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Transcriptional Regulation

Leukemia Proto-Oncoprotein MLL Forms a SET1-Like Histone Methyltransferase Complex with Menin To Regulate Hox Gene Expression

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Pages 5639-5649 | Received 16 Feb 2004, Accepted 19 Apr 2004, Published online: 27 Mar 2023

REFERENCES

  • Aasland, R., Gibson T. J., and Stewart A. F.. 1995. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20:56–59.
  • Agarwal, S. K., Guru S. C., Heppner C., Erdos M. R., Collins R. M., Park S. Y., Saggar S., Chandrasekharappa S. C., Collins F. S., Spiegel A. M., Marx S. J., and Burns A. L.. 1999. Menin interacts with the AP1 transcription factor JunD and represses JunD-activated transcription. Cell 96:143–152.
  • Agarwal, S. K., Novotny E. A., Crabtree J. S., Weitzman J. B., Yaniv M., Burns A. L., Chandrasekharappa S. C., Collins F. S., Spiegel A. M., and Marx S. J.. 2003. Transcription factor JunD, deprived of menin, switches from growth suppressor to growth promoter. Proc. Natl. Acad. Sci. USA 100:10770–10775.
  • Alvarez-Venegas, R., and Avramova Z.. 2002. SET-domain proteins of the Su(var)3-9, E(z) and trithorax families. Gene 285:25–37.
  • Armstrong, S. A., Staunton J. E., Silverman L. B., Pieters R., den Boer M. L., Minden M. D., Sallan S. E., Lander E. S., Golub T. R., and Korsmeyer S. J.. 2002. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat. Genet. 30:41–47.
  • Ayton, P. M., and Cleary M. L.. 2001. Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins. Oncogene 20:5695–5707.
  • Ayton, P. M., and Cleary M. L.. 2003. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev. 17:2298–2307.
  • Breen, T. R., and Harte P. J.. 1993. Trithorax regulates multiple homeotic genes in the bithorax and antennapedia complexes and exerts different tissue-specific, parasegment-specific and promoter-specific effects on each. Development 117:119–134.
  • Butler, L. H., Slany R., Cui X., Cleary M. L., and Mason D. Y.. 1997. The HRX proto-oncogene product is widely expressed in human tissues and localizes to nuclear structures. Blood 89:3361–3370.
  • Chandrasekharappa, S. C., Guru S. C., Manickam P., Olufemi S. E., Collins F. S., Emmert-Buck M. R., Debelenko L. V., Zhuang Z., Lubensky I. A., Liotta L. A., Crabtree J. S., Wang Y., Roe B. A., Weisemann J., Boguski M. S., Agarwal S. K., Kester M. B., Kim Y. S., Heppner C., Dong Q., Spiegel A. M., Burns A. L., and Marx S. J.. 1997. Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 276:404–407.
  • Chandrasekharappa, S. C., and Teh B. T.. 2003. Functional studies of the MEN1 gene. J. Intern. Med. 253:606–615.
  • Collins, E. C., and Rabbitts T. H.. 2002. The promiscuous MLL gene links chromosomal translocations to cellular differentiation and tumour tropism. Trends Mol. Med. 8:436–442.
  • Cui, X., De Vivo I., Slany R., Miyamoto A., Firestein R., and Cleary M. L.. 1998. Association of SET domain and myotubularin-related proteins modulates growth control. Nat. Genet. 18:331–337.
  • Dimartino, J. F., and Cleary M. L.. 1999. Mll rearrangements in haematological malignancies: lessons from clinical and biological studies. Br. J. Haematol. 106:614–626.
  • Djabali, M., Selleri L., Parry P., Bower M., Young B. D., and Evans G. A.. 1992. A trithorax-like gene is interrupted by chromosome 11q23 translocations in acute leukaemias. Nat. Genet. 2:113–118.
  • Ernst, P., Wang J., Huang M., Goodman R. H., and Korsmeyer S. J.. 2001. MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol. Cell. Biol. 21:2249–2258.
