119
Views
56
CrossRef citations to date
0
Altmetric
Article

AML1/RUNX1 Phosphorylation by Cyclin-Dependent Kinases Regulates the Degradation of AML1/RUNX1 by the Anaphase-Promoting Complex

, , , &
Pages 7420-7429 | Received 06 Apr 2006, Accepted 25 Jul 2006, Published online: 27 Mar 2023

REFERENCES

  • Bain, J., H. McLauchlan, M. Elliott, and P. Cohen. 2003. The specificities of protein kinase inhibitors: an update. Biochem. J. 371:199–204.
  • Bernardin, F., and A. D. Friedman. 2002. AML1 stimulates G1 to S progression via its transactivation domain. Oncogene 21:3247–3252.
  • Bernardin-Fried, F., T. Kummalue, S. Leijen, M. I. Collector, K. Ravid, and A. D. Friedman. 2004. AML1/RUNX1 increases during G1 to S cell cycle progression independent of cytokine-dependent phosphorylation and induces cyclin D3 gene expression. J. Biol. Chem. 279:15678–15687.
  • Biggs, J. R., Y. Zhang, L. F. Peterson, M. Garcia, D. E. Zhang, and A. S. Kraft. 2005. Phosphorylation of AML1/RUNX1 regulates its degradation and nuclear matrix association. Mol. Cancer Res. 3:391–401.
  • Burns, C. E., D. Traver, E. Mayhall, J. L. Shepard, and L. I. Zon. 2005. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev. 19:2331–2342.
  • Chen, C. L., D. C. Broom, Y. Liu, J. C. de Nooij, Z. Li, C. Cen, O. A. Samad, T. M. Jessell, C. J. Woolf, and Q. Ma. 2006. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365–377.
  • Chow, J. P., W. Y. Siu, H. T. Ho, K. H. Ma, C. C. Ho, and R. Y. Poon. 2003. Differential contribution of inhibitory phosphorylation of CDC2 and CDK2 for unperturbed cell cycle control and DNA integrity checkpoints. J. Biol. Chem. 278:40815–40828.
  • Davis, R. J. 1993. The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268:14553–14556.
  • Erickson, P. F., G. Dessev, R. S. Lasher, G. Philips, M. Robinson, and H. A. Drabkin. 1996. ETO and AML1 phosphoproteins are expressed in CD34+ hematopoietic progenitors: implications for t(8;21) leukemogenesis and monitoring residual disease. Blood 88:1813–1823.
  • Huang, G., K. Shigesada, K. Ito, H. J. Wee, T. Yokomizo, and Y. Ito. 2001. Dimerization with PEBP2beta protects RUNX1/AML1 from ubiquitin-proteasome-mediated degradation. EMBO J. 20:723–733.
  • Imai, Y., M. Kurokawa, Y. Yamaguchi, K. Izutsu, E. Nitta, K. Mitani, M. Satake, T. Noda, Y. Ito, and H. Hirai. 2004. The corepressor mSin3A regulates phosphorylation-induced activation, intranuclear location, and stability of AML1. Mol. Cell Biol. 24:1033–1043.
  • Iwatsuki, K., K. Tanaka, T. Kaneko, R. Kazama, S. Okamoto, Y. Nakayama, Y. Ito, M. Satake, S. Takahashi, A. Miyajima, T. Watanabe, and T. Hara. 2005. Runx1 promotes angiogenesis by downregulation of insulin-like growth factor-binding protein-3. Oncogene 24:1129–1137.
  • Jiang, H., F. Zhang, T. Kurosu, and B. M. Peterlin. 2005. Runx1 binds positive transcription elongation factor b and represses transcriptional elongation by RNA polymerase II: possible mechanism of CD4 silencing. Mol. Cell. Biol. 25:10675–10683.
  • Kramer, I., M. Sigrist, J. C. de Nooij, I. Taniuchi, T. M. Jessell, and S. Arber. 2006. A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron 49:379–393.
  • Levanon, D., R. E. Goldstein, Y. Bernstein, H. Tang, D. Goldenberg, S. Stifani, Z. Paroush, and Y. Groner. 1998. Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors. Proc. Natl. Acad. Sci. USA 95:11590–11595.
