UHRF1 depletion causes a G 2/M arrest, activation of DNA damage response and apoptosis

Biochemical Journal

Volumn 435, Issue 1, 2011, Pages 175-185

  Tien, Amy L ^a   Senbanerjee, Sucharita ^a   Kulkarni, Atul ^b   Mudbhary, Raksha ^c   Goudreau, Bernadette ^a   Ganesan, Shridar ^b   Sadler, Kirsten C ^c   Ukomadu, Chinweike ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Caspase; Cell cycle; Methylation; Phosphorylation; Ubiquitin like protein containing PHD and RING finger domains 1 (UHRF1)

Indexed keywords

AZACITIDINE; CASPASE 3; CASPASE 8; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; HISTONE H2AX; HOMEODOMAIN PROTEIN; PROTEIN P53; PROTEIN TYROSINE PHOSPHATASE; RING FINGER PROTEIN; SERINE; UBIQUITIN; UBIQUITIN LIKE PROTEIN CONTAINING PLANT HOMEODOMAIN AND RING FINGER DOMAIN 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CELL ACTIVATION; CELL CYCLE ARREST; CELL CYCLE BLOCK; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL DIVISION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; EPIGENETICS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

APOPTOSIS; CASPASE 3; CASPASE 8; CCAAT-ENHANCER-BINDING PROTEINS; CDC2 PROTEIN KINASE; CDC25 PHOSPHATASES; CELL LINE, TUMOR; DNA DAMAGE; G2 PHASE; GENE SILENCING; HISTONES; HUMANS; IN SITU NICK-END LABELING; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; RNA, SMALL INTERFERING; ULTRAVIOLET RAYS;

EID: 79952850692     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100840     Document Type: Article

References (37)