  • Firestein, R., Cui X., Huie P., and Cleary M. L.. 2000. SET domain-dependent regulation of transcriptional silencing and growth control by SUV39H1, a mammalian ortholog of Drosophila Su(var)3-9. Mol. Cell. Biol. 20:4900–4909.
  • Freiman, R. N., and Herr W.. 1997. Viral mimicry: common mode of association with HCF by VP16 and the cellular protein LZIP. Genes Dev. 11:3122–3127.
  • Goo, Y. H., Sohn Y. C., Kim D. H., Kim S. W., Kang M. J., Jung D. J., Kwak E., Barlev N. A., Berger S. L., Chow V. T., Roeder R. G., Azorsa D. O., Meltzer P. S., Suh P. G., Song E. J., Lee K. J., Lee Y. C., and Lee J. W.. 2003. Activating signal cointegrator 2 belongs to a novel steady-state complex that contains a subset of trithorax group proteins. Mol. Cell. Biol. 23:140–149.
  • Gori, F., and Demay M. B.. 2004. BIG-3, a novel WD-40 repeat protein, is expressed in the developing growth plate and accelerates chondrocyte differentiation in vitro. Endocrinology 145:1050–1054.
  • Goto, H., Motomura S., Wilson A. C., Freiman R. N., Nakabeppu Y., Fukushima K., Fujishima M., Herr W., and Nishimoto T.. 1997. A single-point mutation in HCF causes temperature-sensitive cell-cycle arrest and disrupts VP16 function. Genes Dev. 11:726–737.
  • Gu, Y., Nakamura T., Alder H., Prasad R., Canaani O., Cimino G., Croce C. M., and Canaani E.. 1992. The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene. Cell 71:701–708.
  • Hanson, R. D., Hess J. L., Yu B. D., Ernst P., van Lohuizen M., Berns A., van der Lugt N. M., Shashikant C. S., Ruddle F. H., Seto M., and Korsmeyer S. J.. 1999. Mammalian trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc. Natl. Acad. Sci. USA 96:14372–14377.
  • Hsieh, J. J., Cheng E. H., and Korsmeyer S. J.. 2003. Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression. Cell 115:293–303.
  • Hsieh, J. J., Ernst P., Erdjument-Bromage H., Tempst P., and Korsmeyer S. J.. 2003. Proteolytic cleavage of MLL generates a complex of N- and C-terminal fragments that confers protein stability and subnuclear localization. Mol. Cell. Biol. 23:186–194.
  • Hsu, K., and Look A. T.. 2003. Turning on a dimer: new insights into MLL chimeras. Cancer Cell 4:81–83.
  • Hughes, C. M., Rozenblatt-Rosen O., Milne T. A., Copeland T. D., Levine S. S., Lee J. C., Hayes D. N., Shanmugam K. S., Bhattacharjee A., Biondi C. A., Kay G. F., Hayward N. K., Hess J. L., and Meyerson M.. 2004. Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13:587–597.
  • Huret, J. L., Dessen P., and Bernheim A.. 2001. An atlas of chromosomes in hematological malignancies. Example: 11q23 and MLL partners. Leukemia 15:987–989.
  • Ikegawa, S., Isomura M., Koshizuka Y., and Nakamura Y.. 1999. Cloning and characterization of ASH2L and Ash2l, human and mouse homologs of the Drosophila ash2 gene. Cytogenet. Cell Genet. 84:167–172.
  • Jin, S., Mao H., Schnepp R. W., Sykes S. M., Silva A. C., D'Andrea A. D., and Hua X.. 2003. Menin associates with FANCD2, a protein involved in repair of DNA damage. Cancer Res. 63:4204–4210.
  • Johnson, K. M., Mahajan S. S., and Wilson A. C.. 1999. Herpes simplex virus transactivator VP16 discriminates between HCF-1 and a novel family member, HCF-2. J. Virol. 73:3930–3940.
  • Kim, H., Lee J. E., Cho E. J., Liu J. O., and Youn H. D.. 2003. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 63:6135–6139.
  • Kristie, T. M., Pomerantz J. L., Twomey T. C., Parent S. A., and Sharp P. A.. 1995. The cellular C1 factor of the herpes simplex virus enhancer complex is a family of polypeptides. J. Biol. Chem. 270:4387–4394.
