Interaction and cooperation of the CCAAT-box enhancer-binding protein β (C/EBPβ) with the homeodomain-interacting protein kinase 2 (Hipk2)

Journal of Biological Chemistry

Volumn 288, Issue 31, 2013, Pages 22257-22269

  Steinmann, Simone ^a   Coulibaly, Anna ^a   Ohnheiser, Johanna ^a   Jakobs, Anke ^a   Klempnauer, Karl Heinz ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BZIP TRANSCRIPTION FACTORS; DIRECT INTERACTIONS; ENHANCER-BINDING PROTEINS; HOMEODOMAIN-INTERACTING PROTEIN KINASE 2; ISOFORMS; PHYSIOLOGICAL SUBSTRATE; PROTEIN KINASE;

ENZYMES; PHOSPHORYLATION;

PROTEINS;

CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; E1A ASSOCIATED P300 PROTEIN; HOMEODOMAIN INTERACTING PROTEIN KINASE 2;

ADIPOCYTE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL STRAIN 3T3; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

C/EBPΒ; HIPK2; P300; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-PROTEIN INTERACTIONS; TRANSCRIPTION;

3T3-L1 CELLS; AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CELL LINE; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84881221535     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.487769     Document Type: Article

References (53)

1. Cao, Z., Umek, R. M., and McKnight, S. L. (1991) Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 5, 1538-1552
2. Lin, F.-T., and Lane, M. D. (1992) Antisense CCAAT/enhancer-binding protein RNA suppresses coordinate gene expression and triglyceride accumulation during differentiation of 3T3-L1 preadipocytes. Genes Dev. 6, 533-544
3. Müller, C., Kowenz-Leutz, E., Grieser-Ade, S., Graf, T., and Leutz, A. (1995) NF-M (chicken C/EBPβ) induces eosinophilic differentiation and apoptosis in a hematopoietic progenitor cell line. EMBO J. 14, 6127-6235
4. Yeh, W.-C., Cao, Z., Classon, M., and McKnight, S. L. (1995) Cascade regulation of terminal adipocyte differentiation by three members of the C/EBP family of leucine zipper proteins. Genes Dev. 9, 168-181
5. Zhang, D. E., Zhang, P., Wang, N. D., Hetherington, C. J., Darlington, G. J., and Tenen, D. G. (1997) Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer-binding protein β-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 94, 569-574
6. Pedersen, T. A., Kowenz-Leutz, E., Leutz, A., and Nerlov, C. (2001) Cooperation between C/EBPβ, TBP/TFIIB, and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev. 15, 3208-3216
7. Ramji, D. P., and Foka, P. (2002) CCAAT/enhancer-binding proteins. Structure, function, and regulation. Biochem. J. 365, 561-575
8. Tang, Q. Q., Otto, T. C., and Lane, M. D. (2003) CCAAT/enhancer-binding proteinβ is required for mitotic clonal expansion during adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 850-855
9. Nerlov, C. (2007) The C/EBP family of transcription factors. A paradigm for interaction between gene expression and proliferation control. Trends Cell Biol. 17, 318-324
10. Descombes, P., and Schibler, U. (1991) A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67, 569-579
11. Calkhoven, C. F., Müller, C., and Leutz, A. (2000) Translational control of C/EBPβ and C/EBPβ isoform expression. Genes Dev. 14, 1920-1932
12. Ossipow, V., Descombes, P., and Schibler, U. (1993) CCAAT/enhancerbinding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc. Natl. Acad. Sci. U.S.A. 90, 8219-8223
13. Raught, B., Gingras, A. C., James, A., Medina, D., Sonenberg, N., and Rosen, J. M. (1996) Expression of a translationally regulated, dominantnegative CCAAT/enhancer-binding protein β isoform and up-regulation of the eukaryotic translation initiation factor 2-are correlated with neoplastic transformation of mammary epithelial cells. Cancer Res. 56, 4382-4386
14. Lincoln, A. J., Monczak, Y., Williams, S. C., and Johnson, P. F. (1998) Inhibition of CCAAT/enhancer-binding protein β and β translation by upstream open reading frames. J. Biol. Chem. 273, 9552-9560
