAMETRIC; TRANS-ACTIVATORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84921444088     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.115980     Document Type: Article

References (51)

1. Achour, M., Fuhrmann, G., Alhosin, M., Ronde, P., Chataigneau, T., Mousli, M., Schini-Kerth, V. B. and Bronner, C. (2009). UHRF1 recruits the histone acetyltransferase Tip60 and controls its expression and activity. Biochem. Biophys. Res. Commun. 390, 523-528.
2. Amsterdam, A., Nissen, R. M., Sun, Z., Swindell, E. C., Farrington, S. and Hopkins, N. (2004). Identification of 315 genes essential for early zebrafish development. Proc. Natl. Acad. Sci. USA 101, 12792-12797.
3. Anderson, R. M., Bosch, J. A., Goll, M. G., Hesselson, D., Dong, P. D. S., Shin, D., Chi, N. C., Shin, C. H., Schlegel, A., Halpern, M. et al. (2009). Loss of Dnmt1 catalytic activity reveals multiple roles for DNA methylation during pancreas development and regeneration. Dev. Biol. 334, 213-223.
4. Arima, Y., Hirota, T., Bronner, C., Mousli, M., Fujiwara, T., Niwa, S.-i., Ishikawa, H. and Saya, H. (2004). Down-regulation of nuclear protein ICBP90 by p53/ p21Cip1/WAF1-dependent DNA-damage checkpoint signals contributes to cell cycle arrest at G1/S transition. Genes Cells 9, 131-142.
5. Arita, K., Ariyoshi, M., Tochio, H., Nakamura, Y. and Shirakawa, M. (2008). Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455, 818-821.
6. Avvakumov, G.V., Walker, J.R., Xue, S., Li, Y., Duan, S., Bronner, C., Arrowsmith, C. H. and Dhe-Paganon, S. (2008). Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455, 822-825.
7. Bashtrykov, P., Jankevicius, G., Jurkowska, R. Z., Ragozin, S. and Jeltsch, A. (2014). The UHRF1 protein stimulates the activity and specificity of the maintenance DNA methyltransferase DNMT1 by an allosteric mechanism. J. Biol. Chem. 289, 4106-4115.
8. Berkyurek, A. C., Suetake, I., Arita, K., Takeshita, K., Nakagawa, A., Shirakawa, M. and Tajima, S. (2014). The DNA methyltransferase Dnmt1 directly interacts with the SET and RING finger-associated (SRA) domain of the multifunctional protein Uhrf1 to facilitate accession of the catalytic center to hemi-methylated DNA. J. Biol. Chem. 289, 379-386.
9. Biniszkiewicz, D., Gribnau, J., Ramsahoye, B., Gaudet, F., Eggan, K., Humpherys, D., Mastrangelo, M.-A., Jun, Z., Walter, J. and Jaenisch, R. (2002). Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol. Cell. Biol. 22, 2124-2135.
10. Bostick, M., Kim, J. K., Esteve, P.-O., Clark, A., Pradhan, S. and Jacobsen, S. E. (2007). UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317, 1760-1764.
11. Chen, T., Hevi, S., Gay, F., Tsujimoto, N., He, T., Zhang, B., Ueda, Y. and Li, E. (2007). Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet. 39, 391-396.
12. Cheng, J., Yang, Y., Fang, J., Xiao, J., Zhu, T., Chen, F., Wang, P., Li, Z., Yang, H. and Xu, Y. (2013). Structural insight into coordinated recognition of trimethylated histone H3 lysine 9 (H3K9me3) by the plant homeodomain (PHD) and tandem tudor domain (TTD) of UHRF1 (ubiquitin-like, containing PHD and RING finger domains, 1) protein. J. Biol. Chem. 288, 1329-1339.
13. Chu, J., Loughlin, E. A., Gaur, N. A., SenBanerjee, S., Jacob, V., Monson, C., Kent, B., Oranu, A., Ding, Y., Ukomadu, C. et al. (2012). UHRF1 phosphorylation by cyclin A2/cyclin-dependent kinase 2 is required for zebrafish embryogenesis. Mol. Biol. Cell 23, 59-70.
14. Dong, P. D. S., Munson, C. A., Norton, W., Crosnier, C., Pan, X., Gong, Z., Neumann, C. J. and Stainier, D. Y. R. (2007). Fgf10 regulates hepatopancreatic ductal system patterning and differentiation. Nat. Genet. 39, 397-402.
15. Dorn, E. S. and Cook, J. G. (2011). Nucleosomes in the neighborhood: new roles for chromatin modifications in replication origin control. Epigenetics 6, 552-559.
