Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1

Molecular and Cellular Biology

Volumn 25, Issue 23, 2005, Pages 10338-10351

  Duan, Zhijun ^a   Zarebski, Adrian ^b   Montoya Durango, Diego ^b   Grimes, H Leighton ^b   Horwitz, Marshall ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; GROWTH FACTOR INDEPENDENT 1; HISTONE DEACETYLASE 1; HISTONE LYSINE METHYLTRANSFERASE; ONCOPROTEIN; PROTEIN G9A; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BONE MARROW CELL; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DEMETHYLATION; DNA MODIFICATION; ENZYME MODIFICATION; EPIGENETICS; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; INNER EAR; NEUROSECRETORY CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION;

CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HISTOCOMPATIBILITY ANTIGENS; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; METHYLATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 27944504221     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.23.10338-10351.2005     Document Type: Article

References (64)

1. Akagi, K., T. Suzuki, R. M. Stephens, N. A. Jenkins, and N. G. Copeland. 2004. RTCGD: retroviral tagged cancer gene database. Nucleic Acids Res. 32:D523-D527.
2. Ayyanathan, K., M. S. Lechner, P. Bell, G. G. Maul, D. C. Schultz, Y. Yamada, K. Tanaka, K. Torigoe, and F. J. Rauscher III. 2003. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 17:1855-1869.
3. Benson, K. F., F. Q. Li, R. E. Person, D. Albani, Z. Duan, J. Wechsler, K. Meade-White, K. Williams, G. M. Acland, G. Niemeyer, C. D. Lothrop, and M. Horwitz. 2003. Mutations associated with neutropenia in dogs and humans disrupt intracellular transport of neutrophil elastase. Nat. Genet. 35:90-96.
4. Berger, S. L. 2002. Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12:142-148.
5. Boulias, K., and I. Talianidis. 2004. Functional role of G9a-induced histone methylation in small heterodimer partner-mediated transcriptional repression. Nucleic Acids Res. 32:6096-6103.
6. Cellot, S., and G. Sauvageau. 2005. Gfi-1: another piece in the HSC puzzle. Trends Immunol. 26:68-71.
7. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
8. Duan, Z., and M. Horwitz. 2003. Gfi-1 oncoproteins in hematopoiesis. Hematology 8:339-344.
9. Duan, Z., and M. Horwitz. 2005. Gfi-1 takes center stage in hematopoietic stem cells. Trends Mol. Med. 11:49-52.
10. Duan, Z., and M. Horwitz. 2003. Targets of the transcriptional represser oncoprotein Gfi-1. Proc. Natl. Acad. Sci. USA 100:5932-5937.
11. Duan, Z., F. Q. Li, J. Wechsler, K. Meade-White, K. Williams, K. F. Benson, and M. Horwitz. 2004. A novel notch protein, N2N, targeted by neutrophil elastase and implicated in hereditary neutropenia. Mol. Cell Biol. 24:58-70.
12. Feinberg, A. P., and B. Tycko. 2004. The history of cancer epigenetics. Nat. Rev. Cancer 4:143-153.
13. Gilks, C. B., S. E. Bear, H. L. Grimes, and P. N. Tsichlis. 1993. Progression of interleukin-2 (IL-2)-dependent rat T-cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein. Mol. Cell. Biol. 13:1759-1768.
14. Goldmit, M., Y. Ji, J. Skok, E. Roldan, S. Jung, H. Cedar, and Y. Bergman. 2005. Epigenetic ontogeny of the Igk locus during B cell development. Nat. Immunol. 6:198-203.
15. 1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16:6263-6272.
16. Gyory, I., J. Wu, G. Fejer, E. Seto, and K. L. Wright. 2004. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 5:299-308.
17. Hertzano, R., M. Montcouquiol, S. Rashi-Elkeles, R. Elkon, R. Yucel, W. N. Frankel, G. Rechavi, T. Moroy, T. B. Friedman, M. W. Kelley, and K. B. Avraham. 2004. Transcription profiling of inner ears from Pou4f3(ddl/ddl) identifies Gfi1 as a target of the Pou4f3 deafness gene. Hum. Mol. Genet. 13:2143-2153.
18. Hock, H., M. J. Hamblen, H. M. Rooke, J. W. Schindler, S. Saleque, Y. Fujiwara, and S. H. Orkin. 2004. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431:1002-1007.
19. Hock, H., M. J. Hamblen, H. M. Rooke, D. Traver, R. T. Bronson, S. Cameron, and S. H. Orkin. 2003. Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity 18:109-120.
20. Jafar-Nejad, H., and H. J. Bellen. 2004. Gfi/Pag-3/senseless zinc finger proteins: a unifying theme? Mol. Cell. Biol. 24:8803-8812.
21. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074-1080.
22. Johnson, K., D. L. Pflugh, D. Yu, D. G. Hesslein, K. I. Lin, A. L. Bothwell, A. Thomas-Tikhonenko, D. G. Schatz, and K. Calame. 2004. B cell-specific loss of histone 3 lysine 9 methylation in the V(H) locus depends on Pax5. Nat. Immunol. 5:853-861.
23. Karsunky, H., I. Mende, T. Schmidt, and T. Moroy. 2002. High levels of the onco-protein Gfi-1 accelerate T-cell proliferation and inhibit activation induced T-cell death in Jurkat T-cells. Oncogene 21:1571-1579.
24. Karsunky, H., H. Zeng, T. Schmidt, B. Zevnik, R. Kluge, K. W. Schmid, U. Duhrsen, and T. Moroy. 2002. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat. Genet. 30:295-300.
25. Kazanjian, A., D. Wallis, N. Au, R. Nigam, K. J. Venken, P. T. Cagle, B. F. Dickey, H. J. Bellen, C. B. Gilks, and H. L. Grimes. 2004. Growth factor independence-1 is expressed in primary human neuroendocrine lung carcinomas and mediates the differentiation of murine pulmonary neuroendocrine cells. Cancer Res. 64:6874-6882.
26. Kouzarides, T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:198-209.
27. Kuo, M. H., and C. D. Allis. 1998. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20:615-626.
28. Lukasova, E., Z. Koristek, M. Falk, S. Kozubek, S. Grigoryev, M. Kozubek, V. Ondrej, and I. Kroupova. 2005. Methylation of histones in myeloid leukemias as a potential marker of granulocyte abnormalities. J. Leukoc. Biol. 77:100-111.
29. Ma, J. 2005. Crossing the line between activation and repression. Trends Genet. 21:54-59.
30. McGhee, L., J. Bryan, L. Elliott, H. L. Grimes, A. Kazanjian, J. N. Davis, and S. Meyers. 2003. Gfi-1 attaches to the nuclear matrix, associates with ETO (MTG8) and histone deacetylase proteins, and represses transcription using a TSA-sensitive mechanism. J. Cell. Biochem. 89:1005-10018.
31. Moroy, T. 2005. The zinc finger transcription factor growth factor independence 1 (Gfi1). Int. J. Biochem. Cell Biol. 37:541-546.
32. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
33. Nishio, H., and M. J. Walsh. 2004. CCAAT displacement protein/cut homolog recruits G9a histone lysine methyltransferase to repress transcription. Proc. Natl. Acad. Sci. USA 101:11257-11262.
34. Ogawa, H., K. Ishiguro, S. Gaubatz, D. M. Livingston, and Y. Nakatani. 2002. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 296:1132-1136.
35. Osawa, M., T. Yamaguchi, Y. Nakamura, S. Kaneko, M. Onodera, K. Sawada, A. Jegalian, H. Wu, H. Nakauchi, and A. Iwama. 2002. Erythroid expansion mediated by the Gfi-1B zinc finger protein: role in normal hematopoiesis. Blood 100:2769-2777.
36. Park, J. H., Q. Yu, B. Erman, J. S. Appelbaum, D. Montoya-Durango, H. L. Grimes, and A. Singer. 2004. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 21:289-302.
37. Person, R. E., F. Q. Li, Z. Duan, K. F. Benson, J. Wechsler, H. A. Papadaki, G. Eliopoulos, C. Kaufman, S. J. Bertolone, B. Nakamoto, T. Papayannopoulou, H. L. Grimes, and M. Horwitz. 2003. Mutations in proto-oncogene GFI1 cause human neutropenia and target ELA2. Nat. Genet. 34:308-312.
38. Peters, A. H., S. Kubicek, K. Mechtler, R. J. O'Sullivan, A. A. Deryck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, Y. Shinkai, J. H. Martens, and T. Jenuwein. 2003. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12:1577-1589.
39. Peters, A. H., D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, C. Schofer, K. Weipoltshammer, M. Pagani, M. Lachner, A. Kohlmaier, S. Opravil, M. Doyle, M. Sibilia, and T. Jenuwein. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323-337.
40. Rea, S., F. Eisenhaber, D. O'Carroll, B. D. Strahl, Z. W. Sun, M. Schmid, S. Opravil, K. Mechtler, C. P. Ponting, C. D. Allis, and T. Jenuwein. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593-599.
41. Rice, J. C., S. D. Briggs, B. Ueberheide, C. M. Barber, J. Shabanowitz, D. F. Hunt, Y. Shinkai, and C. D. Allis. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12:1591-1598.
42. Rodel, B., K. Tavassoli, H. Karsunky, T. Schmidt, M. Bachmann, F. Schaper, P. Heinrich, K. Shuai, H. P. Elsasser, and T. Moroy. 2000. The zinc finger protein Gfi-1 can enhance STAT3 signaling by interacting with the STAT3 inhibitor PIAS3. EMBO J. 19:5845-5855.
