RSK-mediated phosphorylation in the C/EBPβ leucine zipper regulates DNA binding, dimerization, and growth arrest activity

Molecular and Cellular Biology

Volumn 30, Issue 11, 2010, Pages 2621-2635

  Lee, Sook ^a   Shuman, Jon D ^a,e   Guszczynski, Tad ^a   Sakchaisri, Krisada ^a   Sebastian, Thomas ^a   Copeland, Terry D ^a   Miller, Maria ^a   Cohen, Michael S ^b   Taunton, Jack ^b   Smart, Robert C ^c   Xiao, Zhen ^d   Yu, Li Rong ^d,f   Veenstra, Timothy D ^d   Johnson, Peter F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d SAIC FREDERICK INC   (United States)

^e Brewton Parker College   (United States)

^f NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; HOMODIMER; LEUCINE ZIPPER PROTEIN; RAS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; DNA BINDING; ELECTRICITY; GROWTH DISORDER; HUMAN; HUMAN CELL; METHYLATION; MUTATION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL CYCLE; CELL LINE; DNA; GROWTH SUBSTANCES; HUMANS; LEUCINE ZIPPERS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RAS PROTEINS; RATS; RIBOSOMAL PROTEIN S6 KINASES; SEQUENCE ALIGNMENT; TRANSCRIPTIONAL ACTIVATION;

EID: 77952620263     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00782-09     Document Type: Article

References (50)