  • Kumar, A. R., Hudson W. A., Chen W., Nishiuchi R., Yao Q., and Kersey J. H.. 2003. Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia. Blood 100:1823–1828.
  • Kuzmichev, A., Nishioka K., Erdjument-Bromage H., Tempst P., and Reinberg D.. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16:2893–2905.
  • LaJeunesse, D., and Shearn A.. 1995. Trans-regulation of thoracic homeotic selector genes of the antennapedia and bithorax complexes by the trithorax group genes: absent, small, and homeotic discs 1 and 2. Mech. Dev. 53:123–139.
  • Lin, S. Y., and Elledge S. J.. 2003. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113:881–889.
  • Lu, R., Yang P., Padmakumar S., and Misra V.. 1998. The herpesvirus transactivator VP16 mimics a human basic domain leucine zipper protein, luman, in its interaction with HCF. J. Virol. 72:6291–6297.
  • Luciano, R. L., and Wilson A. C.. 2003. HCF-1 functions as a coactivator for the zinc finger protein Krox20. J. Biol. Chem. 278:51116–51124.
  • Martin, M. E., Milne T. A., Bloyer S., Galoian K., Shen W., Gibbs D., Brock H. W., Slany R., and Hess J. L.. 2003. Dimerization of MLL fusion proteins immortalizes hematopoietic cells. Cancer Cell 4:197–207.
  • Miller, T., Krogan N. J., Dover J., Erdjument-Bromage H., Tempst P., Johnston M., Greenblatt J. F., and Shilatifard A.. 2001. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 98:12902–12907.
  • Milne, T. A., Briggs S. D., Brock H. W., Martin M. E., Gibbs D., Allis C. D., and Hess J. L.. 2002. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10:1107–1117.
  • Nagy, P. L., Griesenbeck J., Kornberg R. D., and Cleary M. L.. 2002. A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc. Natl. Acad. Sci. USA 99:90–94.
  • Nakamura, T., Mori T., Tada S., Krajewski W., Rozovskaia T., Wassell R., Dubois G., Mazo A., Croce C. M., and Canaani E.. 2002. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10:1119–1128.
  • Petruk, S., Sedkov Y., Smith S., Tillib S., Kraevski V., Nakamura T., Canaani E., Croce C. M., and Mazo A.. 2001. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294:1331–1334.
  • Poisson, A., Zablewska B., and Gaudray P.. 2003. Menin interacting proteins as clues toward the understanding of multiple endocrine neoplasia type 1. Cancer Lett. 189:1–10.
  • Roguev, A., Schaft D., Shevchenko A., Pijnappel W. W., Wilm M., Aasland R., and Stewart A. F.. 2001. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 20:7137–7148.
  • Rozovskaia, T., Feinstein E., Mor O., Foa R., Blechman J., Nakamura T., Croce C. M., Cimino G., and Canaani E.. 2001. Upregulation of Meis1 and HoxA9 in acute lymphocytic leukemias with the t(4:11) abnormality. Oncogene 20:874–878.
  • Saijo, M., Sakai Y., Kishino T., Niikawa N., Matsuura Y., Morino K., Tamai K., and Taya Y.. 1995. Molecular cloning of a human protein that binds to the retinoblastoma protein and chromosomal mapping. Genomics 27:511–519.
  • Schneider, R., Bannister A. J., and Kouzarides T.. 2002. Unsafe SETs: histone lysine methyltransferases and cancer. Trends Biochem. Sci. 27:396–402.
  • Sedkov, Y., Tillib S., Mizrokhi L., and Mazo A.. 1994. The bithorax complex is regulated by trithorax earlier during Drosophila embryogenesis than is the antennapedia complex, correlating with a bithorax-like expression pattern of distinct early trithorax transcripts. Development 120:1907–1917.
  • Slany, R. K., Lavau C., and Cleary M. L.. 1998. The oncogenic capacity of HRX-ENL requires the transcriptional transactivation activity of ENL and the DNA binding motifs of HRX. Mol. Cell. Biol. 18:122–129.
