91
Views
87
CrossRef citations to date
0
Altmetric
Article

The H3K27me3 Demethylase dUTX Is a Suppressor of Notch- and Rb-Dependent Tumors in Drosophila

, , , , , , , , & show all
Pages 2485-2497 | Received 18 Dec 2009, Accepted 25 Feb 2010, Published online: 20 Mar 2023

REFERENCES

  • Agger, K., P. A. Cloos, J. Christensen, D. Pasini, S. Rose, J. Rappsilber, I. Issaeva, E. Canaani, A. E. Salcini, and K. Helin. 2007. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449:731–734.
  • Bagchi, S., R. Weinmann, and P. Raychaudhuri. 1991. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F. Cell 65:1063–1072.
  • Baonza, A., and M. Freeman. 2005. Control of cell proliferation in the Drosophila eye by Notch signaling. Dev. Cell 8:529–539.
  • Blatch, G. L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932–939.
  • Boyer, L. A., K. Plath, J. Zeitlinger, T. Brambrink, L. A. Medeiros, T. I. Lee, S. S. Levine, M. Wernig, A. Tajonar, M. K. Ray, G. W. Bell, A. P. Otte, M. Vidal, D. K. Gifford, R. A. Young, and R. Jaenisch. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441:349–353.
  • Bracken, A. P., N. Dietrich, D. Pasini, K. H. Hansen, and K. Helin. 2006. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20:1123–1136.
  • Bracken, A. P., D. Pasini, M. Capra, E. Prosperini, E. Colli, and K. Helin. 2003. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 22:5323–5335.
  • Bray, S. J. 2006. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7:678–689.
  • Buckles, G. R., C. Rauskolb, J. L. Villano, and F. N. Katz. 2001. Four-jointed interacts with dachs, abelson and enabled and feeds back onto the Notch pathway to affect growth and segmentation in the Drosophila leg. Development 128:3533–3542.
  • Cagan, R. L., and D. F. Ready. 1989. Notch is required for successive cell decisions in the developing Drosophila retina. Genes Dev. 3:1099–1112.
  • Cao, R., L. Wang, H. Wang, L. Xia, H. Erdjument-Bromage, P. Tempst, R. S. Jones, and Y. Zhang. 2002. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039–1043.
  • Chao, J. L., Y. C. Tsai, S. J. Chiu, and Y. H. Sun. 2004. Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development 131:3839–3847.
  • Chellappan, S. P., S. Hiebert, M. Mudryj, J. M. Horowitz, and J. R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053–1061.
  • Chittenden, T., D. M. Livingston, and W. G. Kaelin, Jr. 1991. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell 65:1073–1082.
  • Cho, Y. W., T. Hong, S. Hong, H. Guo, H. Yu, D. Kim, T. Guszczynski, G. R. Dressler, T. D. Copeland, M. Kalkum, and K. Ge. 2007. PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J. Biol. Chem. 282:20395–20406.
  • Czermin, B., R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185–196.
  • de Celis, J. F., and A. Garcia-Bellido. 1994. Roles of the Notch gene in Drosophila wing morphogenesis. Mech. Dev. 46:109–122.
  • de Celis, J. F., A. Garcia-Bellido, and S. J. Bray. 1996. Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122:359–369.
  • del Alamo, D., and M. Mlodzik. 2008. Self-modulation of Notch signaling during ommatidial development via the Roughened eye transcriptional repressor. Development 135:2895–2904.
  • De Santa, F., M. G. Totaro, E. Prosperini, S. Notarbartolo, G. Testa, and G. Natoli. 2007. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130:1083–1094.
  • Dominguez, M., and J. F. de Celis. 1998. A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye. Nature 396:276–278.
  • Dominguez, M., D. Ferres-Marco, F. J. Gutierrez-Avino, S. A. Speicher, and M. Beneyto. 2004. Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster. Nat. Genet. 36:31–39.
  • Du, W., M. Vidal, J. E. Xie, and N. Dyson. 1996. RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev. 10:1206–1218.
  • Duronio, R. J., and P. H. O'Farrell. 1995. Developmental control of the G1 to S transition in Drosophila: cyclin E is a limiting downstream target of E2F. Genes Dev. 9:1456–1468.