1. Akira, S., H. Isshiki, T. Sugita, O. Tanabe, S. Kinoshita, Y. Nishio, T. Nakajima, T. Hirano, and T. Kishimoto. 1990. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 9:1897-1906. (Pubitemid 20170023)
2. Bedford, M. T., and S. G. Clarke. 2009. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33:1-13.
3. Buck, M., V. Poli, T. Hunter, and M. Chojkier. 2001. C/EBPbeta phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol. Cell 8:807-816. (Pubitemid 33030214)
4. Buck, M., V. Poli, P. van der Geer, M. Chojkier, and T. Hunter. 1999. Phosphorylation of rat serine 105 or mouse threonine 217 in C/EBP beta is required for hepatocyte proliferation induced by TGF alpha. Mol. Cell 4:1087-1092. (Pubitemid 30054914)
5. Buck, M., H. Turler, and M. Chojkier. 1994. LAP (NF-IL-6), a tissue-specific transcriptional activator, is an inhibitor of hepatoma cell proliferation. EMBO J. 13:851-860. (Pubitemid 24057516)
6. Bundy, L. M., and L. Sealy. 2003. CCAAT/enhancer binding protein beta (C/EBPbeta)-2 transforms normal mammary epithelial cells and induces epithelial to mesenchymal transition in culture. Oncogene 22:869-883.
7. Campbell, S. L., R. Khosravi-Far, K. L. Rossman, G. J. Clark, and C. J. Der. 1998. Increasing complexity of Ras signaling. Oncogene 17:1395-1413.
8. Chinery, R., J. A. Brockman, D. T. Dransfield, and R. J. Coffey. 1997. Antioxidant-induced nuclear translocation of CCAAT/enhancer-binding protein beta. A critical role for protein kinase A-mediated phosphorylation of Ser299. J. Biol. Chem. 272:30356-30361. (Erratum, J. Biol. Chem. 273: 15308, 1998.)
9. Cohen, M. S., C. Zhang, K. M. Shokat, and J. Taunton. 2005. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 308:1318-1321.
10. Cooper, C., A. Henderson, S. Artandi, N. Avitahl, and K. Calame. 1995. Ig/EBP (C/EBP gamma) is a transdominant negative inhibitor of C/EBP family transcriptional activators. Nucleic Acids Res. 23:4371-4377.
11. Dalby, K. N., N. Morrice, F. B. Caudwell, J. Avruch, and P. Cohen. 1998. Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK. J. Biol. Chem. 273:1496-1505.
12. Descombes, P., and U. Schibler. 1991. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 67:569-579. (Pubitemid 121001471)
13. Fan, H. Y., Z. Liu, M. Shimada, E. Sterneck, P. F. Johnson, S. M. Hedrick, and J. S. Richards. 2009. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324:938-941.
14. Gomis, R. R., C. Alarcon, C. Nadal, C. Van Poznak, and J. Massague. 2006. C/EBPbeta at the core of the TGFbeta cytostatic response and its evasion in metastatic breast cancer cells. Cancer Cell 10:203-214.
15. Greenbaum, L. E., W. Li, D. E. Cressman, Y. Peng, G. Ciliberto, V. Poli, and R. Taub. 1998. CCAAT enhancer-binding protein beta is required for normal hepatocyte proliferation in mice after partial hepatectomy. J. Clin. Invest. 102:996-1007.
16. Hattori, T., N. Ohoka, Y. Inoue, H. Hayashi, and K. Onozaki. 2003. C/EBP family transcription factors are degraded by the proteasome but stabilized by forming dimer. Oncogene 22:1273-1280. (Pubitemid 36384589)
17. Huang, J., and S. L. Berger. 2008. The emerging field of dynamic lysine methylation of non-histone proteins. Curr. Opin. Genet. Dev. 18:152-158.
18. Kowenz-Leutz, E., G. Twamley, S. Ansieau, and A. Leutz. 1994. Novel mechanism of C/EBP β (NF-M) transcriptional control: activation through derepression. Genes Dev. 8:2781-2791. (Pubitemid 24375426)
19. Krylov, D., I. Mikhailenko, and C. Vinson. 1994. A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions. EMBO J. 13:2849-2861. (Pubitemid 24191695)
20. Kuilman, T., C. Michaloglou, L. C. Vredeveld, S. Douma, R. van Doorn, C. J. Desmet, L. A. Aarden, W. J. Mooi, and D. S. Peeper. 2008. Oncogeneinduced senescence relayed by an interleukin-dependent inflammatory network. Cell 133:1019-1031. (Pubitemid 351787746)
21. Lee, S. J., and S. G. Kim. 2006. Role of p90 ribosomal S6-kinase-1 in oltipraz-induced specific phosphorylation of CCAAT/enhancer binding protein-beta for GSTA2 gene transactivation. Mol. Pharmacol. 69:385-396.
22. McKnight, S. L., and R. Kingsbury. 1982. Transcriptional control signals of a eukaryotic protein-coding gene. Science 217:316-324. (Pubitemid 12090729)
23. Mo, X., E. Kowenz-Leutz, H. Xu, and A. Leutz. 2004. Ras induces mediator complex exchange on C/EBP beta. Mol. Cell 13:241-250. (Pubitemid 38183270)
24. Nakajima, T., S. Kinoshita, T. Sasagawa, K. Sasaki, M. Naruto, T. Kishimoto, and S. Akira. 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.
25. Newman, J. R., and A. E. Keating. 2003. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097-2101.
26. Parkin, S. E., M. Baer, T. D. Copeland, R. C. Schwartz, and P. F. Johnson. 2002. Regulation of CCAAT/enhancer-binding protein (C/EBP) activator proteins by heterodimerization with C/EBPgamma (Ig/EBP). J. Biol. Chem. 277:23563-23572.