  • So, C. W., Karsunky H., Wong P., Weissman I. L., and Cleary M. L.. 2004. Leukemic transformation of hematopietic progenitors by MLL-GAS7 in the absence of Hoxa7 or Hoxa9. Blood 103:3192–3199.
  • So, C. W., Lin M., Ayton P. M., Chen E. H., and Cleary M. L.. 2003. Dimerization contributes to oncogenic activation of MLL chimeras in acute leukemias. Cancer Cell 4:99–110.
  • Sukhodolets, K. E., Hickman A. B., Agarwal S. K., Sukhodolets M. V., Obungu V. H., Novotny E. A., Crabtree J. S., Chandrasekharappa S. C., Collins F. S., Spiegel A. M., Burns A. L., and Marx S. J.. 2003. The 32-kilodalton subunit of replication protein A interacts with menin, the product of the MEN1 tumor suppressor gene. Mol. Cell. Biol. 23:493–509.
  • Tkachuk, D. C., Kohler S., and Cleary M. L.. 1992. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 71:691–700.
  • Wang, J., Zhou Y., Yin B., Du G., Huang X., Li G., Shen Y., Yuan J., and Qiang B.. 2001. ASH2L: alternative splicing and downregulation during induced megakaryocytic differentiation of multipotential leukemia cell lines. J. Mol. Med. 79:399–405.
  • Wilson, A. C., LaMarco K., Peterson M. G., and Herr W.. 1993. The VP16 accessory protein HCF is a family of polypeptides processed from a large precursor protein. Cell 74:115–125.
  • Wilson, A. C., Peterson M. G., and Herr W.. 1995. The HCF repeat is an unusual proteolytic cleavage signal. Genes Dev. 9:2445–2458.
  • Wysocka, J., and Herr W.. 2003. The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem. Sci. 28:294–304.
  • Wysocka, J., Myers M. P., Laherty C. D., Eisenman R. N., and Herr W.. 2003. Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev. 17:896–911.
  • Xia, Z. B., Anderson M., Diaz M. O., and Zeleznik-Le N. J.. 2003. MLL repression domain interacts with histone deacetylases, the polycomb group proteins HPC2 and BMI-1, and the corepressor C-terminal-binding protein. Proc. Natl. Acad. Sci. USA 100:8342–8347.
  • Yeoh, E. J., Ross M. E., Shurtleff S. A., Williams W. K., Patel D., Mahfouz R., Behm F. G., Raimondi S. C., Relling M. V., Patel A., Cheng C., Campana D., Wilkins D., Zhou X., Li J., Liu H., Pui C. H., Evans W. E., Naeve C., Wong L., and Downing J. R.. 2002. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1:133–143.
  • Yokoyama, A., Kitabayashi I., Ayton P. M., Cleary M. L., and Ohki M.. 2002. Leukemia proto-oncoprotein MLL is proteolytically processed into 2 fragments with opposite transcriptional properties. Blood 100:3710–3718.
  • Yu, B. D., Hanson R. D., Hess J. L., Horning S. E., and Korsmeyer S. J.. 1998. MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc. Natl. Acad. Sci. USA 95:10632–10636.
  • Yu, B. D., Hess J. L., Horning S. E., Brown G. A., and Korsmeyer S. J.. 1995. Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378:505–508.
  • Zeisig, B. B., Milne T., Garcia-Cuellar M. P., Schreiner S., Martin M. E., Fuchs U., Borkhardt A., Chanda S. K., Walker J., Soden R., Hess J. L., and Slany R. K.. 2004. Hoxa9 and Meis1 are key targets for MLL-ENL-mediated cellular immortalization. Mol. Cell. Biol. 24:617–628.
  • Zeisig, B. B., Schreiner S., Garcia-Cuellar M. P., and Slany R. K.. 2003. Transcriptional activation is a key function encoded by MLL fusion partners. Leukemia 17:359–365.
  • Zeleznik-Le, N. J., Harden A. M., and Rowley J. D.. 1994. 11q23 translocations split the “AT-hook” cruciform DNA-binding region and the transcriptional repression domain from the activation domain of the mixed-lineage leukemia (MLL) gene. Proc. Natl. Acad. Sci. USA 91:10610–10614.

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