  • Fan, Y., and A. Bergmann. 4 December 2009, posting date. The cleaved-caspase-3 antibody is a marker of caspase-9-like DRONC activity in Drosophila. Cell Death Differ. 10.1038/cdd.2009.185.
  • Ferres-Marco, D., I. Gutierrez-Garcia, D. M. Vallejo, J. Bolivar, F. J. Gutierrez-Avino, and M. Dominguez. 2006. Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature 439:430–436.
  • Fischle, W., Y. Wang, S. A. Jacobs, Y. Kim, C. D. Allis, and S. Khorasanizadeh. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17:1870–1881.
  • Frise, E., J. A. Knoblich, S. Younger-Shepherd, L. Y. Jan, and Y. N. Jan. 1996. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl. Acad. Sci. U. S. A. 93:11925–11932.
  • Guo, M., L. Y. Jan, and Y. N. Jan. 1996. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27–41.
  • Hamel, P. A., R. M. Gill, R. A. Phillips, and B. L. Gallie. 1992. Transcriptional repression of the E2-containing promoters EIIaE, c-myc, and RB1 by the product of the RB1 gene. Mol. Cell. Biol. 12:3431–3438.
  • Hanahan, D., and R. A. Weinberg. 2000. The hallmarks of cancer. Cell 100:57–70.
  • Hong, S., Y. W. Cho, L. R. Yu, H. Yu, T. D. Veenstra, and K. Ge. 2007. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. U. S. A. 104:18439–18444.
  • Hueber, S. D., and I. Lohmann. 2008. Shaping segments: Hox gene function in the genomic age. Bioessays 30:965–979.
  • Issaeva, I., Y. Zonis, T. Rozovskaia, K. Orlovsky, C. M. Croce, T. Nakamura, A. Mazo, L. Eisenbach, and E. Canaani. 2007. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol. Cell. Biol. 27:1889–1903.
  • Karim, F. D., and G. M. Rubin. 1998. Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 125:1–9.
  • Ketel, C. S., E. F. Andersen, M. L. Vargas, J. Suh, S. Strome, and J. A. Simon. 2005. Subunit contributions to histone methyltransferase activities of fly and worm Polycomb group complexes. Mol. Cell. Biol. 25:6857–6868.
  • Kleer, C. G., Q. Cao, S. Varambally, R. Shen, I. Ota, S. A. Tomlins, D. Ghosh, R. G. Sewalt, A. P. Otte, D. F. Hayes, M. S. Sabel, D. Livant, S. J. Weiss, M. A. Rubin, and A. M. Chinnaiyan. 2003. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 100:11606–11611.
  • Klose, R. J., E. M. Kallin, and Y. Zhang. 2006. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 7:715–727.
  • Kondo, Y., L. Shen, A. S. Cheng, S. Ahmed, Y. Boumber, C. Charo, T. Yamochi, T. Urano, K. Furukawa, B. Kwabi-Addo, D. L. Gold, Y. Sekido, T. H. Huang, and J. P. Issa. 2008. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat. Genet. 40:741–750.
  • Krejci, A., F. Bernard, B. E. Housden, S. Collins, and S. J. Bray. 2009. Direct response to Notch activation: signaling crosstalk and incoherent logic. Sci. Signal. 2:ra1.
  • Kuzmichev, A., K. Nishioka, H. Erdjument-Bromage, P. Tempst, and D. Reinberg. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the enhancer of Zeste protein. Genes Dev. 16:2893–2905.
  • Lan, F., P. E. Bayliss, J. L. Rinn, J. R. Whetstine, J. K. Wang, S. Chen, S. Iwase, R. Alpatov, I. Issaeva, E. Canaani, T. M. Roberts, H. Y. Chang, and Y. Shi. 2007. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449:689–694.
  • Lee, M. G., R. Villa, P. Trojer, J. Norman, K. P. Yan, D. Reinberg, L. Di Croce, and R. Shiekhattar. 2007. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318:447–450.
  • Lee, T., and L. Luo. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24:251–254.