16. Dovey, M., Patton, E. E., Bowman, T., North, T., Goessling, W., Zhou, Y. and Zon, L. I. (2009). Topoisomerase II alpha is required for embryonic development and liver regeneration in zebrafish. Mol. Cell. Biol. 29, 3746-3753.
17. Du, Z., Song, J., Wang, Y., Zhao, Y., Guda, K., Yang, S., Kao, H.-Y., Xu, Y., Willis, J., Markowitz, S. D. et al. (2010). DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation-driven ubiquitination. Sci. Signal. 3, ra80.
18. Feng, S., Cokus, S. J., Zhang, X., Chen, P.-Y., Bostick, M., Goll, M. G., Hetzel, J., Jain, J., Strauss, S. H., Halpern, M. E. et al. (2010). Conservation and divergence of methylation patterning in plants and animals. Proc. Natl. Acad. Sci. USA 107, 8689-8694.
19. Hashimoto, H., Horton, J. R., Zhang, X., Bostick, M., Jacobsen, S. E. and Cheng, X. (2008). The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455, 826-829.
20. Hervouet, E., Lalier, L., Debien, E., Cheray, M., Geairon, A., Rogniaux, H., Loussouarn, D., Martin, S. A., Vallette, F. M. and Cartron, P.-F. (2010). Disruption of Dnmt1/PCNA/UHRF1 interactions promotes tumorigenesis from human and mice glial cells. PLoS ONE 5, e11333.
21. Hopfner, R., Mousli, M., Oudet, P. and Bronner, C. (2002). Overexpression of ICBP90, a novel CCAAT-binding protein, overcomes cell contact inhibition by forcing topoisomerase II alpha expression. Anticancer Res. 22, 3165-3170.
22. Jacob, Y., Stroud, H., LeBlanc, C., Feng, S., Zhuo, L., Caro, E., Hassel, C., Gutierrez, C., Michaels, S. D. and Jacobsen, S. E. (2010). Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466, 987-991.
23. Jegu, T., Latrasse, D., Delarue, M., Mazubert, C., Bourge, M., Hudik, E., Blanchet, S., Soler, M.-N., Charon, C., De Veylder, L. et al. (2013). Multiple functions of Kip-related protein5 connect endoreduplication and cell elongation. Plant Physiol. 161, 1694-1705.
24. Karpf, A. R. and Matsui, S.-i. (2005). Genetic disruption of cytosine DNA methyltransferase enzymes induces chromosomal instability in human cancer cells. Cancer Res. 65, 8635-8639.
25. Kim, J. K., Esteve, P.-O., Jacobsen, S. E. and Pradhan, S. (2009). UHRF1 binds G9a and participates in p21 transcriptional regulation in mammalian cells. Nucleic Acids Res. 37, 493-505.
26. Li, X., Meng, Q., Rosen, E. M. and Fan, S. (2011). UHRF1 confers radioresistance to human breast cancer cells. Int. J. Radiat. Biol. 87, 263-273.
27. Milutinovic, S., Zhuang, Q., Niveleau, A. and Szyf, M. (2003). Epigenomic stress response: knockdown of DNA methyltransferase 1 triggers an intra-S-phase arrest of DNA replication and induction of stress response genes. J. Biol. Chem. 278, 14985-14995.
28. Milutinovic, S., Brown, S. E., Zhuang, Q. and Szyf, M. (2004). DNA methyltransferase 1 knock down induces gene expression by a mechanism independent of DNA methylation and histone deacetylation. J. Biol. Chem. 279, 27915-27927.
29. Mistry, H., Tamblyn, L., Butt, H., Sisgoreo, D., Gracias, A., Larin, M., Gopalakrishnan, K., Hande, M. P. and McPherson, J. P. (2010). UHRF1 is a genome caretaker that facilitates the DNA damage response to gamma-irradiation. Genome Integr. 1, 7.
30. Mudbhary, R. and Sadler, K. C. (2011). Epigenetics, development, and cancer: zebrafish make their mark. Birth Defects Res. C Embryo Today 93, 194-203.
31. Mudbhary, R., Hoshida, Y., Chernyavskaya, Y., Jacob, V., Villanueva, N., Fiel, M. I., Chen, X., Kojima, K., Thung, S., Bronson, R. T. et al. (2014). UHRF1 overexpression drives DNA hypomethylation and hepatocellular carcinoma. Cancer Cell 25, 196-209.
32. Muto, M., Kanari, Y., Kubo, E., Takabe, T., Kurihara, T., Fujimori, A. and Tatsumi, K. (2002). Targeted disruption of Np95 gene renders murine embryonic stem cells hypersensitive to DNA damaging agents and DNA replication blocks. J. Biol. Chem. 277, 34549-34555.
