20
Views
60
CrossRef citations to date
0
Altmetric
Article

Sumoylation of EKLF Promotes Transcriptional Repression and Is Involved in Inhibition of Megakaryopoiesis

, &
Pages 8547-8560 | Received 03 Apr 2007, Accepted 30 Sep 2007, Published online: 27 Mar 2023

REFERENCES

  • Ahringer, J. 2000. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16:351–356.
  • Armstrong, J. A., J. J. Bieker, and B. M. Emerson. 1998. A SWI/SNF-related chromatin remodeling complex, E-RC1, is required for tissue-specific transcriptional regulation by EKLF in vitro. Cell 95:93–104.
  • Besnault-Mascard, L., C. Leprince, M. T. Auffredou, B. Meunier, M. F. Bourgeade, J. Camonis, H. K. Lorenzo, and A. Vazquez. 2005. Caspase-8 sumoylation is associated with nuclear localization. Oncogene 24:3268–3273.
  • Bieker, J. 2001. EKLF and the development of the erythroid lineage, p. 71–84. In K. Ravid and J. D. Licht (ed.), Transcription factors: normal and malignant development of blood cells. Wiley Interscience, Hoboken, NJ.
  • Bieker, J. J. 2001. Kruppel-like factors: three fingers in many pies. J. Biol. Chem. 276:34355–34358.
  • Bieker, J. J., and C. M. Southwood. 1995. The erythroid Krüppel-like factor transactivation domain is a critical component for cell-specific inducibility of a β-globin promoter. Mol. Cell. Biol. 15:852–860.
  • Brand, M., J. A. Ranish, N. T. Kummer, J. Hamilton, K. Igarashi, C. Francastel, T. H. Chi, G. R. Crabtree, R. Aebersold, and M. Groudine. 2004. Dynamic changes in transcription factor complexes during erythroid differentiation revealed by quantitative proteomics. Nat. Struct. Mol. Biol. 11:73–80.
  • Chen, X., and J. J. Bieker. 2004. Stage-specific repression by the EKLF transcriptional activator. Mol. Cell. Biol. 24:10416–10424.
  • Chen, X., and J. J. Bieker. 2001. Unanticipated repression function linked to erythroid Krüppel-like factor. Mol. Cell. Biol. 21:3118–3125.
  • David, G., M. A. Neptune, and R. A. DePinho. 2002. SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J. Biol. Chem. 277:23658–23663.
  • Desterro, J. M., M. S. Rodriguez, and R. T. Hay. 1998. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell 2:233–239.
  • Donze, D., T. M. Townes, and J. J. Bieker. 1995. Role of erythroid Kruppel-like factor in human gamma- to beta-globin gene switching. J. Biol. Chem. 270:1955–1959.
  • Drissen, R., R. J. Palstra, N. Gillemans, E. Splinter, F. Grosveld, S. Philipsen, and W. de Laat. 2004. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev. 18:2485–2490.
  • Drissen, R., M. von Lindern, A. Kolbus, S. Driegen, P. Steinlein, H. Beug, F. Grosveld, and S. Philipsen. 2005. The erythroid phenotype of EKLF-null mice: defects in hemoglobin metabolism and membrane stability. Mol. Cell. Biol. 25:5205–5214.
  • Feng, W. C., C. M. Southwood, and J. J. Bieker. 1994. Analyses of beta-thalassemia mutant DNA interactions with erythroid Kruppel-like factor (EKLF), an erythroid cell-specific transcription factor. J. Biol. Chem. 269:1493–1500.
  • Frontelo, P., D. Manwani, M. Galdass, H. Karsunky, F. Lohmann, P. G. Gallagher, and J. J. Bieker. 22 August 2007. Novel role for EKLF in megakaryocyte lineage commitment. Blood [Epub ahead of print.] https://doi.org/10.1182/blood-2007-03-082065.
  • Fujita, N., D. L. Jaye, C. Geigerman, A. Akyildiz, M. R. Mooney, J. M. Boss, and P. A. Wade. 2004. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 119:75–86.
  • Funnell, A. P. W., C. A. Maloney, L. J. Thompson, J. Keys, M. Tallack, A. C. Perkins, and M. Crossley. 2007. Erythroid Krüppel-like factor directly activates the basic Krüppel-like factor gene in erythroid cells. Mol. Cell. Biol. 27:2777–2790.
  • Gill, G. 2003. Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr. Opin. Genet. Dev. 13:108–113.
  • Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18:2046–2059.
