Target proteins of C/EBPαp30 in AML: C/EBPαp30 enhances sumoylation of C/EBPαp42 via up-regulation of Ubc9

Blood

Volumn 110, Issue 9, 2007, Pages 3301-3309

  Geletu, Mulu ^a   Balkhi, Mumtaz Y ^a   Peer Zada, Abdul A ^a   Christopeit, Maximilian ^a   Pulikkan, John A ^a   Trivedi, Arun K ^a   Tenen, Daniel G ^b   Behre, Gerhard ^a,c  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b HARVARD INSTITUTES OF MEDICINE   (United States)

^c MARTIN LUTHER UNIVERSITÄT HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CD34 ANTIGEN; GRANULOCYTE COLONY STIMULATING FACTOR; PROTEIN P30; PROTEIN P42; PROTEIN UBC9; SMALL INTERFERING RNA;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE MUTATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GRANULOCYTE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN TARGETING; SUMOYLATION; TRANSACTIVATION; UPREGULATION;

EID: 36148968960     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-01-071035     Document Type: Article

References (52)

1. Radomska HS, Huettner CS, Zhang P, Cheng T, Scadden DT, Tenen DG. CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol. 1998;18:4301-4314.
2. Behre G, Singh SM, Liu H, et al. Ras signaling enhances the activity of C/EBP alpha to induce granulocytic differentiation by phosphorylation of serine 248. J Biol Chem. 2002;277:26293-26299.
3. Scott LM, Civin CI, Rorth P, Friedman AD. A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells. Blood. 1992;80:1725-1735.
4. Pabst T, Mueller BU, Harakawa N, et al. AML1-ETO downregulates the granulocytic differentiation factor C/EBPalpha in t(8;21) myeloid leukemia. Nat Med. 2001;7:444-451.
5. Pabst T, Mueller BU, Zhang P, et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-alpha (C/EBPalpha), in acute myeloid leukemia. Nat Genet. 2001;27:263-270.
6. Preudhomme C, Sagot C, Boissel N, et al. Favorable prognostic significance of CEBPA mutations in patients with de novo acute myeloid leukemia: a study from the Acute Leukemia French Association (ALFA). Blood. 2002;100:2717-2723.
7. Gombart AF, Hofmann WK, Kawano S, et al. Mutations in the gene encoding the transcription factor CCAAT/enhancer binding protein alpha in myelodysplastic syndromes and acute myeloid leukemias. Blood. 2002;99:1332-1340.
8. Lin FT, MacDougald OA, Diehl AM, Lane MD. A 30-kDa alternative translation product of the CCAAT/enhancer binding protein alpha message: transcriptional activator lacking antimitotic activity. Proc Natl Acad Sci U S A. 1993;90:9606-9610.
9. Cleaves R, Wang QF, Friedman AD. C/EBPalphap30, a myeloid leukemia oncoprotein, limits G-CSF receptor expression but not terminal granulopoiesis via site-selective inhibition of C/EBP DNA binding. Oncogene. 2004;23:716-725.
10. D'Alo F, Johansen LM, Nelson EA, et al. The amino terminal and E2F interaction domains are critical for C/EBP alpha-mediated induction of granulopoietic development of hematopoietic cells. Blood. 2003;102:3163-3171.
11. Paz-Priel I, Cai DH, Wang D, et al. CCAAT/enhancer binding protein alpha (C/EBPalpha) and C/EBPalpha myeloid oncoproteins induce bcl-2 via interaction of their basic regions with nuclear factor-kappaB p50. Mol Cancer Res. 2005;3:585-596.
12. Johnson ES, Blobel G. Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J Biol Chem. 1997;272:26799-26802.
13. Schwarz SE, Matuschewski K, Liakopoulos D, Scheffner M, Jentsch S. The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme. Proc Natl Acad Sci U S A. 1998;95:560-564.
14. Dieckhoff P, Bolte M, Sancak Y, Braus GH, Irniger S. Smt3/SUMO and Ubc9 are required for efficient APC/C-mediated proteolysis in budding yeast. Mol Microbiol. 2004;51:1375-1387.
15. Seufert W, Futcher B, Jentsch S. Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature. 1995;373:78-81.
16. Spence J, Sadis S, Haas AL, Finley D. A ubiquitin mutant with specific defects in DNA repair and multiubiquitination. Mol Cell Biol. 1995;15:1265-1273.
17. al-Khodairy F, Enoch T, Hagan IM, Carr AM. The Schizosaccharomyces pombe hus5 gene encodes a ubiquitin conjugating enzyme required for normal mitosis. J Cell Sci. 1995;108:475-486.
18. Mo YY, Yu Y, Theodosiou E, Rachel Ee PL, Beck WT. A role for Ubc9 in tumorigenesis. Oncogene. 2005;24:2677-2683.
19. Mo YY, Moschos SJ. Targeting Ubc9 for cancer therapy. Expert Opin Ther Targets. 2005;9:1203-1216.
20. Mao Y, Desai SD, Liu LF. SUMO-1 conjugation to human DNA topoisomerase II isozymes. J Biol Chem. 2000;275:26066-26073.
21. Rodriguez MS, Desterro JM, Lain S, Midgley CA, Lane DP, Hay RT. SUMO-1 modification activates the transcriptional response of p53. EMBO J. 1999;18:6455-6461.
22. Gostissa M, Hengstermann A, Fogal V, et al. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J. 1999;18:6462-6471.
23. Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ. Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system. Genomics. 1996;37:183-186.