  • Littlepage, L. E., and J. V. Ruderman. 2002. Identification of a new APC/C recognition domain, the A box, which is required for the Cdh1-dependent destruction of the kinase Aurora-A during mitotic exit. Genes Dev. 16:2274–2285.
  • Lou, J., W. Cao, F. Bernardin, K. Ayyanathan, F. J. RauscherIII, and A. D. Friedman. 2000. Exogenous Cdk4 overcomes reduced Cdk4 RNA and inhibition of G1 progression in hematopoietic cells expressing a dominant-negative CBF—a model for overcoming inhibition of proliferation by CBF oncoproteins. Oncogene 19:2695–2703.
  • Lutterbach, B., J. J. Westendorf, B. Linggi, S. Isaac, E. Seto, and S. W. Hiebert. 2000. A mechanism of repression by acute myeloid leukemia-1, the target of multiple chromosomal translocations in acute leukemia. J. Biol. Chem. 275:651–656.
  • Major, M. L., R. Lepe, and R. H. Costa. 2004. Forkhead box M1B transcriptional activity requires binding of Cdk-cyclin complexes for phosphorylation-dependent recruitment of p300/CBP coactivators. Mol. Cell. Biol. 24:2649–2661.
  • Meyers, S., J. R. Downing, and S. W. Hiebert. 1993. Identification of AML-1 and the (8;21) translocation protein (AML-1/ETO) as sequence-specific DNA-binding proteins: the runt homology domain is required for DNA binding and protein-protein interactions. Mol. Cell. Biol. 13:6336–6345.
  • Mikhail, F. M., K. K. Sinha, Y. Saunthararajah, and G. Nucifora. 2005. Normal and transforming functions of RUNX1: a perspective. J. Cell Physiol.
  • Miyoshi, H., M. Ohira, K. Shimizu, K. Mitani, H. Hirai, T. Imai, K. Yokoyama, E. Soeda, and M. Ohki. 1995. Alternative splicing and genomic structure of the AML1 gene involved in acute myeloid leukemia. Nucleic Acids Res. 23:2762–2769.
  • Miyoshi, H., K. Shimizu, T. Kozu, N. Maseki, Y. Kaneko, and M. Ohki. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. USA 88:10431–10434.
  • Mulloy, J. C., J. Cammenga, K. L. MacKenzie, F. J. Berguido, M. A. Moore, and S. D. Nimer. 2002. The AML1-ETO fusion protein promotes the expansion of human hematopoietic stem cells. Blood 99:15–23.
  • Murray, A. W. 2004. Recycling the cell cycle: cyclins revisited. Cell 116:221–234.
  • Okuda, T., J. van Deursen, S. W. Hiebert, G. Grosveld, and J. R. Downing. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321–330.
  • Osato, M., N. Asou, E. Abdalla, K. Hoshino, H. Yamasaki, T. Okubo, H. Suzushima, K. Takatsuki, T. Kanno, K. Shigesada, and Y. Ito. 1999. Biallelic and heterozygous point mutations in the runt domain of the AML1/PEBP2alphaB gene associated with myeloblastic leukemias. Blood 93:1817–1824.
  • Peterson, L. F., A. Boyapati, V. Ranganathan, A. Iwama, D. G. Tenen, S. Tsai, and D. E. Zhang. 2005. The hematopoietic transcription factor AML1 (RUNX1) is negatively regulated by the cell cycle protein cyclin D3. Mol. Cell. Biol. 25:10205–10219.
  • Petrovick, M. S., S. W. Hiebert, A. D. Friedman, C. J. Hetherington, D. G. Tenen, and D. E. Zhang. 1998. Multiple functional domains of AML1: PU. 1 and C/EBPα synergize with different regions of AML1. Mol. Cell. Biol. 18:3915–3925.
  • Qiao, M., P. Shapiro, M. Fosbrink, H. Rus, R. Kumar, and A. Passaniti. 2006. Cell cycle-dependent phosphorylation of the RUNX2 transcription factor by cdc2 regulates endothelial cell proliferation. J. Biol. Chem. 281:7118–7128.