27. Piwien-Pilipuk, G., O. MacDougald, and J. Schwartz. 2002. Dual regulation of phosphorylation and dephosphorylation of C/EBPbeta modulate its transcriptional activation and DNA binding in response to growth hormone. J. Biol. Chem. 277:44557-44565.
28. Piwien-Pilipuk, G., D. Van Mater, S. E. Ross, O. A. MacDougald, and J. Schwartz. 2001. Growth hormone regulates phosphorylation and function of CCAAT/enhancer-binding protein beta by modulating Akt and glycogen synthase kinase-3. J. Biol. Chem. 276:19664-19671.
29. Ramji, D. P., and P. Foka. 2002. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365:561-575. (Pubitemid 34864439)
30. Robinson, G. W., P. F. Johnson, L. Hennighausen, and E. Sterneck. 1998. The C/EBPbeta transcription factor regulates epithelial cell proliferation and differentiation in the mammary gland. Genes Dev. 12:1907-1916.
31. Sapkota, G. P., L. Cummings, F. S. Newell, C. Armstrong, J. Bain, M. Frodin, M. Grauert, M. Hoffmann, G. Schnapp, M. Steegmaier, P. Cohen, and D. R. Alessi. 2007. BI-D1870 is a specific inhibitor of the p90 RSK (ribosomal S6 kinase) isoforms in vitro and in vivo. Biochem. J. 401:29-38.
32. Seagroves, T. N., S. Krnacik, B. Raught, J. Gay, B. Burgess-Beusse, G. J. Darlington, and J. M. Rosen. 1998. C/EBPbeta, but not C/EBPalpha, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev. 12:1917-1928.
33. Sebastian, T., and P. F. Johnson. 2009. RasV12-mediated down-regulation of CCAAT/enhancer binding protein {beta} in immortalized fibroblasts requires loss of p19Arf and facilitates bypass of oncogene-induced senescence. Cancer Res. 69:2588-2598.
34. Sebastian, T., and P. F. Johnson. 2006. Stop and go: anti-proliferative and mitogenic functions of the transcription factor C/EBPbeta. Cell Cycle 5:953-957.
35. Sebastian, T., R. Malik, S. Thomas, J. Sage, and P. F. Johnson. 2005. C/EBPbeta cooperates with RB:E2F to implement Ras(V12)-induced cellular senescence. EMBO J. 24:3301-3312.
36. Serrano, M., A. W. Lin, M. E. McCurrach, D. Beach, and S. W. Lowe. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602. (Pubitemid 27152402)
37. 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/EBPbeta mediates oncogenic cooperativity between C/EBPbeta and H-RasV12. Mol. Cell. Biol. 24:7380-7391.
38. Szilák, L., J. Moitra, and C. Vinson. 1997. Design of a leucine zipper coiled coil stabilized 1.4 kcal mol-1 by phosphorylation of a serine in the e position. Protein Sci. 6:1273-1283. (Pubitemid 27260161)
39. Tang, Q. Q., M. Gronborg, H. Huang, J. W. Kim, T. C. Otto, A. Pandey, and M. D. Lane. 2005. Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 102:9766-9771.
40. Tang, Q. Q., and M. D. Lane. 1999. Activation and centromeric localization of CCAAT/enhancer-binding proteins during the mitotic clonal expansion of adipocyte differentiation. Genes Dev. 13:2231-2241.
41. Tang, Q. Q., T. C. Otto, and M. D. Lane. 2003. CCAAT/enhancer-binding protein beta is required for mitotic clonal expansion during adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:850-855.
42. Tang, Q. Q., T. C. Otto, and M. D. Lane. 2003. Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:44-49.
43. Vinson, C., M. Myakishev, A. Acharya, A. A. Mir, J. R. Moll, and M. Bonovich. 2002. Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22:6321-6335.
44. Vinson, C. R., T. W. Hai, and S. M. Boyd. 1993. Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Genes Dev. 7:1047-1058.
45. Wada, N., M. Matsumura, Y. Ohba, N. Kobayashi, T. Takizawa, and Y. Nakanishi. 1995. Transcription stimulation of the Fas-encoding gene by nuclear factor for interleukin-6 expression upon influenza virus infection. J. Biol. Chem. 270:18007-18012.
46. Wegner, M., Z. Cao, and M. G. Rosenfeld. 1992. Calcium-regulated phosphorylation within the leucine zipper of C/EBP beta. Science 256:370-373.
47. Williams, S. C., M. Baer, A. J. Dillner, and P. F. Johnson. 1995. CRP2 (C/EBPβ) contains a bipartite regulatory domain that controls transcriptional activation, DNA binding and cell specificity. EMBO J. 14:3170-3183.
48. Zhao, X., S. Zhuang, Y. Chen, G. R. Boss, and R. B. Pilz. 2005. Cyclic GMP-dependent protein kinase regulates CCAAT enhancer-binding protein beta functions through inhibition of glycogen synthase kinase-3. J. Biol. Chem. 280:32683-32692.
49. Zhu, S., H. S. Oh, M. Shim, E. Sterneck, P. F. Johnson, and R. C. Smart. 1999. C/EBPbeta modulates the early events of keratinocyte differentiation involving growth arrest and keratin 1 and keratin 10 expression. Mol. Cell. Biol. 19:7181-7190.
50. Zhu, S., K. Yoon, E. Sterneck, P. F. Johnson, and R. C. Smart. 2002. CCAAT/enhancer binding protein-beta is a mediator of keratinocyte survival and skin tumorigenesis involving oncogenic Ras signaling. Proc. Natl. Acad. Sci. U. S. A. 99:207-212.