1. Zhou, B. B. and Elledge, S. J. (2000) The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439
2. Hopfner, R., Mousli, M., Jeltsch, J. M., Voulgaris, A., Lutz, Y., Marin, C., Bellocq, J. P., Oudet, P. and Bronner, C. (2000) ICBP90, a novel human CCAAT binding protein, involved in the regulation of topoisomerase IIα expression. Cancer Res. 60, 121-128 (Pubitemid 30058741)
3. 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
4. Sharif, J., Muto, M., Takebayashi, S., 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 (Pubitemid 350231331)
5. 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 (Pubitemid 39424918)
6. 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
7. Citterio, E., Papait, R., Nicassio, F., Vecchi, M., Gomiero, P., Mantovani, R., Di Fiore, P. P. and Bonapace, I. M. (2004) Np95 is a histone-binding protein endowed with ubiquitin ligase activity. Mol. Cell. Biol. 24, 2526-2535
8. Hashimoto, H., Horton, J. R., Zhang, X. and Cheng, X. (2009) UHRF1, a modular multi-domain protein, regulates replication-coupled crosstalk between DNA methylation and histone modifications. Epigenetics 4, 8-14
9. Karagianni, P., Amazit, L., Qin, J. and Wong, J. (2008) ICBP90, a novel methyl K9 H3 binding protein linking protein ubiquitination with heterochromatin formation. Mol. Cell. Biol. 28, 705-717
10. 1/S transition during the cell cycle. Oncogene 24, 7337-7345
11. 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 hemimethylated DNA by the SRA domain of human UHRF1. Nature 455, 822-825
12. 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
13. Arita, K., Ariyoshi, M., Tochio, H., Nakamura, Y. and Shirakawa, M. (2008) Recognition of hemimethylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455, 818-821
14. Jenkins, Y., Markovtsov, V., Lang, W., Sharma, P., Pearsall, D., Warner, J., Franci, C., Huang, B., Huang, J., Yam, G. C. et al. (2005) Critical role of the ubiquitin ligase activity of UHRF1, a nuclear RING finger protein, in tumor cell growth. Mol. Biol. Cell 16, 5621-5629
15. 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. U.S.A. 104, 1570-1575
16. Mousli, M., Hopfner, R., Abbady, A. Q., Monte, D., Jeanblanc, M., Oudet, P., Louis, B. and Bronner, C. (2003) ICBP90 belongs to a new family of proteins with an expression that is deregulated in cancer cells. Br. J. Cancer 89, 120-127 (Pubitemid 36897947)
17. Bonapace, I. M., Latella, L., Papait, R., Nicassio, F., Sacco, A., Muto, M., Crescenzi, M. and Di Fiore, P. P. (2002) Np95 is regulated by E1A during mitotic reactivation of terminally differentiated cells and is essential for S-phase entry. J. Cell Biol. 157, 909-914 (Pubitemid 34839765)
18. 1/S transition. Genes Cells 9, 131-142
19. 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
20. Mortusewicz, O., Schermelleh, L., Walter, J., Cardoso, M. C. and Leonhardt, H. (2005) Recruitment of DNA methyltransferase I to DNA repair sites. Proc. Natl. Acad. Sci. U.S.A. 102, 8905-8909
21. 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
22. Ukomadu, C. and Dutta, A. (2003) Inhibition of cdk2 activating phosphorylation by mevastatin. J. Biol. Chem. 278, 4840-4846
23. Morgan, D. O. (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261-291
24. Glotzer, M. (1995) Cell cycle. The only way out of mitosis. Curr. Biol. 5, 970-972
25. Matsuoka, S., Rotman, G., Ogawa, A., Shiloh, Y., Tamai, K. and Elledge, S. J. (2000) Ataxia telangiectasia-mutated phosphorylates Chk2 in vivoand in vitro. Proc. Natl. Acad. Sci. U.S.A. 97, 10389-10394
26. 2/M checkpoint. Mol. Cell. Biol. 24, 7140-7150
27. Shieh, S. Y., Ikeda, M., Taya, Y. and Prives, C. (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91, 325-334 (Pubitemid 27467963)
28. Hirao, A., Kong, Y. Y., Matsuoka, S., Wakeham, A., Ruland, J., Yoshida, H., Liu, D., Elledge, S. J. and Mak, T. W. (2000) DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287, 1824-1827
29. 20, requires tetramerization. EMBO J. 18, 1815-1823
30. Deyoung, M. P. and Ellisen, L. W. (2007) p63 and p73 in human cancer: defining the network. Oncogene 26, 5169-5183
31. Sidi, S., Sanda, T., Kennedy, R. D., Hagen, A. T., Jette, C. A., Hoffmans, R., Pascual, J., Imamura, S., Kishi, S., Amatruda, J. F. et al. (2008) Chk1 suppresses a caspase 2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase 3. Cell 133, 864-877 (Pubitemid 351715394)
32. Afshar, G., Jelluma, N., Yang, X., Basila, D., Arvold, N. D., Karlsson, A., Yount, G. L., Dansen, T. B., Koller, E. and Haas-Kogan, D. A. (2006) Radiation-induced caspase 8 mediates p53-independent apoptosis in glioma cells. Cancer Res. 66, 4223-4232
33. Zhu, M. and Weiss, R. S. (2007) Increased common fragile site expression, cell proliferation defects, and apoptosis following conditional inactivation of mouse Hus1 in primary cultured cells. Mol. Biol. Cell 18, 1044-1055
34. Liu, S., Bekker-Jensen, S., Mailand, N., Lukas, C., Bartek, J. and Lukas, J. (2006) Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol. 26, 6056-6064
35. Puc, J. and Parsons, R. (2005) PTEN loss inhibits CHK1 to cause double stranded-DNA breaks in cells. Cell Cycle 4, 927-929 (Pubitemid 41359759)
36. Brown, K. D. and Robertson, K. D. (2007) DNMT1 knockout delivers a strong blow to genome stability and cell viability. Nat. Genet. 39, 289-290
37. Mistry, H., Gibson, L., Yun, J. W., Sarras, H., Tamblyn, L. and McPherson, J. P. (2008) Interplay between Np95 and Eme1 in the DNA damage response. Biochem. Biophys. Res. Commun. 375, 321-325