33. Nishiyama, A., Yamaguchi, L., Sharif, J., Johmura, Y., Kawamura, T., Nakanishi, K., Shimamura, S., Arita, K., Kodama, T., Ishikawa, F. et al. (2013). Uhrf1-dependent H3K23 ubiquitylation couples maintenance DNA methylation and replication. Nature 502, 249-253.
34. Obata, Y., Furusawa, Y., Endo, T. A., Sharif, J., Takahashi, D., Atarashi, K., Nakayama, M., Onawa, S., Fujimura, Y., Takahashi, M. et al. (2014). The epigenetic regulator Uhrf1 facilitates the proliferation and maturation of colonic regulatory T cells. Nat. Immunol. 15, 571-579.
35. Papait, R., Pistore, C., Grazini, U., Babbio, F., Cogliati, S., Pecoraro, D., Brino, L., Morand, A.-L., Dechampesme, A.-M., Spada, F. et al. (2008). The PHD domain of Np95 (mUHRF1) is involved in large-scale reorganization of pericentromeric heterochromatin. Mol. Biol. Cell 19, 3554-3563.
36. Qian, C., Li, S., Jakoncic, J., Zeng, L., Walsh, M. J. and Zhou, M.-M. (2008). Structure and hemimethylated CpG binding of the SRA domain from human UHRF1. J. Biol. Chem. 283, 34490-34494.
37. Qin, W., Leonhardt, H. and Spada, F. (2011). Usp7 and Uhrf1 control ubiquitination and stability of the maintenance DNA methyltransferase Dnmt1. J. Cell. Biochem. 112, 439-444.
38. Reich, M., Liefeld, T., Gould, J., Lerner, J., Tamayo, P. and Mesirov, J. P. (2006). GenePattern 2.0. Nat. Genet. 38, 500-501.
39. Rottach, A., Frauer, C., Pichler, G., Bonapace, I. M., Spada, F. and Leonhardt, H. (2010). The multi-domain protein Np95 connects DNA methylation and histone modification. Nucleic Acids Res. 38, 1796-1804.
40. Sadler, K. C., Krahn, K. N., Gaur, N. A. and Ukomadu, C. (2007). Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. Proc. Natl. Acad. Sci. USA 104, 1570-1575.
41. Sharif, J., Muto, M., Takebayashi, S.-i., Suetake, I., Iwamatsu, A., Endo, T. A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K. et al. (2007). The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912.
42. Stroud, H., Hale, C. J., Feng, S., Caro, E., Jacob, Y., Michaels, S. D. and Jacobsen, S. E. (2012). DNA methyltransferases are required to induce heterochromatic re-replication in Arabidopsis. PLoS Genet. 8, e1002808.
43. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S. et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550.
44. Taylor, E. M., Bonsu, N. M., Price, R. J. and Lindsay, H. D. (2013). Depletion of Uhrf1 inhibits chromosomal DNA replication in Xenopus egg extracts. Nucleic Acids Res. 41, 7725-7737.
45. Tien, A. L., Senbanerjee, S., Kulkarni, A., Mudbhary, R., Goudreau, B., Ganesan, S., Sadler, K.C. and Ukomadu, C.(2011). UHRF1 depletion causesaG2/M arrest, activation of DNA damage response and apoptosis. Biochem. J. 435, 175-185.
46. Tittle, R. K., Sze, R., Ng, A., Nuckels, R. J., Swartz, M. E., Anderson, R. M., Bosch, J., Stainier, D. Y. R., Eberhart, J. K. and Gross, J. M. (2011). Uhrf1 and Dnmt1 are required for development and maintenance of the zebrafish lens. Dev. Biol. 350, 50-63.
47. Truong, L. N. and Wu, X. (2011). Prevention of DNA re-replication in eukaryotic cells. J. Mol. Cell Biol. 3, 13-22.
48. Unoki, M., Nishidate, T. and Nakamura, Y. (2004). ICBP90, an E2F-1 target, recruits HDAC1 and binds to methyl-CpG through its SRA domain. Oncogene 23, 7601-7610.
49. Unterberger, A., Andrews, S. D., Weaver, I. C. G. and Szyf, M. (2006). DNA methyltransferase 1 knockdown activates a replication stress checkpoint. Mol. Cell. Biol. 26, 7575-7586.
50. Vijayaraghavalu, S., Dermawan, J. K., Cheriyath, V. and Labhasetwar, V. (2013). Highly synergistic effect of sequential treatment with epigenetic and anticancer drugs to overcome drug resistance in breast cancer cells is mediated via activation of p21 gene expression leading to G2/M cycle arrest. Mol. Pharm. 10, 337-352.
51. Xie, S., Jakoncic, J. and Qian, C. (2012). UHRF1 double tudor domain and the adjacent PHD finger act together to recognize K9me3-containing histone H3 tail. J. Mol. Biol. 415, 318-328.