The PR-Set7 binding domain of Riz1 is required for the H4K20me1-H3K9me1 trans-tail 'histone code' and Riz1 tumor suppressor function

Nucleic Acids Research

Volumn 42, Issue 6, 2014, Pages 3580-3589

  Congdon, Lauren M ^a   Sims, Jennifer K ^a   Tuzon, Creighton T ^a   Rice, Judd C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL LINE, TUMOR; CELL NUCLEUS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HISTONE CODE; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84898950576     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1377     Document Type: Article

References (32)

1. Jenuwein, T. and Allis, C. D. (2001) Translating the histone code. Science, 293, 1074-1080.
2. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315-326.
3. Sims, J. K., Houston, S. I., Magazinnik, T. and Rice, J. C. (2006) A trans-tail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J. Biol. Chem., 281, 12760-12766.
4. Sims, J. K. and Rice, J. C. (2008) PR-Set7 establishes a repressive trans-tail histone code that regulates differentiation. Mol. Cell. Biol., 28, 4459-4468.
5. Spektor, T. M., Congdon, L. M., Veerappan, C. S. and Rice, J. C. (2011) The UBC9 E2 SUMO conjugating enzyme binds the PRSet7 histone methyltransferase to facilitate target gene repression. PLoS One, 6, e22785.
6. Houston, S. I., McManus, K. J., Adams, M. M., Sims, J. K., Carpenter, P. B., Hendzel, M. J. and Rice, J. C. (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J. Biol. Chem., 283, 19478-19488.
7. Wu, S., Wang, W., Kong, X., Congdon, L. M., Yokomori, K., Kirschner, M. W. and Rice, J. C. (2010) Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev., 24, 2531-2542.
8. Ishizuka, T. and Lazar, M. A. (2003) The N-CoR/histone deacetylase 3 complex is required for repression by thyroid hormone receptor. Mol. Cell. Biol., 23, 5122-5131.
9. Hitchler, M. J. and Rice, J. C. (2011) Genome-wide epigenetic analysis of human pluripotent stem cells by ChIP and ChIP-Seq. Methods Mol. Biol., 767, 253-267.
10. Shinkai, Y. and Tachibana, M. (2011) H3K9 methyltransferase G9a and the related molecule GL P. Genes Dev., 25, 781-788.
11. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. and Rauscher, F. J. III (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zincfinger proteins. Genes Dev., 16, 919-932.
12. Kim, K. C., Geng, L. and Huang, S. (2003) Inactivation of a histone methyltransferase by mutations in human cancers. Cancer Res., 63, 7619-7623.
13. Huang, S., Shao, G. and Liu, L. (1998) The PR domain of the Rb-binding zinc finger protein RIZ1 is a protein binding interface and is related to the SET domain functioning in chromatin-mediated gene expression. J. Biol. Chem., 273, 15933-15939.
14. Yokochi, T., Poduch, K., Ryba, T., Lu, J., Hiratani, I., Tachibana, M., Shinkai, Y. and Gilbert, D. M. (2009) G9a selectively represses a class of late-replicating genes at the nuclear periphery. Proc. Natl Acad. Sci. USA, 106, 19363-19368.
15. Liu, L., Shao, G., Steele-Perkins, G. and Huang, S. (1997) The retinoblastoma interacting zinc finger gene RIZ produces a PR domain-lacking product through an internal promoter. J. Biol. Chem., 272, 2984-2991.
16. Congdon, L. M., Houston, S. I., Veerappan, C. S., Spektor, T. M. and Rice, J. C. (2010) PR-Set7-mediated monomethylation of histone H4 lysine 20 at specific genomic regions induces transcriptional repression. J. Cell. Biochem., 110, 609-619.