  • Lee, T. I., R. G. Jenner, L. A. Boyer, M. G. Guenther, S. S. Levine, R. M. Kumar, B. Chevalier, S. E. Johnstone, M. F. Cole, K. Isono, H. Koseki, T. Fuchikami, K. Abe, H. L. Murray, J. P. Zucker, B. Yuan, G. W. Bell, E. Herbolsheimer, N. M. Hannett, K. Sun, D. T. Odom, A. P. Otte, T. L. Volkert, D. P. Bartel, D. A. Melton, D. K. Gifford, R. Jaenisch, and R. A. Young. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125:301–313.
  • Lees, J. A., K. J. Buchkovich, D. R. Marshak, C. W. Anderson, and E. Harlow. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10:4279–4290.
  • Ligoxygakis, P., S. Y. Yu, C. Delidakis, and N. E. Baker. 1998. A subset of notch functions during Drosophila eye development require Su(H) and the E(spl) gene complex. Development 125:2893–2900.
  • Lin, B. T., S. Gruenwald, A. O. Morla, W. H. Lee, and J. Y. Wang. 1991. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J. 10:857–864.
  • Min, J., Y. Zhang, and R. M. Xu. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17:1823–1828.
  • Montgomery, N. D., D. Yee, A. Chen, S. Kalantry, S. J. Chamberlain, A. P. Otte, and T. Magnuson. 2005. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr. Biol. 15:942–947.
  • Moss, T. J., and L. L. Wallrath. 2007. Connections between epigenetic gene silencing and human disease. Mutat. Res. 618:163–174.
  • Muller, J., C. M. Hart, N. J. Francis, M. L. Vargas, A. Sengupta, B. Wild, E. L. Miller, M. B. O'Connor, R. E. Kingston, and J. A. Simon. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197–208.
  • Negre, N., J. Hennetin, L. V. Sun, S. Lavrov, M. Bellis, K. P. White, and G. Cavalli. 2006. Chromosomal distribution of PcG proteins during Drosophila development. PLoS Biol. 4:e170.
  • Newsome, T. P., B. Asling, and B. J. Dickson. 2000. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127:851–860.
  • Papayannopoulos, V., A. Tomlinson, V. M. Panin, C. Rauskolb, and K. D. Irvine. 1998. Dorsal-ventral signaling in the Drosophila eye. Science 281:2031–2034.
  • Patel, S. R., D. Kim, I. Levitan, and G. R. Dressler. 2007. The BRCT-domain containing protein PTIP links PAX2 to a histone H3, lysine 4 methyltransferase complex. Dev. Cell 13:580–592.
  • Pearson, J. C., D. Lemons, and W. McGinnis. 2005. Modulating Hox gene functions during animal body patterning. Nat. Rev. Genet. 6:893–904.
  • Pellock, B. J., E. Buff, K. White, and I. K. Hariharan. 2007. The Drosophila tumor suppressors Expanded and Merlin differentially regulate cell cycle exit, apoptosis, and Wingless signaling. Dev. Biol. 304:102–115.
  • Plath, K., J. Fang, S. K. Mlynarczyk-Evans, R. Cao, K. A. Worringer, H. Wang, C. C. de la Cruz, A. P. Otte, B. Panning, and Y. Zhang. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131–135.
  • Rebay, I., R. J. Fleming, R. G. Fehon, L. Cherbas, P. Cherbas, and S. Artavanis-Tsakonas. 1991. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 67:687–699.
  • Reynolds-Kenneally, J., and M. Mlodzik. 2005. Notch signaling controls proliferation through cell-autonomous and non-autonomous mechanisms in the Drosophila eye. Dev. Biol. 285:38–48.
  • Robertson, G., M. Hirst, M. Bainbridge, M. Bilenky, Y. Zhao, T. Zeng, G. Euskirchen, B. Bernier, R. Varhol, A. Delaney, N. Thiessen, O. L. Griffith, A. He, M. Marra, M. Snyder, and S. Jones. 2007. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 4:651–657.
  • Saucedo, L. J., and B. A. Edgar. 2007. Filling out the Hippo pathway. Nat. Rev. Mol. Cell Biol. 8:613–621.
  • Schlesinger, Y., R. Straussman, I. Keshet, S. Farkash, M. Hecht, J. Zimmerman, E. Eden, Z. Yakhini, E. Ben-Shushan, B. E. Reubinoff, Y. Bergman, I. Simon, and H. Cedar. 2007. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat. Genet. 39:232–236.