43. Scheijen, B., J. Jonkers, D. Acton, and A. Berns. 1997. Characterization of pal-1, a common proviral insertion site in murine leukemia virus-induced lymphomas of c-myc and Pim-1 transgenic mice. J. Virol. 71:9-16.
44. Schmidt, T., H. Karsunky, E. Gau, B. Zevnik, H. P. Elsasser, and T. Moroy. 1998. Zinc finger protein GFI-1 has low oncogenic potential but cooperates strongly with pim and myc genes in T-cell lymphomagenesis. Oncogene 17:2661-2667.
45. Schmidt, T., H. Karsunky, B. Rodel, B. Zevnik, H. P. Elsasser, and T. Moroy. 1998. Evidence implicating Gfi-1 and Pim-1 in pre-T-cell differentiation steps associated with beta-selection. EMBO J. 17:5349-5359.
46. Schmidt, T., M. Zornig, R. Beneke, and T. Moroy. 1996. MoMuLV proviral integrations identified by Sup-F selection in tumors from infected myc/pim bitransgenic mice correlate with activation of the gfi-1 gene. Nucleic Acids Res. 24:2528-2534.
47. Schultz, D. C., K. Ayyanathan, D. Negorev, G. G. Maul, and F. J. Rauscher 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 zinc-finger proteins. Genes Dev. 16:919-932.
48. Sharina, I. G., E. Martin, A. Thomas, K. L. Uray, and F. Murad. 2003. CCAAT-binding factor regulates expression of the beta1 subunit of soluble guanylyl cyclase gene in the BE2 human neuroblastoma cell line. Proc. Natl. Acad. Sci. USA 100:11523-11528.
49. Shin, M. S., T. N. Fredrickson, J. W. Hartley, T. Suzuki, K. Agaki, and H. C. Morse III. 2004. High-throughput retroviral tagging for identification of genes involved in initiation and progression of mouse splenic marginal zone lymphomas. Cancer Res. 64:4419-4427.
50. Sims, R. J., III, K. Nishioka, and D. Reinberg. 2003. Histone lysine methylation: a signature for chromatin function. Trends Genet. 19:629-639.
51. Tachibana, M., K. Sugimoto, T. Fukushima, and Y. Shinkai. 2001. Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 276:25309-25317.
52. Tachibana, M., K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta, M. Ohki, M. Fukuda, N. Takeda, H. Niida, H. Kato, and Y. Shinkai. 2002. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16:1779-1791.
53. Thiagalingam, S., K. H. Cheng, H. J. Lee, N. Mineva, A. Thiagalingam, and J. F. Ponte. 2003. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann. N. Y. Acad. Sci. 983:84-100.
54. WAF1 and inhibits myeloid cell differentiation. Mol. Cell. Biol. 18:2462-2473.
55. Wallis, D., M. Hamblen, Y. Zhou, K, J. Venken, A. Schumacher, H. L. Grimes, H. Y. Zoghbi, S. H. Orkin, and H. J. Bellen. 2003. The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development 130:221-232.
56. Yang, L., L. Xia, D. Y. Wu, H. Wang, H. A. Chansky, W. H. Schubach, D. D. Hickstein, and Y. Zhang. 2002. Molecular cloning of ESET, a novel histone H3-specific methyltransferase that interacts with ERG transcription factor. Oncogene 21:148-152.
57. Yap, Y. L., M. P. Wong, X. W. Zhang, D. Hernandez, R. Gras, D. K. Smith, and A. Danchin. 2005. Conserved transcription factor binding sites of cancer markers derived from primary lung adenocarcinoma microarrays. Nucleic Acids Res. 33:409-421.
58. Yu, J., C. Angelin-Duclos, J. Greenwood, J. Liao, and K. Calame. 2000. Transcriptional repression by Blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol. Cell. Biol. 20:2592-2603.
59. + T cell progenitors and CD4/CD8 lineage decision in the thymus. J. Exp. Med. 197:831-844.
60. Zeng, H., R. Yucel, C. Kosan, L. Klein-Hitpass, and T. Moroy. 2004. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO J. 23:4116-4125.
61. Zhang, Y., and D. Reinberg. 2001. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15:2343-2360.
62. Zhu, J., L. Guo, B. Min, C. J. Watson, J. Hu-Li, H. A. Young, P. N. Tsichlis, and W. E. Paul. 2002. Growth factor independent-1 induced by IL-4 regulates Th2 cell proliferation. Immunity 16:733-744.
63. Zornig, M., T. Schmidt, H. Karsunky, A. Grzeschiczek, and T. Moroy. 1996. Zinc finger protein GFI-1 cooperates with myc and pim-1 in T-cell lymphomagenesis by reducing the requirements for IL-2. Oncogene 12:1789-1801.
64. Zweidler-Mckay, P. A., H. L. Grimes, M. M. Flubacher, and P. N. Tsichlis. 1996. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol. Cell. Biol. 16:4024-4034.