  • Girdwood, D., D. Bumpass, O. A. Vaughan, A. Thain, L. A. Anderson, A. W. Snowden, E. Garcia-Wilson, N. D. Perkins, and R. T. Hay. 2003. P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11:1043–1054.
  • Girdwood, D. W., M. H. Tatham, and R. T. Hay. 2004. SUMO and transcriptional regulation. Semin. Cell Dev. Biol. 15:201–210.
  • Gong, L., T. Kamitani, K. Fujise, L. S. Caskey, and E. T. Yeh. 1997. Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem. 272:28198–28201.
  • Hay, R. T. 2005. SUMO: a history of modification. Mol. Cell 18:1–12.
  • Hodge, D., E. Coghill, J. Keys, T. Maguire, B. Hartmann, A. McDowall, M. Weiss, S. Grimmond, and A. Perkins. 2006. A global role for EKLF in definitive and primitive erythropoiesis. Blood 107:3359–3370.
  • Hoege, C., B. Pfander, G. L. Moldovan, G. Pyrowolakis, and S. Jentsch. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141.
  • Hong, W., M. Nakazawa, Y. Y. Chen, R. Kori, C. R. Vakoc, C. Rakowski, and G. A. Blobel. 2005. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 24:2367–2378.
  • Johnson, E. S. 2004. Protein modification by SUMO. Annu. Rev. Biochem. 73:355–382.
  • Kadam, S., and B. M. Emerson. 2003. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11:377–389.
  • Kerscher, O., R. Felberbaum, and M. Hochstrasser. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22:159–180.
  • Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, R. Kingston, and K. Georgopoulos. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10:345–355.
  • Kirsh, O., J. S. Seeler, A. Pichler, A. Gast, S. Muller, E. Miska, M. Mathieu, A. Harel-Bellan, T. Kouzarides, F. Melchior, and A. Dejean. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. EMBO J. 21:2682–2691.
  • Kotaja, N., U. Karvonen, O. A. Jänne, and J. J. Palvimo. 2002. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22:5222–5234.
  • Kuhl, C., A. Atzberger, F. Iborra, B. Nieswandt, C. Porcher, and P. Vyas. 2005. GATA1-mediated megakaryocyte differentiation and growth control can be uncoupled and mapped to different domains in GATA1. Mol. Cell. Biol. 25:8592–8606.
  • Leight, E. R., D. Glossip, and K. Kornfeld. 2005. Sumoylation of LIN-1 promotes transcriptional repression and inhibition of vulval cell fates. Development 132:1047–1056.
  • Mahajan, M. C., G. J. Narlikar, G. Boyapaty, R. E. Kingston, and S. M. Weissman. 2005. Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the beta-globin locus control region. Proc. Natl. Acad. Sci. USA 102:15012–15017.
  • Miller, I. J., and J. J. Bieker. 1993. A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Krüppel family of nuclear proteins. Mol. Cell. Biol. 13:2776–2786.
  • Minty, A., X. Dumont, M. Kaghad, and D. Caput. 2000. Covalent modification of p73alpha by SUMO-1. Two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. J. Biol. Chem. 275:36316–36323.
  • Nuez, B., D. Michalovich, A. Bygrave, R. Ploemacher, and F. Grosveld. 1995. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375:316–318.
  • Ohi, M. D., C. W. Vander Kooi, J. A. Rosenberg, W. J. Chazin, and K. L. Gould. 2003. Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol 10:250–255.
  • O'Neill, D. W., S. S. Schoetz, R. A. Lopez, M. Castle, L. Rabinowitz, E. Shor, D. Krawchuk, M. G. Goll, M. Renz, H.-P. Seelig, S. Han, R. H. Seong, S. D. Park, T. Agalioti, N. Munshi, D. Thanos, H. Erdjument-Bromage, P. Tempst, and A. Bank. 2000. An Ikaros-containing chromatin-remodeling complex in adult-type erythroid cells. Mol. Cell. Biol. 20:7572–7582.
  • Orkin, S. H., H. H. Kazazian, Jr., S. E. Antonarakis, S. C. Goff, C. D. Boehm, J. P. Sexton, P. G. Waber, and P. J. Giardina. 1982. Linkage of beta-thalassaemia mutations and beta-globin gene polymorphisms with DNA polymorphisms in human beta-globin gene cluster. Nature 296:627–631.
  • Ouyang, L., X. Chen, and J. J. Bieker. 1998. Regulation of erythroid Kruppel-like factor (EKLF) transcriptional activity by phosphorylation of a protein kinase casein kinase II site within its interaction domain. J. Biol. Chem. 273:23019–23025.