24. Schmidt D, Muller S. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci U S A. 2002;99:2872-2877.
25. Subramanian L, Benson MD, Iniguez-Lluhi JA. A synergy control motif within the attenuator domain of CCAAT/enhancer-binding protein alpha inhibits transcriptional synergy through its PIASy-enhanced modification by SUMO-1 or SUMO-3. J Biol Chem. 2003;278:9134-9141.
26. Sato Y, Miyake K, Kaneoka H, Iijima S. Sumoylation of CCAAT/enhancer-binding protein alpha and its functional roles in hepatocyte differentiation. J Biol Chem. 2006;281:21629-21639.
27. Ross SE, Radomska HS, Wu B, et al. Phosphorylation of C/EBPalpha inhibits granulopoiesis. Mol Cell Biol. 2004;24:675-686.
28. Behre G, Smith LT, Tenen DG. Use of a promoterless Renilla luciferase vector as an internal control plasmid for transient co-transfection assays of Ras-mediated transcription activation. Biotechniques. 1999;26:24-26,28.
29. Zada AA, Singh SM, Reddy VA, et al. Downregulation of c-Jun expression and cell cycle regulatory molecules in acute myeloid leukemia cells upon CD44 ligation. Oncogene. 2003;22:2296-2308.
30. Balkhi MY, Trivedi AK, Geletu M, et al. Proteomics of acute myeloid leukaemia: cytogenetic risk groups differ specifically in their proteome, interactome and post-translational protein modifications. Oncogene. 2006;25:7041-7058.
31. Erickson RL, Hemati N, Ross SE, MacDougald OA. p300 coactivates the adipogenic transcription factor CCAAT/enhancer-binding protein alpha. J Biol Chem. 2001;276:16348-16355.
32. Callewaert L, Verrijdt G, Haelens A, Claessens F. Differential effect of small ubiquitin-like modifier (SUMO)-ylation of the androgen receptor in the control of cooperativity on selective versus canonical response elements. Mol Endocrinol. 2004;18:1438-1449.
33. Schwieger M, Lohler J, Fischer M, Herwig U, Tenen DG, Stocking C. A dominant-negative mutant of C/EBPalpha, associated with acute myeloid leukemias, inhibits differentiation of myeloid and erythroid progenitors of man but not mouse. Blood. 2004;103:2744-2752.
34. Nakagawa K, Kuzumaki N. Transcriptional activity of megakaryoblastic leukemia 1 (MKL1) is repressed by SUMO modification. Genes Cells. 2005;10:835-850.
35. Chakrabarti SR, Sood R, Nandi S, Nucifora G. Posttranslational modification of TEL and TEL/AML1 by SUMO-1 and cell-cycle-dependent assembly into nuclear bodies. Proc Natl Acad Sci U S A. 2000;97:13281-13285.
36. Verger A, Perdomo J, Crossley M. Modification with SUMO: a role in transcriptional regulation. EMBO Rep. 2003;4:137-142.
37. Gill G. Something about SUMO inhibits transcription. Curr Opin Genet Dev. 2005;15:536-541.
38. Johnson ES. Protein modification by SUMO. Annu Rev Biochem. 2004;73:355-382.
39. Kuo HY, Chang CC, Jeng JC, et al. SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci U S A. 2005;102:16973-16978.
40. Girdwood DW, Tatham MH, Hay RT. SUMO and transcriptional regulation. Semin Cell Dev Biol. 2004;15:201-210.
41. Kim J, Cantwell CA, Johnson PF, Pfarr CM, Williams SC. Transcriptional activity of CCAAT/enhancer-binding proteins is controlled by a conserved inhibitory domain that is a target for sumoylation. J Biol Chem. 2002;277:38037-38044.
42. Radomska HS, Basseres DS, Zheng R, et al. Block of C/EBP alpha function by phosphorylation in acute myeloid leukemia with FLT3 activating mutations. J Exp Med. 2006;203:371-381.
43. Holmstrom S, Van Antwerp ME, Iniguez-Lluhi JA. Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc Natl Acad Sci U S A. 2003;100:15758-15763.
44. Chupreta S, Holmstrom S, Subramanian L, Iniguez-Lluhi JA. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol Cell Biol. 2005;25:4272-4282.
45. Gill G. Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr Opin Genet Dev. 2003;13:108-113.
46. Matunis MJ, Coutavas E, Blobel G. A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol. 1996;135:1457-1470.
47. Lin X, Liang M, Liang YY, Brunicardi FC, Feng XH. SUMO-1/Ubc9 promotes nuclear accumulation and metabolic stability of tumor suppressor Smad4. J Biol Chem. 2003;278:31043-31048.
48. Wang QF, Friedman AD. CCAAT/enhancer-binding proteins are required for granulopoiesis independent of their induction of the granulocyte colony-stimulating factor receptor. Blood. 2002;99:2776-2785.
49. Iwama A, Osawa M, Hirasawa R, et al. Reciprocal roles for CCAAT/enhancer binding protein (C/EBP) and PU. 1 transcription factors in Langerhans cell commitment. J Exp Med. 2002;195:547-558.
50. Moschos SJ, Smith AP, Mandic M, et al. SAGE and antibody array analysis of melanoma-infiltrated lymph nodes: identification of Ubc9 as an important molecule in advanced-stage melanomas. Oncogene. 2007;26:4216-4225.
51. Nacerddine K, Lehembre F, Bhaumik M, et al. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell. 2005;9:769-779.
52. Nowak M, Hammerschmidt M. Ubc9 regulates mitosis and cell survival during zebrafish development. Mol Biol Cell. 2006;17:5324-5336.