  • Shuman, J. D., T. Sebastian, P. Kaldis, T. D. Copeland, S. Zhu, R. C. Smart, and P. F. Johnson. 2004. Cell cycle-dependent phosphorylation of C/EBPβ mediates oncogenic cooperativity between C/EBPβ and H-RasV12. Mol. Cell. Biol. 24:7380–7391.
  • Song, W. J., M. G. Sullivan, R. D. Legare, S. Hutchings, X. Tan, D. Kufrin, J. Ratajczak, I. C. Resende, C. Haworth, R. Hock, M. Loh, C. Felix, D. C. Roy, L. Busque, D. Kurnit, C. Willman, A. M. Gewirtz, N. A. Speck, J. H. Bushweller, F. P. Li, K. Gardiner, M. Poncz, J. M. Maris, and D. G. Gilliland. 1999. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat. Genet. 23:166–175.
  • Strom, D. K., J. Nip, J. J. Westendorf, B. Linggi, B. Lutterbach, J. R. Downing, N. Lenny, and S. W. Hiebert. 2000. Expression of the AML-1 oncogene shortens the G(1) phase of the cell cycle. J. Biol. Chem. 275:3438–3445.
  • Tanaka, T., M. Kurokawa, K. Ueki, K. Tanaka, Y. Imai, K. Mitani, K. Okazaki, N. Sagata, Y. Yazaki, Y. Shibata, T. Kadowaki, and H. Hirai. 1996. The extracellular signal-regulated kinase pathway phosphorylates AML1, an acute myeloid leukemia gene product, and potentially regulates its transactivation ability. Mol. Cell. Biol. 16:3967–3979.
  • Theriault, F. M., H. N. Nuthall, Z. Dong, R. Lo, F. Barnabe-Heider, F. D. Miller, and S. Stifani. 2005. Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J. Neurosci. 25:2050–2061.
  • Ubersax, J. A., E. L. Woodbury, P. N. Quang, M. Paraz, J. D. Blethrow, K. Shah, K. M. Shokat, and D. O. Morgan. 2003. Targets of the cyclin-dependent kinase Cdk1. Nature 425:859–864.
  • van Wijnen, A. J., G. S. Stein, J. P. Gergen, Y. Groner, S. W. Hiebert, Y. Ito, P. Liu, J. C. Neil, M. Ohki, and N. Speck. 2004. Nomenclature for Runt-related (RUNX) proteins. Oncogene 23:4209–4210.
  • Vodermaier, H. C. 2004. APC/C and SCF: controlling each other and the cell cycle. Curr. Biol. 14:R787–R796.
  • Wang, S., Y. Zhang, J. Soosairajah, and A. S. Kraft. Regulation of AML1 during the G2/M transition. Leukemia Res., in press.
  • Wang, Q., T. Stacy, M. Binder, M. Marin-Padilla, A. H. Sharpe, and N. A. Speck. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. USA 93:3444–3449.
  • Wang, X., C. Blagden, J. Fan, S. J. Nowak, I. Taniuchi, D. R. Littman, and S. J. Burden. 2005. Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev. 19:1715–1722.
  • Wasch, R., and D. Engelbert. 2005. Anaphase-promoting complex-dependent proteolysis of cell cycle regulators and genomic instability of cancer cells. Oncogene 24:1–10.
  • Wee, H. J., G. Huang, K. Shigesada, and Y. Ito. 2002. Serine phosphorylation of RUNX2 with novel potential functions as negative regulatory mechanisms. EMBO Rep. 3:967–974.
  • Wotton, S. F., K. Blyth, A. Kilbey, A. Jenkins, A. Terry, F. Bernardin-Fried, A. D. Friedman, E. W. Baxter, J. C. Neil, and E. R. Cameron. 2004. RUNX1 transformation of primary embryonic fibroblasts is revealed in the absence of p53. Oncogene 23:5476–5486.
  • Zhang, Y., J. R. Biggs, and A. S. Kraft. 2004. Phorbol ester treatment of K562 cells regulates the transcriptional activity of AML1c through phosphorylation. J. Biol. Chem. 279:53116–53125.

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.