17. Xie, M., Shao, G., Buyse, I. M. and Huang, S. (1997) Transcriptional repression mediated by the PR domain zinc finger gene RI Z. J. Biol. Chem., 272, 26360-26366.
18. Steele-Perkins, G., Fang, W., Yang, X. H., Van Gele, M., Carling, T., Gu, J., Buyse, I. M., Fletcher, J. A., Liu, J., Bronson, R. et al. (2001) Tumor formation and inactivation of RIZ1, an Rb-binding member of a nuclear protein-methyltransferase superfamily. Genes Dev., 15, 2250-2262.
19. Chadwick, R. B., Jiang, G. L., Bennington, G. A., Yuan, B., Johnson, C. K., Stevens, M. W., Niemann, T. H., Peltomaki, P., Huang, S. and de la Chapelle, A. (2000) Candidate tumor suppressor RIZ is frequently involved in colorectal carcinogenesis. Proc. Natl Acad. Sci. USA, 97, 2662-2667.
20. He, L., Yu, J. X., Liu, L., Buyse, I. M., Wang, M. S., Yang, Q. C., Nakagawara, A., Brodeur, G. M., Shi, Y. E. and Huang, S. (1998) RIZ1, but not the alternative RIZ2 product of the same gene, is underexpressed in breast cancer, and forced RIZ1 expression causes G2-M cell cycle arrest and/or apoptosis. Cancer Res., 58, 4238-4244.
21. Liu, Z. Y., Wang, J. Y., Liu, H. H., Ma, X. M., Wang, C. L., Zhang, X. P., Tao, Y. Q., Lu, Y. C., Liao, J. C. and Hu, G. H. (2012) Retinoblastoma protein-interacting zinc-finger gene 1 (RIZ1) dysregulation in human malignant meningiomas. Oncogene, 32, 1216-1222.
22. Jiang, G., Liu, L., Buyse, I. M., Simon, D. and Huang, S. (1999) Decreased RIZ1 expression but not RIZ2 in hepatoma and suppression of hepatoma tumorigenicity by RIZ1. Int. J. Cancer, 83, 541-546.
23. Piao, Z., Fang, W., Malkhosyan, S., Kim, H., Horii, A., Perucho, M. and Huang, S. (2000) Frequent frameshift mutations of RIZ in sporadic gastrointestinal and endometrial carcinomas with microsatellite instability. Cancer Res., 60, 4701-4704.
24. Sakurada, K., Furukawa, T., Kato, Y., Kayama, T., Huang, S. and Horii, A. (2001) RIZ, the retinoblastoma protein interacting zinc finger gene, is mutated in genetically unstable cancers of the pancreas, stomach, and colorectum. Genes Chromosomes Cancer, 30, 207-211.
25. Poetsch, M., Dittberner, T. and Woenckhaus, C. (2002) Frameshift mutations of RIZ, but no point mutations in RIZ1 exons in malignant melanomas with deletions in 1p36. Oncogene, 21, 3038-3042.
26. Kalakonda, N., Fischle, W., Boccuni, P., Gurvich, N., Hoya-Arias, R., Zhao, X., Miyata, Y., Macgrogan, D., Zhang, J., Sims, J. K. et al. (2008) Histone H4 lysine 20 monomethylation promotes transcriptional repression by L3MBTL1. Oncogene, 27, 4293-4304.
27. Li, Y., Sun, L., Zhang, Y., Wang, D., Wang, F., Liang, J., Gui, B. and Shang, Y. (2011) The histone modifications governing TFF1 transcription mediated by estrogen receptor. J. Biol. Chem., 286, 13925-13936.
28. Carling, T., Kim, K. C., Yang, X. H., Gu, J., Zhang, X. K. and Huang, S. (2004) A histone methyltransferase is required for maximal response to female sex hormones. Mol. Cell. Biol., 24, 7032-7042.
29. Jiang, G. L. and Huang, S. (2001) Adenovirus expressing RIZ1 in tumor suppressor gene therapy of microsatellite-unstable colorectal cancers. Cancer Res., 61, 1796-1798.
30. Wu, S. and Rice, J. C. (2011) A new regulator of the cell cycle: the PR-Set7 histone methyltransferase. Cell Cycle, 10, 68-72.
31. Tardat, M., Brustel, J., Kirsh, O., Lefevbre, C., Callanan, M., Sardet, C. and Julien, E. (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol., 12, 1086-1093.
32. Tardat, M., Murr, R., Herceg, Z., Sardet, C. and Julien, E. (2007) PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J. Cell Biol., 179, 1413-1426.