  • Perkins, A. 1999. Erythroid Kruppel like factor: from fishing expedition to gourmet meal. Int. J. Biochem. Cell. Biol. 31:1175–1192.
  • Perkins, A. C., A. H. Sharpe, and S. H. Orkin. 1995. Lethal beta-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375:318–322.
  • Pichler, A., and F. Melchior. 2002. Ubiquitin-related modifier SUMO1 and nucleocytoplasmic transport. Traffic 3:381–387.
  • Pilon, A. M., D. G. Nilson, D. Zhou, J. Sangerman, T. M. Townes, D. M. Bodine, and P. G. Gallagher. 2006. Alterations in expression and chromatin configuration of the alpha hemoglobin-stabilizing protein gene in erythroid Krüppel-like factor-deficient mice. Mol. Cell. Biol. 26:4368–4377.
  • Quadrini, K. J., and J. J. Bieker. 2006. EKLF/KLF1 is ubiquitinated in vivo and its stability is regulated by activation domain sequences through the 26S proteasome. FEBS Lett. 580:2285–2293.
  • Ramirez-Carrozzi, V. R., A. A. Nazarian, C. C. Li, S. L. Gore, R. Sridharan, A. N. Imbalzano, and S. T. Smale. 2006. Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev. 20:282–296.
  • Rodriguez, M. S., J. M. Desterro, S. Lain, C. A. Midgley, D. P. Lane, and R. T. Hay. 1999. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 18:6455–6461.
  • Rodriguez, P., E. Bonte, J. Krijgsveld, K. E. Kolodziej, B. Guyot, A. J. Heck, P. Vyas, E. de Boer, F. Grosveld, and J. Strouboulis. 2005. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24:2354–2366.
  • Ross, S., J. L. Best, L. I. Zon, and G. Gill. 2002. SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol. Cell 10:831–842.
  • Shiio, Y., and R. N. Eisenman. 2003. Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 100:13225–13230.
  • Shyu, Y.-C., T.-L. Lee, C.-Y. Ting, S.-C. Wen, L.-J. Hsieh, Y.-C. Li, J.-L. Hwang, C.-C. Lin, and C.-K. Shen. 2005. Sumoylation of p45/NF-E2: nuclear positioning and transcriptional activation of the mammalian β-like globin gene locus. Mol. Cell. Biol. 25:10365–10378.
  • Southwood, C. M., K. M. Downs, and J. J. Bieker. 1996. Erythroid Kruppel-like factor exhibits an early and sequentially localized pattern of expression during mammalian erythroid ontogeny. Dev. Dyn. 206:248–259.
  • Tetteroo, P. A., F. Massaro, A. Mulder, R. Schreuder-van Gelder, and A. E. von dem Borne. 1984. Megakaryoblastic differentiation of proerythroblastic K562 cell-line cells. Leuk. Res. 8:197–206.
  • Weger, S., E. Hammer, and R. Heilbronn. 2004. SUMO-1 modification regulates the protein stability of the large regulatory protein Rep78 of adeno associated virus type 2 (AAV-2). Virology 330:284–294.
  • Yang, S. H., and A. D. Sharrocks. 2004. SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13:611–617.
  • Zhang, W., and J. J. Bieker. 1998. Acetylation and modulation of erythroid Kruppel-like factor (EKLF) activity by interaction with histone acetyltransferases. Proc. Natl. Acad. Sci. USA 95:9855–9860.
  • Zhang, W., S. Kadam, B. M. Emerson, and J. J. Bieker. 2001. Site-specific acetylation by p300 or CREB binding protein regulates erythroid Krüppel-like factor transcriptional activity via its interaction with the SWI-SNF complex. Mol. Cell. Biol. 21:2413–2422.
  • Zhang, Y., Y. Nagata, G. Yu, H. G. Nguyen, M. R. Jones, P. Toselli, C. W. Jackson, M. Tatsuka, K. Todokoro, and K. Ravid. 2004. Aberrant quantity and localization of Aurora-B/AIM-1 and survivin during megakaryocyte polyploidization and the consequences of Aurora-B/AIM-1-deregulated expression. Blood 103:3717–3726.
  • Zhao, J. 4 September 2007. Sumoylation regulates diverse biological processes. Cell Mol. Life Sci. [Epub ahead of print.] https://doi.org/10.1007/s00018-007-7137-4.
  • Zheng, N., P. Wang, P. D. Jeffrey, and N. P. Pavletich. 2000. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102:533–539.

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.