15. Wethmar, K., Bégay, V., Smink, J. J., Zaragoza, K., Wiesenthal, V., Dörken, B., Calkhoven, C. F., and Leutz, A. (2010) C/EBPβδ uORF Mice. A genetic model for uORF-mediated translational control in mammals. Genes Dev. 24, 15-20
16. Nakajima, T., Kinoshita, S., Sasagawa, T., Sasaki, K., Naruto, M., Kishimoto, T., and Akira, S. (1993) Phosphorylation at threonine 235 by a ras-dependent mitogen-activated protein kinase cascade is essential for transcription factor NF-IL6. Proc. Natl. Acad. Sci. U.S.A. 90, 2207-2211
17. Trautwein, C., Caelles, C., van der Geer, P., Hunter, T., Karin, M., and Chojkier, M. (1993) Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain. Nature 364, 544-547
18. Buck, M., Poli, V., van der Geer, P., Chojkier, M., and Hunter, T. (1999) Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBP β is required for hepatocyte proliferation induced by TGFα. Mol. Cell 4, 1087-1092
19. Ceseña, T. I., Cardinaux, J. R., Kwok, R., and Schwartz, J. (2007) CCAAT/enhancer-binding protein (C/EBP) β is acetylated at multiple lysines. Acetylation of C/EBPβ at lysine 39 modulates its ability to activate transcription. J. Biol. Chem. 282, 956-967
20. Joo, M., Park, G.Y., Wright, J. G., Blackwell, T. S., Atchison, M. L., and Christman, J. W. (2004) Transcriptional regulation of the cyclooxygenase-2 gene in macrophages by PU. 1. J. Biol. Chem. 279, 6658-6665
21. Xu, M., Nie, L., Kim, S. H., and Sun, X. H. (2003) STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPβ. EMBO J. 22, 893-904
22. Eaton, E. M., and Sealy, L. (2003) Modification of CCAAT/enhancerbinding protein-β by the small ubiquitin-like modifier (SUMO) family members, SUMO-2 and SUMO-3. J. Biol. Chem. 278, 33416-33421
23. Mink, S., Haenig, B., and Klempnauer, K.-H. (1997) Interaction and functional collaboration of p300 and C/EBPβ. Mol. Cell. Biol. 17, 6609-6617
24. Kowenz-Leutz, E., Twamley, G., Ansieau, S., and Leutz, A. (1994) Novel mechanism of C/EBPβ (NF-M) transcriptional control. Activation through derepression. Genes Dev. 8, 2781-2791
25. Johnson, P. F. (2005) Molecular stop signs. Regulation of cell-cycle arrest by C/EBP transcription factors. J. Cell Sci. 118, 2545-2555
26. Pless, O., Kowenz-Leutz, E., Knoblich, M., Lausen, J., Beyermann, M., Walsh, M. J., and Leutz, A. (2008) G9a-mediated lysine methylation alters the function of CCAAT/enhancer-binding protein-β. J. Biol. Chem. 283, 26357-26363
27. Kowenz-Leutz, E., Pless, O., Dittmar, G., Knoblich, M., and Leutz, A. (2010) Crosstalk between C/EBPβ phosphorylation, arginine methylation, and SWI/SNF/Mediator implies an indexing transcription factor code. EMBO J. 29, 1105-1115
28. Zahnow, C. A., Cardiff, R. D., Laucirica, R., Medina, D., and Rosen, J. M. (2001) A role for CCAAT/enhancer-binding protein β-liver-enriched inhibitory protein in mammary epithelial cell proliferation. Cancer Res. 61, 261-269
29. Bundy, L. M., and Sealy, L. (2003) CCAAT/enhancer-binding protein-β (C/EBPβ)-2 transforms normal mammary epithelial cells and induces epithelial to mesenchymal transition in culture. Oncogene 22, 869-883
30. Nerlov, C. (2004) C/EBPβ mutations in acute myeloid leukemias. Nat. Rev. Cancer 4, 394-400
31. Gomis, R. R., Alarcón, C., Nadal, C., Van Poznak, C., and Massagué, J. (2006) C/EBPβ at the core of the TGFα cytostatic response and its evasion in metastatic breast cancer cells. Cancer Cell 10, 203-214
32. Schwartz, C., Beck, K., Mink, S., Schmolke, M., Budde, B., Wenning, D., and Klempnauer K.-H. (2003) Recruitment of p300 by C/EBPβ triggers phosphorylation of p300 and modulates coactivator activity. EMBO J. 22, 882-892
33. Steinmann, S., Schulte, K., Beck, K., Chachra, S., Bujnicki, T., and Klempnauer, K.-H. (2009) v-Myc inhibits C/EBPβ activity by preventing C/EBPα-induced phosphorylation of the co-activator p300. Oncogene 28, 2446-2455
34. Lane, M. D., Tang, Q. Q., and Jiang, M. S. (1999) Role of the CCAAT enhancer-binding proteins (C/EBPs) in adipocyte differentiation. Biochem. Biophys. Res. Commun. 266, 677-683