  • Schwartz, Y. B., T. G. Kahn, D. A. Nix, X. Y. Li, R. Bourgon, M. Biggin, and V. Pirrotta. 2006. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat. Genet. 38:700–705.
  • Schwartz, Y. B., and V. Pirrotta. 2007. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8:9–22.
  • Shearn, A. 1989. The ash-1, ash-2 and trithorax genes of Drosophila melanogaster are functionally related. Genetics 121:517–525.
  • Sjolund, J., C. Manetopoulos, M. T. Stockhausen, and H. Axelson. 2005. The Notch pathway in cancer: differentiation gone awry. Eur. J. Cancer 41:2620–2629.
  • Smith, E. R., M. G. Lee, B. Winter, N. M. Droz, J. C. Eissenberg, R. Shiekhattar, and A. Shilatifard. 2008. Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol. Cell. Biol. 28:1041–1046.
  • Spana, E. P., and C. Q. Doe. 1996. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17:21–26.
  • Sparmann, A., and M. van Lohuizen. 2006. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 6:846–856.
  • Squazzo, S. L., H. O'Geen, V. M. Komashko, S. R. Krig, V. X. Jin, S. W. Jang, R. Margueron, D. Reinberg, R. Green, and P. J. Farnham. 2006. Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res. 16:890–900.
  • Sun, X., and S. Artavanis-Tsakonas. 1997. Secreted forms of DELTA and SERRATE define antagonists of Notch signaling in Drosophila. Development 124:3439–3448.
  • Tapon, N., N. Ito, B. J. Dickson, J. E. Treisman, and I. K. Hariharan. 2001. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105:345–355.
  • Thomas, U., S. A. Speicher, and E. Knust. 1991. The Drosophila gene Serrate encodes an EGF-like transmembrane protein with a complex expression pattern in embryos and wing discs. Development 111:749–761.
  • Tolhuis, B., E. de Wit, I. Muijrers, H. Teunissen, W. Talhout, B. van Steensel, and M. van Lohuizen. 2006. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat. Genet. 38:694–699.
  • van Haaften, G., G. L. Dalgliesh, H. Davies, L. Chen, G. Bignell, C. Greenman, S. Edkins, C. Hardy, S. O'Meara, J. Teague, A. Butler, J. Hinton, C. Latimer, J. Andrews, S. Barthorpe, D. Beare, G. Buck, P. J. Campbell, J. Cole, S. Forbes, M. Jia, D. Jones, C. Y. Kok, C. Leroy, M. L. Lin, D. J. McBride, M. Maddison, S. Maquire, K. McLay, A. Menzies, T. Mironenko, L. Mulderrig, L. Mudie, E. Pleasance, R. Shepherd, R. Smith, L. Stebbings, P. Stephens, G. Tang, P. S. Tarpey, R. Turner, K. Turrell, J. Varian, S. West, S. Widaa, P. Wray, V. P. Collins, K. Ichimura, S. Law, J. Wong, S. T. Yuen, S. Y. Leung, G. Tonon, R. A. DePinho, Y. T. Tai, K. C. Anderson, R. J. Kahnoski, A. Massie, S. K. Khoo, B. T. Teh, M. R. Stratton, and P. A. Futreal. 2009. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat. Genet. 41:521–523.
  • Varambally, S., S. M. Dhanasekaran, M. Zhou, T. R. Barrette, C. Kumar-Sinha, M. G. Sanda, D. Ghosh, K. J. Pienta, R. G. Sewalt, A. P. Otte, M. A. Rubin, and A. M. Chinnaiyan. 2002. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624–629.
  • Wang, J. K., M. C. Tsai, G. Poulin, A. S. Adler, S. Chen, H. Liu, Y. Shi, and H. Y. Chang. 2010. The histone demethylase UTX enables RB-dependent cell fate control. Genes Dev. 24:327–332.
  • Xu, T., and G. M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117:1223–1237.
  • Zweidler-McKay, P. A., and W. S. Pear. 2004. Notch and T cell malignancy. Semin. Cancer Biol. 14:329–340.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.