35. Plachetka, A., Chayka, O., Wilczek, C., Melnik, S., Bonifer, C., and Klempnauer, K.-H. (2008) C/EBPβ induces chromatin opening at a cell-typespecific enhancer. Mol. Cell. Biol. 28, 2102-2112
36. Hofmann, T. G., Möller, A., Sirma, H., Zentgraf, H., Taya, Y., Dröge, W., Will, H., and Schmitz, M. L. (2002) Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat. Cell Biol. 4, 1-10
37. Schubert, S., Horstmann, S., Bartusel, T., and Klempnauer, K.-H. (2004) The cooperation of B-Myb with the coactivator p300 is orchestrated by cyclins A and D1. Oncogene 23, 1392-1404
38. D'Orazi, G., Cecchinelli, B., Bruno, T., Manni, I., Higashimoto, Y., Saito, S., Gostissa, M., Coen, S., Marchetti, A., Del Sal, G., Piaggio, G., Fanciulli, M., Appella, E., and Soddu, S. (2002) Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser-46 and mediates apoptosis. Nat. Cell Biol. 4, 11-19
39. Choi, C. Y., Kim, Y. H., Kim, Y. O., Park, S. J., Kim, E. A., Riemenschneider, W., Gajewski, K., Schulz, R. A., and Kim, Y. (2005) Phosphorylation by the DHIPK2 protein kinase modulates the corepressor activity of Groucho. J. Biol. Chem. 280, 21427-22136
40. Aikawa, Y., Nguyen, L. A., Isono, K., Takakura, N., Tagata, Y., Schmitz, M. L., Koseki, H., and Kitabayashi, I. (2006) Roles of HIPK1 and HIPK2 in AML1-and p300-dependent transcription, hematopoiesis and blood vessel formation. EMBO J. 25, 3955-3965
41. Kim, E. A., Noh, Y. T., Ryu, M. J., Kim, H. T., Lee, S. E., Kim, C. H., Lee, C., Kim, Y. H., and Choi, C. Y. (2006) Phosphorylation and transactivation of Pax6 by homeodomain-interacting protein kinase 2. J. Biol. Chem. 281, 7489-7497
42. Zhang, Q., and Wang, Y. (2007) Homeodomain-interacting protein kinase-2 (HIPK2) phosphorylates HMGA1a at Ser-35, Thr-52, and Thr-77 and modulates its DNA binding affinity. J. Proteome Res. 6, 4711-4719
43. Otto, T. C., and Lane, M. D. (2005) Adipose development. From stem cell to adipocyte. Crit. Rev. Biochem. Mol. Biol. 40, 229-242
44. Tang, Q. Q., Grønborg, M., Huang, H., Kim, J.-W., Otto, T. C., Pandey, A., and Lane, M. D. (2005) Sequential phosphorylation of CCAAT enhancerbinding protein-β by MAPK and glycogen synthase kinase 3b is required for adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 9766-9771
45. Li, X., Kim, J. W., Grønborg, M., Urlaub, H., Lane, M. D., and Tang, Q. Q. (2007) Role of cdk2 in the sequential phosphorylation/activation of C/EBPβ during adipocyte differentiation. Proc. Natl. Acad. Sci. U.S.A. 104, 11597-11602
46. Trivedi, A. K., Bararia, D., Christopeit, M., Peerzada, A. A., Singh, S. M., Kieser, A., Hiddemann, W., Behre, H. M., and Behre, G. (2007) Proteomic identification of C/EBP-DBD multiprotein complex. JNK1 activates stem cell regulator C/EBPβ by inhibiting its ubiquitination. Oncogene 26, 1789-1801
47. Ross, S. E., Radomska, H. S., Wu, B., Zhang, P., Winnay, J. N., Bajnok, L., Wright, W. S., Schaufele, F., Tenen, D. G., and MacDougald, O. A. (2004) Phosphorylation of C/EBPβ inhibits granulopoiesis. Mol. Cell. Biol. 24, 675-686
48. Shuman, J. D., Sebastian, T., Kaldis, P., Copeland, T. D., Zhu, S., Smart, R. C., and Johnson, P. F. (2004) Cell cycle-dependent phosphorylation of C/EBPβ mediates oncogenic cooperativity between C/EBPβ and H-RasV12. Mol. Cell. Biol. 24, 7380-7391
49. Mo, X., Kowenz-Leutz, E., Xu, H., and Leutz, A. (2004) Ras induces mediator complex exchange on C/EBP β. Mol. Cell 13, 241-250
50. Atwood, A. A., and Sealy, L. (2010) Regulation of C/EBPβ1 by Ras in mammary epithelial cells and the role of C/EBPβ1 in oncogene-induced senescence. Oncogene 29, 6004-6015
51. Smink, J. J., and Leutz, A. (2012) Instruction of mesenchymal cell fate by the transcription factor C/EBPβ. Gene 497, 10-17
52. Kowenz-Leutz, E., and Leutz, A. (1999) A C/EBP β isoform recruits the SWI/SNF complex to activate myeloid genes. Mol. Cell 4, 735-743
53. Erickson, R. L., Hemati, N., Ross, S. E., and MacDougald, O. A. (2001) p300 coactivates the adipogenic transcription factor CCAAT/enhancer-binding protein β. J. Biol. Chem. 276, 16348-16355